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G-protein Coupled Receptors in Stem Cell Self-Renewal and Differentiation

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Abstract

Stem cells have great potential for understanding early development, treating human disease, tissue trauma and early phase drug discovery. The factors that control the regulation of stem cell survival, proliferation, migration and differentiation are still emerging. Some evidence now exists demonstrating the potent effects of various G-protein coupled receptor (GPCR) ligands on the biology of stem cells. This review aims to give an overview of the current knowledge of the regulation of embryonic and somatic stem cell maintenance and differentiation by GPCR ligands.

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Abbreviations

2-AG:

2-Arachidonoylglycerol

AEA:

Anandamide

ATX:

Autotaxin

CNS:

Central nervous system

CM:

Cardiomyocyte

DAGL:

Diacylglycerol lipase

GDP:

Guanosine diphosphate

GEF:

Guanine nucleotide exchange factors

GTP:

Guanosine triphosphate

GPCR:

G-protein coupled receptor

G-CSF:

Granulocyte colony-stimulating factor

ERK:

Extracellular signal-regulated kinase

ET:

Endothelin

FAAH:

Fatty acid amide hydrolase

hESC:

Human embryonic stem cell

iPSC:

Induced pluripotent stem cell

LPA:

Lysophosphatidic acid

MAGL:

Monoacylglycerol lipase

MAP:

Mitogen-activated protein

MEF:

Mouse embryonic fibroblast

MSC:

Mesenchymal/stromal stem cell

NADA:

N-arachidonoyl-dopamine

NAPE-PLD:

N-acyl-phosphatidylethanolamine-specific phospholipase D

NCC:

Neural crest cells

NS/PC:

Neural stem/progenitor cells

OPC:

Oligodendrocyte progenitor cells

PDGF:

Platelet-derived growth factor

PI3K:

Phosphoinositide 3-kinase

PTX:

Pertussis toxin

S1P:

Sphingosine-1-phosphate

SDF-1:

Stromal-derived factor

SK:

Sphingosine kinase

SVZ:

Subventricular zone

References

  1. Melton, D., & Cowan, C. (2004). ‘Stemness’: Definitions, criteria and standards. In R. Lanza, J. Gearhart, B. Hogan, D. Melton, R. Pedersen, J. Thomson & M. West (Eds), Handbook of stem cells. Elsevier.

  2. Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., et al. (1998). Embryonic stem cell lines derived from human blastocysts. Science, 282, 1145–1147.

    Article  CAS  PubMed  Google Scholar 

  3. Reubinoff, B. E., Pera, M. F., Fong, C. Y., Trounson, A., & Bongso, A. (2000). Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nature Biotechnology, 18, 399–404.

    Article  CAS  PubMed  Google Scholar 

  4. Evans, M. J., & Kaufman, M. H. (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature, 292, 154–156.

    Article  CAS  PubMed  Google Scholar 

  5. Martin, G. R. (1981). Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proceedings of the National Academy of Sciences of the United States of America, 78, 7634–7638.

    Article  CAS  PubMed  Google Scholar 

  6. Verfaillie, C. M., Pera, M. F., & Lansdorp, P. M. (2002). Stem cells: hype and reality. Hematology American Society of Hematology Education Program, 369−391.

  7. Kristiansen, K. (2004). Molecular mechanisms of ligand binding, signaling, and regulation within the superfamily of G-protein-coupled receptors: molecular modeling and mutagenesis approaches to receptor structure and function. Pharmacology & Therapeutics, 103, 21–80.

    Article  CAS  Google Scholar 

  8. Cotton, M., & Claing, A. (2009). G protein-coupled receptors stimulation and the control of cell migration. Cellular Signalling, 21, 1045–1053.

    Article  CAS  PubMed  Google Scholar 

  9. Malbon, C. C. (2005). G proteins in development. Nature Reviews. Molecular Cell Biology, 6, 689–701.

    Article  CAS  PubMed  Google Scholar 

  10. Wettschureck, N., & Offermanns, S. (2005). Mammalian G proteins and their cell type specific functions. Physiological Reviews, 85, 1159–1204.

    Article  CAS  PubMed  Google Scholar 

  11. Nakamura, K., Salomonis, N., Tomoda, K., Yamanaka, S., & Conklin, B. R. (2009). G(i)-coupled GPCR signaling controls the formation and organization of human pluripotent colonies. PLoS ONE, 4, e7780.

    Article  PubMed  CAS  Google Scholar 

  12. Pebay, A., Wong, R. C., Pitson, S. M., et al. (2005). Essential roles of sphingosine-1-phosphate and platelet-derived growth factor in the maintenance of human embryonic stem cells. Stem Cells, 23, 1541–1548.

    Article  CAS  PubMed  Google Scholar 

  13. Papayannopoulou, T., Priestley, G. V., Bonig, H., & Nakamoto, B. (2003). The role of G-protein signaling in hematopoietic stem/progenitor cell mobilization. Blood, 101, 4739–4747.

    Article  CAS  PubMed  Google Scholar 

  14. Layden, B. T., Newman, M., Chen, F., Fisher, A., & Lowe, W. L., Jr. (2010). G protein coupled receptors in embryonic stem cells: a role for Gs-alpha signaling. PLoS ONE, 5, e9105.

    Article  PubMed  CAS  Google Scholar 

  15. Tikhonova, I. G., & Costanzi, S. (2009). Unraveling the structure and function of G protein-coupled receptors through NMR spectroscopy. Current Pharmaceutical Design, 15, 4003–4016.

    Article  CAS  PubMed  Google Scholar 

  16. Ritter, S. L., & Hall, R. A. (2009). Fine-tuning of GPCR activity by receptor-interacting proteins. Nature Reviews. Molecular Cell Biology, 10, 819–830.

    Article  CAS  PubMed  Google Scholar 

  17. Rosenbaum, D. M., Rasmussen, S. G., & Kobilka, B. K. (2009). The structure and function of G-protein-coupled receptors. Nature, 459, 356–363.

    Article  CAS  PubMed  Google Scholar 

  18. Harmar, A. J., Hills, R. A., Rosser, E. M., et al. (2009). IUPHAR-DB: the IUPHAR database of G protein-coupled receptors and ion channels. Nucleic Acids Research, 37, D680–D685.

    Article  CAS  PubMed  Google Scholar 

  19. Wennerberg, K., Rossman, K. L., & Der, C. J. (2005). The Ras superfamily at a glance. Journal of Cell Science, 118, 843–846.

    Article  CAS  PubMed  Google Scholar 

  20. Horuk, R. (2001). Chemokine receptors. Cytokine & Growth Factor Reviews, 12, 313–335.

    Article  CAS  Google Scholar 

  21. Kucia, M., Jankowski, K., Reca, R., et al. (2004). CXCR4-SDF-1 signalling, locomotion, chemotaxis and adhesion. Journal of Molecular Histology, 35, 233–245.

    Article  CAS  PubMed  Google Scholar 

  22. Schier, A. F. (2003). Chemokine signaling: rules of attraction. Current Biology, 13, R192–R194.

    Article  CAS  PubMed  Google Scholar 

  23. van Amerongen, R., & Nusse, R. (2009). Towards an integrated view of Wnt signaling in development. Development, 136, 3205–3214.

    Article  PubMed  CAS  Google Scholar 

  24. Nusse, R. (2008). Wnt signaling and stem cell control. Cell Research, 18, 523–527.

    Article  CAS  PubMed  Google Scholar 

  25. Faherty, S., Fitzgerald, A., Keohan, M., & Quinlan, L. R. (2007). Self-renewal and differentiation of mouse embryonic stem cells as measured by Oct4 expression: the role of the cAMP/PKA pathway. In Vitro Cellular & Developmental Biology. Animal, 43, 37–47.

    Article  CAS  Google Scholar 

  26. Rodgers, A., Mormeneo, D., Long, J. S., Delgado, A., Pyne, N. J., & Pyne, S. (2009). Sphingosine 1-phosphate regulation of extracellular signal-regulated kinase-1/2 in embryonic stem cells. Stem Cells and Development, 18, 1319–1330.

    Article  CAS  PubMed  Google Scholar 

  27. Todorova, M. G., Fuentes, E., Soria, B., Nadal, A., & Quesada, I. (2009). Lysophosphatidic acid induces Ca2+ mobilization and c-Myc expression in mouse embryonic stem cells via the phospholipase C pathway. Cellular Signalling, 21, 523–528.

    Article  CAS  PubMed  Google Scholar 

  28. Kleger, A., Busch, T., Liebau, S., et al. (2007). The bioactive lipid sphingosylphosphorylcholine induces differentiation of mouse embryonic stem cells and human promyelocytic leukaemia cells. Cellular Signalling, 19, 367–377.

    Article  CAS  PubMed  Google Scholar 

  29. Inniss, K., & Moore, H. (2006). Mediation of apoptosis and proliferation of human embryonic stem cells by sphingosine-1-phosphate. Stem Cells and Development, 15, 789–796.

    Article  CAS  PubMed  Google Scholar 

  30. Dottori, M., Leung, J., Turnley, A. M., & Pebay, A. (2008). Lysophosphatidic acid inhibits neuronal differentiation of neural stem/progenitor cells derived from human embryonic stem cells. Stem Cells, 26, 1146–1154.

    Article  CAS  PubMed  Google Scholar 

  31. Schuck, S., Soloaga, A., Schratt, G., Arthur, J. S., & Nordheim, A. (2003). The kinase MSK1 is required for induction of c-fos by lysophosphatidic acid in mouse embryonic stem cells. BMC Molecular Biology, 4, 6.

    Article  PubMed  Google Scholar 

  32. Burdon, T., Stracey, C., Chambers, I., Nichols, J., & Smith, A. (1999). Suppression of SHP-2 and ERK signalling promotes self-renewal of mouse embryonic stem cells. Developmental Biology, 210, 30–43.

    Article  CAS  PubMed  Google Scholar 

  33. Burdon, T., Smith, A., & Savatier, P. (2002). Signalling, cell cycle and pluripotency in embryonic stem cells. Trends in Cell Biology, 12, 432–438.

    Article  CAS  PubMed  Google Scholar 

  34. Takahashi, K., & Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126, 663–676.

    Article  CAS  PubMed  Google Scholar 

  35. Takahashi, K., Tanabe, K., Ohnuki, M., et al. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 131, 861–872.

    Article  CAS  PubMed  Google Scholar 

  36. Avery, K., Avery, S., Shepherd, J., Heath, P. R., & Moore, H. (2008). Sphingosine-1-phosphate mediates transcriptional regulation of key targets associated with survival, proliferation, and pluripotency in human embryonic stem cells. Stem Cells and Development, 17, 1195–1205.

    Article  CAS  PubMed  Google Scholar 

  37. Wong, R. C., Tellis, I., Jamshidi, P., Pera, M., & Pebay, A. (2007). Anti-apoptotic effect of sphingosine-1-phosphate and platelet-derived growth factor in human embryonic stem cells. Stem Cells and Development, 16, 989–1001.

    Article  CAS  PubMed  Google Scholar 

  38. Piomelli, D. (2005). The endocannabinoid system: a drug discovery perspective. Current Opinion in Investigational Drugs, 6, 672–679.

    CAS  PubMed  Google Scholar 

  39. Piomelli, D. (2003). The molecular logic of endocannabinoid signalling. Nature Reviews. Neuroscience, 4, 873–884.

    Article  CAS  PubMed  Google Scholar 

  40. Demuth, D. G., & Molleman, A. (2006). Cannabinoid signalling. Life Sciences, 78, 549–563.

    Article  CAS  PubMed  Google Scholar 

  41. Jiang, S., Fu, Y., Williams, J., et al. (2007). Expression and function of cannabinoid receptors CB1 and CB2 and their cognate cannabinoid ligands in murine embryonic stem cells. PLoS ONE, 2, e641.

    Article  PubMed  CAS  Google Scholar 

  42. Bari, M., Tedesco, M., Battista, N., et al. (2010). Characterization of the endocannabinoid system in mouse embryonic stem cells. Stem Cells Development, doi:10.1089/scd.2009.0515.

  43. Ross, R. A. (2003). Anandamide and vanilloid TRPV1 receptors. British Journal of Pharmacology, 140, 790–801.

    Article  CAS  PubMed  Google Scholar 

  44. Southgate, T. D., McGinn, O. J., Castro, F. V., et al. (2010). CXCR4 mediated chemotaxis is regulated by 5T4 oncofetal glycoprotein in mouse embryonic cells. PLoS ONE, 5, e9982.

    Article  PubMed  CAS  Google Scholar 

  45. Walsh, J., & Andrews, P. W. (2003). Expression of Wnt and Notch pathway genes in a pluripotent human embryonal carcinoma cell line and embryonic stem cell. Apmis, 111, 197–210. discussion -1.

    Article  CAS  PubMed  Google Scholar 

  46. Rho, J. Y., Yu, K., Han, J. S., et al. (2006). Transcriptional profiling of the developmentally important signalling pathways in human embryonic stem cells. Human Reproduction, 21, 405–412.

    Article  CAS  PubMed  Google Scholar 

  47. Brandenberger, R., Wei, H., Zhang, S., et al. (2004). Transcriptome characterization elucidates signaling networks that control human ES cell growth and differentiation. Nature Biotechnology, 22, 707–716.

    Article  PubMed  Google Scholar 

  48. Davidson, K. C., Jamshidi, P., Daly, R., Hearn, M. T., Pera, M. F., & Dottori, M. (2007). Wnt3a regulates survival, expansion, and maintenance of neural progenitors derived from human embryonic stem cells. Molecular and Cellular Neurosciences, 36, 408–415.

    Article  CAS  PubMed  Google Scholar 

  49. Dravid, G., Ye, Z., Hammond, H., et al. (2005). Defining the role of Wnt/{beta}-catenin signaling in the survival, proliferation, and self-renewal of human embryonic stem cells. Stem Cells, 23, 1489–1501.

    Article  CAS  PubMed  Google Scholar 

  50. Sato, N., Meijer, L., Skaltsounis, L., Greengard, P., & Brivanlou, A. H. (2004). Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Natural Medicines, 10, 55–63.

    Article  CAS  Google Scholar 

  51. Cheon, S. H., Kim, S. J., Jo, J. Y., Ryu, W. J., Rhee, K., & Roh, S. I. (2006). Defined feeder-free culture system of human embryonic stem cells. Biology of Reproduction, 74, 611–618.

    CAS  Google Scholar 

  52. Hasegawa, K., Fujioka, T., Nakamura, Y., Nakatsuji, N., & Suemori, H. (2006). A method for the selection of human embryonic stem cell sub-lines with high replating efficiency after single cell dissociation. Stem Cells, 24, 2649–2660.

    Article  CAS  PubMed  Google Scholar 

  53. James, D., Levine, A. J., Besser, D., & Hemmati-Brivanlou, A. (2005). TGFbeta/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development, 132, 1273–1282.

    Article  CAS  PubMed  Google Scholar 

  54. Melchior, K., Weiss, J., Zaehres, H., et al. (2008). The WNT receptor FZD7 contributes to self-renewal signaling of human embryonic stem cells. Biological Chemistry, 389, 897–903.

    Article  CAS  PubMed  Google Scholar 

  55. Alexander, S. P. H. (2009). 7TM receptors. British Journal of Pharmacology, 158, s5–s101.

    Article  Google Scholar 

  56. Laslett, A. L., Grimmond, S., Gardiner, B., et al. (2007). Transcriptional analysis of early lineage commitment in human embryonic stem cells. BMC Developmental Biology, 7, 12.

    Article  PubMed  CAS  Google Scholar 

  57. Wong, R. C., Davidson, K. C., Leung, J., Pera, M. F., & Pebay, A. (2009). Acute effect of endothelins on intracellular communication of human embryonic stem cells. Journal of Stem Cells, 4, 47–55.

    PubMed  Google Scholar 

  58. Sautin, Y. Y., Jorgensen, M., Petersen, B. E., Saulnier-Blache, J. S., Crawford, J. M., & Svetlov, S. I. (2002). Hepatic oval (stem) cell expression of endothelial differentiation gene receptors for lysophosphatidic acid in mouse chronic liver injury. Journal of Hematotherapy & Stem Cell Research, 11, 643–649.

    Article  Google Scholar 

  59. Friedman, S. L. (2008). Mechanisms of hepatic fibrogenesis. Gastroenterology, 134, 1655–1669.

    Article  CAS  PubMed  Google Scholar 

  60. Ikeda, H., Watanabe, N., Ishii, I., et al. (2009). Sphingosine 1-phosphate regulates regeneration and fibrosis after liver injury via sphingosine 1-phosphate receptor 2. Journal of Lipid Research, 50, 556–564.

    Article  CAS  PubMed  Google Scholar 

  61. Li, C., Kong, Y., Wang, H., et al. (2009). Homing of bone marrow mesenchymal stem cells mediated by sphingosine 1-phosphate contributes to liver fibrosis. Journal of Hepatology, 50, 1174–1183.

    Article  CAS  PubMed  Google Scholar 

  62. Kushner, J. A., Weir, G. C., & Bonner-Weir, S. (2010). Ductal origin hypothesis of pancreatic regeneration under attack. Cell Metabolism, 11, 2–3.

    Article  CAS  PubMed  Google Scholar 

  63. Regard, J. B., Kataoka, H., Cano, D. A., et al. (2007). Probing cell type-specific functions of Gi in vivo identifies GPCR regulators of insulin secretion. Journal of Clinical Investigation, 117, 4034–4043.

    CAS  PubMed  Google Scholar 

  64. Imasawa, T., Koike, K., Ishii, I., Chun, J., & Yatomi, Y. (2010). Blockade of sphingosine 1-phosphate receptor 2 signaling attenuates streptozotocin-induced apoptosis of pancreatic beta-cells. Biochemical and Biophysical Research Communications, 392, 207–211.

    Article  CAS  PubMed  Google Scholar 

  65. Mizoguchi, T., Verkade, H., Heath, J. K., Kuroiwa, A., & Kikuchi, Y. (2008). Sdf1/Cxcr4 signaling controls the dorsal migration of endodermal cells during zebrafish gastrulation. Development, 135, 2521–2529.

    Article  CAS  PubMed  Google Scholar 

  66. Fukui, A., Goto, T., Kitamoto, J., Homma, M., & Asashima, M. (2007). SDF-1 alpha regulates mesendodermal cell migration during frog gastrulation. Biochemical and Biophysical Research Communications, 354, 472–477.

    Article  CAS  PubMed  Google Scholar 

  67. McGrath, K. E., Koniski, A. D., Maltby, K. M., McGann, J. K., & Palis, J. (1999). Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Developmental Biology, 213, 442–456.

    Article  CAS  PubMed  Google Scholar 

  68. Yasunaga, M., Tada, S., Torikai-Nishikawa, S., et al. (2005). Induction and monitoring of definitive and visceral endoderm differentiation of mouse ES cells. Nature Biotechnology, 23, 1542–1550.

    Article  CAS  PubMed  Google Scholar 

  69. D’Amour, K. A., Agulnick, A. D., Eliazer, S., Kelly, O. G., Kroon, E., & Baetge, E. E. (2005). Efficient differentiation of human embryonic stem cells to definitive endoderm. Nature Biotechnology, 23, 1534–1541.

    Article  PubMed  CAS  Google Scholar 

  70. Hou, J., Charters, A. M., Lee, S. C., et al. (2007). A systematic screen for genes expressed in definitive endoderm by Serial Analysis of Gene Expression (SAGE). BMC Developmental Biology, 7, 92.

    Article  PubMed  CAS  Google Scholar 

  71. Hick, A. C., van Eyll, J. M., Cordi, S., et al. (2009). Mechanism of primitive duct formation in the pancreas and submandibular glands: a role for SDF-1. BMC Developmental Biology, 9, 66.

    Article  PubMed  CAS  Google Scholar 

  72. Grapin-Botton, A., & Constam, D. (2007). Evolution of the mechanisms and molecular control of endoderm formation. Mechanisms of Development, 124, 253–278.

    Article  CAS  PubMed  Google Scholar 

  73. Liu, P., Wakamiya, M., Shea, M. J., Albrecht, U., Behringer, R. R., & Bradley, A. (1999). Requirement for Wnt3 in vertebrate axis formation. Nature Genetics, 22, 361–365.

    Article  CAS  PubMed  Google Scholar 

  74. McLin, V. A., Rankin, S. A., & Zorn, A. M. (2007). Repression of Wnt/beta-catenin signaling in the anterior endoderm is essential for liver and pancreas development. Development, 134, 2207–2217.

    Article  CAS  PubMed  Google Scholar 

  75. Zaret, K. S., & Grompe, M. (2008). Generation and regeneration of cells of the liver and pancreas. Science, 322, 1490–1494.

    Article  CAS  PubMed  Google Scholar 

  76. Ober, E. A., Verkade, H., Field, H. A., & Stainier, D. Y. (2006). Mesodermal Wnt2b signalling positively regulates liver specification. Nature, 442, 688–691.

    Article  CAS  PubMed  Google Scholar 

  77. Tan, X., Behari, J., Cieply, B., Michalopoulos, G. K., & Monga, S. P. (2006). Conditional deletion of beta-catenin reveals its role in liver growth and regeneration. Gastroenterology, 131, 1561–1572.

    Article  CAS  PubMed  Google Scholar 

  78. Hussain, S. Z., Sneddon, T., Tan, X., Micsenyi, A., Michalopoulos, G. K., & Monga, S. P. (2004). Wnt impacts growth and differentiation in ex vivo liver development. Experimental Cell Research, 292, 157–169.

    Article  CAS  PubMed  Google Scholar 

  79. Kroon, E., Martinson, L. A., Kadoya, K., et al. (2008). Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nature Biotechnology, 26, 443–452.

    Article  CAS  PubMed  Google Scholar 

  80. Cho, Y. M., Lim, J. M., Yoo, D. H., et al. (2008). Betacellulin and nicotinamide sustain PDX1 expression and induce pancreatic beta-cell differentiation in human embryonic stem cells. Biochemical and Biophysical Research Communications, 366, 129–134.

    Article  CAS  PubMed  Google Scholar 

  81. Korinek, V., Barker, N., Moerer, P., et al. (1998). Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nature Genetics, 19, 379–383.

    Article  CAS  PubMed  Google Scholar 

  82. Barker, N., van Es, J. H., Kuipers, J., et al. (2007). Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature, 449, 1003–1007.

    Article  CAS  PubMed  Google Scholar 

  83. Barker, N., Huch, M., Kujala, P., et al. (2010). Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell, 6, 25–36.

    Article  CAS  PubMed  Google Scholar 

  84. Whetton, A. D., Lu, Y., Pierce, A., Carney, L., & Spooncer, E. (2003). Lysophospholipids synergistically promote primitive hematopoietic cell chemotaxis via a mechanism involving Vav 1. Blood, 102, 2798–2802.

    Article  CAS  PubMed  Google Scholar 

  85. Yanai, N., Matsui, N., Furusawa, T., Okubo, T., & Obinata, M. (2000). Sphingosine-1-phosphate and lysophosphatidic acid trigger invasion of primitive hematopoietic cells into stromal cell layers. Blood, 96, 139–144.

    CAS  PubMed  Google Scholar 

  86. Pebay, A., Bonder, C. S., & Pitson, S. M. (2007). Stem cell regulation by lysophospholipids. Prostaglandins & Other Lipid Mediators, 84, 83–97.

    Article  CAS  Google Scholar 

  87. Lai, J. M., Lu, C. Y., Yang-Yen, H. F., & Chang, Z. F. (2001). Lysophosphatidic acid promotes phorbol-ester-induced apoptosis in TF-1 cells by interfering with adhesion. The Biochemical Journal, 359, 227–233.

    Article  CAS  PubMed  Google Scholar 

  88. Kimura, T., Boehmler, A. M., Seitz, G., et al. (2004). The sphingosine 1-phosphate receptor agonist FTY720 supports CXCR4-dependent migration and bone marrow homing of human CD34+ progenitor cells. Blood, 103, 4478–4486.

    Article  CAS  PubMed  Google Scholar 

  89. Seitz, G., Boehmler, A. M., Kanz, L., & Mohle, R. (2005). The role of sphingosine 1-phosphate receptors in the trafficking of hematopoietic progenitor cells. Annals of the New York Academy of Sciences, 1044, 84–89.

    Article  CAS  PubMed  Google Scholar 

  90. Jaganathan, B. G., Ruester, B., Dressel, L., et al. (2007). Rho inhibition induces migration of mesenchymal stromal cells (MSCs). Stem Cells, 25, 1966–1974.

    Article  CAS  PubMed  Google Scholar 

  91. Annabi, B., Thibeault, S., Lee, Y. T., et al. (2003). Matrix metalloproteinase regulation of sphingosine-1-phosphate-induced angiogenic properties of bone marrow stromal cells. Experimental Hematology, 31, 640–649.

    Article  CAS  PubMed  Google Scholar 

  92. Meriane, M., Duhamel, S., Lejeune, L., Galipeau, J., & Annabi, B. (2006). Cooperation of matrix metalloproteinases with the RhoA/Rho kinase and mitogen-activated protein kinase kinase-1/extracellular signal-regulated kinase signaling pathways is required for the sphingosine-1-phosphate-induced mobilization of marrow-derived stromal cells. Stem Cells, 24, 2557–2565.

    Article  CAS  PubMed  Google Scholar 

  93. Nincheri, P., Luciani, P., Squecco, R., et al. (2009). Sphingosine 1-phosphate induces differentiation of adipose tissue-derived mesenchymal stem cells towards smooth muscle cells. Cellular and Molecular Life Sciences, 66, 1741–1754.

    Article  CAS  PubMed  Google Scholar 

  94. Chen, J., Baydoun, A. R., Xu, R., et al. (2008). Lysophosphatidic acid protects mesenchymal stem cells against hypoxia and serum deprivation-induced apoptosis. Stem Cells, 26, 135–145.

    Article  CAS  PubMed  Google Scholar 

  95. Dupuis, F., Desplat, V., Praloran, V., & Denizot, Y. (1997). Effects of lipidic mediators on the growth of human myeloid and erythroid marrow progenitors. Journal of Lipid Mediators and Cell Signalling, 16, 117–125.

    Article  CAS  PubMed  Google Scholar 

  96. Lord, A. M., North, T. E., & Zon, L. I. (2007). Prostaglandin E2: making more of your marrow. Cell Cycle, 6, 3054–3057.

    Article  CAS  PubMed  Google Scholar 

  97. Weinreb, M., Shamir, D., Machwate, M., Rodan, G. A., Harada, S., & Keila, S. (2006). Prostaglandin E2 (PGE2) increases the number of rat bone marrow osteogenic stromal cells (BMSC) via binding the EP4 receptor, activating sphingosine kinase and inhibiting caspase activity. Prostaglandins Leukotrienes and Essential Fatty Acids, 75, 81–90.

    Article  CAS  Google Scholar 

  98. Donati, C., Meacci, E., Nuti, F., Becciolini, L., Farnararo, M., & Bruni, P. (2005). Sphingosine 1-phosphate regulates myogenic differentiation: a major role for S1P2 receptor. The FASEB Journal, 19, 449–451.

    CAS  PubMed  Google Scholar 

  99. Meacci, E., Nuti, F., Donati, C., Cencetti, F., Farnararo, M., & Bruni, P. (2008). Sphingosine kinase activity is required for myogenic differentiation of C2C12 myoblasts. Journal of Cellular Physiology, 214, 210–220.

    Article  CAS  PubMed  Google Scholar 

  100. Rapizzi, E., Donati, C., Cencetti, F., Nincheri, P., & Bruni, P. (2008). Sphingosine 1-phosphate differentially regulates proliferation of C2C12 reserve cells and myoblasts. Molecular and Cellular Biochemistry, 314, 193–199.

    Article  CAS  PubMed  Google Scholar 

  101. Becciolini, L., Meacci, E., Donati, C., Cencetti, F., Rapizzi, E., & Bruni, P. (2006). Sphingosine 1-phosphate inhibits cell migration in C2C12 myoblasts. Biochimica et Biophysica Acta, 1761, 43–51.

    CAS  PubMed  Google Scholar 

  102. Nagata, Y., Partridge, T. A., Matsuda, R., & Zammit, P. S. (2006). Entry of muscle satellite cells into the cell cycle requires sphingolipid signaling. The Journal of Cell Biology, 174, 245–253.

    Article  CAS  PubMed  Google Scholar 

  103. Yoshida, S., Fujisawa-Sehara, A., Taki, T., Arai, K., & Nabeshima, Y. (1996). Lysophosphatidic acid and bFGF control different modes in proliferating myoblasts. The Journal of Cell Biology, 132, 181–193.

    Article  CAS  PubMed  Google Scholar 

  104. Jean-Baptiste, G., Yang, Z., Khoury, C., & Greenwood, M. T. (2005). Lysophosphatidic acid mediates pleiotropic responses in skeletal muscle cells. Biochemical and Biophysical Research Communications, 335, 1155–1162.

    Article  CAS  PubMed  Google Scholar 

  105. Meacci, E., Vasta, V., Donati, C., Farnararo, M., & Bruni, P. (1999). Receptor-mediated activation of phospholipase D by sphingosine 1-phosphate in skeletal muscle C2C12 cells. A role for protein kinase C. FEBS Letters, 457, 184–188.

    Article  CAS  PubMed  Google Scholar 

  106. Meacci, E., Becciolini, L., Nuti, F., et al. (2002). A role for calcium in sphingosine 1-phosphate-induced phospholipase D activity in C2C12 myoblasts. FEBS Letters, 521, 200–204.

    Article  CAS  PubMed  Google Scholar 

  107. Meacci, E., Cencetti, F., Donati, C., et al. (2003). Down-regulation of EDG5/S1P2 during myogenic differentiation results in the specific uncoupling of sphingosine 1-phosphate signalling to phospholipase D. Biochimica et Biophysica Acta, 1633, 133–142.

    CAS  PubMed  Google Scholar 

  108. Donati, C., Cencetti, F., Nincheri, P., et al. (2007). Sphingosine 1-phosphate mediates proliferation and survival of mesoangioblasts. Stem Cells, 25, 1713–1719.

    Article  CAS  PubMed  Google Scholar 

  109. Caverzasio, J., Palmer, G., Suzuki, A., & Bonjour, J. P. (2000). Evidence for the involvement of two pathways in activation of extracellular signal-regulated kinase (Erk) and cell proliferation by Gi and Gq protein-coupled receptors in osteoblast-like cells. Journal of Bone and Mineral Research, 15, 1697–1706.

    Article  CAS  PubMed  Google Scholar 

  110. Ishii, M., Egen, J. G., Klauschen, F., et al. (2009). Sphingosine-1-phosphate mobilizes osteoclast precursors and regulates bone homeostasis. Nature, 458, 524–528.

    Article  CAS  PubMed  Google Scholar 

  111. Aronin, C. E., Sefcik, L. S., Tholpady, S. S., et al. (2010). FTY720 promotes local microvascular network formation and regeneration of cranial bone defects. Tissue Engineering. Part A, 16, 1801–1809.

    Article  CAS  Google Scholar 

  112. Ryu, J., Kim, H. J., Chang, E. J., Huang, H., Banno, Y., & Kim, H. H. (2006). Sphingosine 1-phosphate as a regulator of osteoclast differentiation and osteoclast-osteoblast coupling. The EMBO Journal, 25, 5840–5851.

    Article  CAS  PubMed  Google Scholar 

  113. Pederson, L., Ruan, M., Westendorf, J. J., Khosla, S., & Oursler, M. J. (2008). Regulation of bone formation by osteoclasts involves Wnt/BMP signaling and the chemokine sphingosine-1-phosphate. Proceedings of the National Academy of Sciences of the United States of America, 105, 20764–20769.

    Article  CAS  PubMed  Google Scholar 

  114. Roelofsen, T., Akkers, R., Beumer, W., et al. (2008). Sphingosine-1-phosphate acts as a developmental stage specific inhibitor of platelet-derived growth factor-induced chemotaxis of osteoblasts. Journal of Cellular Biochemistry, 105, 1128–1138.

    Article  CAS  PubMed  Google Scholar 

  115. Karagiosis, S. A., Chrisler, W. B., Bollinger, N., & Karin, N. J. (2009). Lysophosphatidic acid-induced ERK activation and chemotaxis in MC3T3-E1 preosteoblasts are independent of EGF receptor transactivation. Journal of Cellular Physiology, 219, 716–723.

    Article  CAS  PubMed  Google Scholar 

  116. Liu, Y. B., Kharode, Y., Bodine, P. V., Yaworsky, P. J., Robinson, J. A., & Billiard, J. (2010). LPA induces osteoblast differentiation through interplay of two receptors: LPA1 and LPA4. Journal of Cellular Biochemistry, 109, 794–800.

    CAS  PubMed  Google Scholar 

  117. Ma, Q., Jones, D., & Springer, T. A. (1999). The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity, 10, 463–471.

    Article  CAS  PubMed  Google Scholar 

  118. Lapidot, T., & Petit, I. (2002). Current understanding of stem cell mobilization: the roles of chemokines, proteolytic enzymes, adhesion molecules, cytokines, and stromal cells. Experimental Hematology, 30, 973–981.

    Article  CAS  PubMed  Google Scholar 

  119. Mohle, R., Bautz, F., Rafii, S., Moore, M. A., Brugger, W., & Kanz, L. (1998). The chemokine receptor CXCR-4 is expressed on CD34+ hematopoietic progenitors and leukemic cells and mediates transendothelial migration induced by stromal cell-derived factor-1. Blood, 91, 4523–4530.

    CAS  PubMed  Google Scholar 

  120. Petit, I., Szyper-Kravitz, M., Nagler, A., et al. (2002). G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nature Immunology, 3, 687–694.

    Article  CAS  PubMed  Google Scholar 

  121. Aiuti, A., Turchetto, L., Cota, M., et al. (1999). Human CD34(+) cells express CXCR4 and its ligand stromal cell-derived factor-1. Implications for infection by T-cell tropic human immunodeficiency virus. Blood, 94, 62–73.

    CAS  PubMed  Google Scholar 

  122. Bautz, F., Denzlinger, C., Kanz, L., & Mohle, R. (2001). Chemotaxis and transendothelial migration of CD34(+) hematopoietic progenitor cells induced by the inflammatory mediator leukotriene D4 are mediated by the 7-transmembrane receptor CysLT1. Blood, 97, 3433–3440.

    Article  CAS  PubMed  Google Scholar 

  123. Xue, X., Cai, Z., Seitz, G., Kanz, L., Moehle, R., & Weisel, K. (2007). Differential effects of G protein-coupled receptors on hematopoietic progenitor cell growth depends on their signaling capacities. Annals of the New York Academy of Sciences, 1106, 180–189.

    Article  CAS  PubMed  Google Scholar 

  124. Dutt, P., Wang, J. F., & Groopman, J. E. (1998). Stromal cell-derived factor-1 alpha and stem cell factor/kit ligand share signaling pathways in hemopoietic progenitors: a potential mechanism for cooperative induction of chemotaxis. Journal of Immunology, 161, 3652–3658.

    CAS  Google Scholar 

  125. Walter, D. H., Rochwalsky, U., Reinhold, J., et al. (2007). Sphingosine-1-phosphate stimulates the functional capacity of progenitor cells by activation of the CXCR4-dependent signaling pathway via the S1P3 receptor. Arteriosclerosis, Thrombosis, and Vascular Biology, 27, 275–282.

    Article  CAS  PubMed  Google Scholar 

  126. Ratajczak, M. Z., Lee, H., Wysoczynski, M., et al. (2010). Novel insight into stem cell mobilization-Plasma sphingosine-1-phosphate is a major chemoattractant that directs the egress of hematopoietic stem progenitor cells from the bone marrow and its level in peripheral blood increases during mobilization due to activation of complement cascade/membrane attack complex. Leukemia, 24, 976–985.

    Article  CAS  PubMed  Google Scholar 

  127. Ratajczak, M. Z., Majka, M., Kucia, M., et al. (2003). Expression of functional CXCR4 by muscle satellite cells and secretion of SDF-1 by muscle-derived fibroblasts is associated with the presence of both muscle progenitors in bone marrow and hematopoietic stem/progenitor cells in muscles. Stem Cells, 21, 363–371.

    Article  CAS  PubMed  Google Scholar 

  128. Zhu, W., Boachie-Adjei, O., Rawlins, B. A., et al. (2007). A novel regulatory role for stromal-derived factor-1 signaling in bone morphogenic protein-2 osteogenic differentiation of mesenchymal C2C12 cells. The Journal of Biological Chemistry, 282, 18676–18685.

    Article  CAS  PubMed  Google Scholar 

  129. Reya, T., & Clevers, H. (2005). Wnt signalling in stem cells and cancer. Nature, 434, 843–850.

    Article  CAS  PubMed  Google Scholar 

  130. Davis, L. A. (2008). Zur Nieden NI. Mesodermal fate decisions of a stem cell: the Wnt switch. Cellular and Molecular Life Sciences, 65, 2658–2674.

    Article  CAS  PubMed  Google Scholar 

  131. Khosla, S., Westendorf, J. J., & Oursler, M. J. (2008). Building bone to reverse osteoporosis and repair fractures. Journal of Clinical Investigation, 118, 421–428.

    Article  CAS  PubMed  Google Scholar 

  132. Rochais, F., Mesbah, K., & Kelly, R. G. (2009). Signaling pathways controlling second heart field development. Circulation Research, 104, 933–942.

    Article  CAS  PubMed  Google Scholar 

  133. Conti, L., & Cattaneo, E. (2010). Neural stem cell systems: physiological players or in vitro entities? Nature Reviews. Neuroscience, 11, 176–187.

    CAS  PubMed  Google Scholar 

  134. Zhao, C., Deng, W., & Gage, F. H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell, 132, 645–660.

    Article  CAS  PubMed  Google Scholar 

  135. Pitson, S. M., & Pebay, A. (2009). Regulation of stem cell pluripotency and neural differentiation by lysophospholipids. Neurosignals, 17, 242–254.

    Article  CAS  PubMed  Google Scholar 

  136. Fotopoulou, S., Oikonomou, N., Grigorieva, E., et al. (2010). ATX expression and LPA signalling are vital for the development of the nervous system. Developmental Biology, 339, 451–464.

    Article  CAS  PubMed  Google Scholar 

  137. Mizugishi, K., Yamashita, T., Olivera, A., Miller, G. F., Spiegel, S., & Proia, R. L. (2005). Essential role for sphingosine kinases in neural and vascular development. Molecular and Cellular Biology, 25, 11113–11121.

    Article  CAS  PubMed  Google Scholar 

  138. Igarashi, N., Okada, T., Hayashi, S., Fujita, T., Jahangeer, S., & Nakamura, S. (2003). Sphingosine kinase 2 is a nuclear protein and inhibits DNA synthesis. The Journal of Biological Chemistry, 278, 46832–46839.

    Article  CAS  PubMed  Google Scholar 

  139. Hait, N. C., Allegood, J., Maceyka, M., et al. (2009). Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science, 325, 1254–1257.

    Article  CAS  PubMed  Google Scholar 

  140. Harkany, T., Guzman, M., Galve-Roperh, I., Berghuis, P., Devi, L. A., & Mackie, K. (2007). The emerging functions of endocannabinoid signaling during CNS development. Trends in Pharmacological Sciences, 28, 83–92.

    Article  CAS  PubMed  Google Scholar 

  141. Galve-Roperh, I., Palazuelos, J., Aguado, T., & Guzman, M. (2009). The endocannabinoid system and the regulation of neural development: potential implications in psychiatric disorders. European Archives of Psychiatry and Clinical Neuroscience, 259, 371–382.

    Article  PubMed  Google Scholar 

  142. Aguado, T., Monory, K., Palazuelos, J., et al. (2005). The endocannabinoid system drives neural progenitor proliferation. The FASEB Journal, 19, 1704–1706.

    CAS  PubMed  Google Scholar 

  143. Jiang, W., Zhang, Y., Xiao, L., et al. (2005). Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic- and antidepressant-like effects. Journal of Clinical Investigation, 115, 3104–3116.

    Article  CAS  PubMed  Google Scholar 

  144. Molina-Holgado, F., Rubio-Araiz, A., Garcia-Ovejero, D., et al. (2007). CB2 cannabinoid receptors promote mouse neural stem cell proliferation. The European Journal of Neuroscience, 25, 629–634.

    Article  PubMed  Google Scholar 

  145. Cravatt, B. F., Demarest, K., Patricelli, M. P., et al. (2001). Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proceedings of the National Academy of Sciences of the United States of America, 98, 9371–9376.

    Article  CAS  PubMed  Google Scholar 

  146. Jin, K., Xie, L., Kim, S. H., et al. (2004). Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice. Molecular Pharmacology, 66, 204–208.

    Article  CAS  PubMed  Google Scholar 

  147. Mulder, J., Aguado, T., Keimpema, E., et al. (2008). Endocannabinoid signaling controls pyramidal cell specification and long-range axon patterning. Proceedings of the National Academy of Sciences of the United States of America, 105, 8760–8765.

    Article  CAS  PubMed  Google Scholar 

  148. Berghuis, P., Dobszay, M. B., Wang, X., et al. (2005). Endocannabinoids regulate interneuron migration and morphogenesis by transactivating the TrkB receptor. Proceedings of the National Academy of Sciences of the United States of America, 102, 19115–19120.

    Article  CAS  PubMed  Google Scholar 

  149. Williams, E. J., Walsh, F. S., & Doherty, P. (2003). The FGF receptor uses the endocannabinoid signaling system to couple to an axonal growth response. The Journal of Cell Biology, 160, 481–486.

    Article  CAS  PubMed  Google Scholar 

  150. Kuwaki, T., Kurihara, H., Cao, W. H., et al. (1997). Physiological role of brain endothelin in the central autonomic control: from neuron to knockout mouse. Progress in Neurobiology, 51, 545–579.

    Article  CAS  PubMed  Google Scholar 

  151. Tsaur, M. L., Wan, Y. C., Lai, F. P., & Cheng, H. F. (1997). Expression of B-type endothelin receptor gene during neural development. FEBS Letters, 417, 208–212.

    Article  CAS  PubMed  Google Scholar 

  152. Nataf, V., Grapin-Botton, A., Champeval, D., Amemiya, A., Yanagisawa, M., & Le Douarin, N. M. (1998). The expression patterns of endothelin-A receptor and endothelin 1 in the avian embryo. Mechanisms of Development, 75, 145–149.

    Article  CAS  PubMed  Google Scholar 

  153. Nakagomi, S., Kiryu-Seo, S., & Kiyama, H. (2000). Endothelin-converting enzymes and endothelin receptor B messenger RNAs are expressed in different neural cell species and these messenger RNAs are coordinately induced in neurons and astrocytes respectively following nerve injury. Neuroscience, 101, 441–449.

    Article  CAS  PubMed  Google Scholar 

  154. Mizuno, N., Kokubu, H., Sato, M., et al. (2005). G protein-coupled receptor signaling through Gq and JNK negatively regulates neural progenitor cell migration. Proceedings of the National Academy of Sciences of the United States of America, 102, 12365–12370.

    Article  CAS  PubMed  Google Scholar 

  155. Bishop, A. L., & Hall, A. (2000). Rho GTPases and their effector proteins. The Biochemical Journal, 348(Pt 2), 241–255.

    Article  CAS  PubMed  Google Scholar 

  156. Konno, D., Yoshimura, S., Hori, K., Maruoka, H., & Sobue, K. (2005). Involvement of the phosphatidylinositol 3-kinase/rac1 and cdc42 pathways in radial migration of cortical neurons. The Journal of Biological Chemistry, 280, 5082–5088.

    Article  CAS  PubMed  Google Scholar 

  157. Ehrenreich, H., Oldenburg, J., Hasselblatt, M., et al. (1999). Endothelin B receptor-deficient rats as a subtraction model to study the cerebral endothelin system. Neuroscience, 91, 1067–1075.

    Article  CAS  PubMed  Google Scholar 

  158. Siren, A. L., Knerlich, F., Schilling, L., Kamrowski-Kruck, H., Hahn, A., & Ehrenreich, H. (2000). Differential glial and vascular expression of endothelins and their receptors in rat brain after neurotrauma. Neurochemical Research, 25, 957–969.

    Article  CAS  PubMed  Google Scholar 

  159. Ripodas, A., de Juan, J. A., Roldan-Pallares, M., et al. (2001). Localisation of endothelin-1 mRNA expression and immunoreactivity in the retina and optic nerve from human and porcine eye. Evidence for endothelin-1 expression in astrocytes. Brain Research, 912, 137–143.

    Article  CAS  PubMed  Google Scholar 

  160. Schinelli, S., Zanassi, P., Paolillo, M., Wang, H., Feliciello, A., & Gallo, V. (2001). Stimulation of endothelin B receptors in astrocytes induces cAMP response element-binding protein phosphorylation and c-fos expression via multiple mitogen-activated protein kinase signaling pathways. The Journal of Neuroscience, 21, 8842–8853.

    CAS  PubMed  Google Scholar 

  161. Gadea, A., Aguirre, A., Haydar, T. F., & Gallo, V. (2009). Endothelin-1 regulates oligodendrocyte development. The Journal of Neuroscience, 29, 10047–10062.

    Article  CAS  PubMed  Google Scholar 

  162. Lim, D. A., & Alvarez-Buylla, A. (1999). Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proceedings of the National Academy of Sciences of the United States of America, 96, 7526–7531.

    Article  CAS  PubMed  Google Scholar 

  163. Gadea, A., Schinelli, S., & Gallo, V. (2008). Endothelin-1 regulates astrocyte proliferation and reactive gliosis via a JNK/c-Jun signaling pathway. The Journal of Neuroscience, 28, 2394–2408.

    Article  CAS  PubMed  Google Scholar 

  164. Le Douarin, N. M., Creuzet, S., Couly, G., & Dupin, E. (2004). Neural crest cell plasticity and its limits. Development, 131, 4637–4650.

    Article  PubMed  CAS  Google Scholar 

  165. Sauka-Spengler, T., & Bronner-Fraser, M. (2008). A gene regulatory network orchestrates neural crest formation. Nature Reviews. Molecular Cell Biology, 9, 557–568.

    Article  CAS  PubMed  Google Scholar 

  166. Clouthier, D. E., & Schilling, T. F. (2004). Understanding endothelin-1 function during craniofacial development in the mouse and zebrafish. Birth Defects Research. Part C: Embryo Today, 72, 190–199.

    Article  CAS  Google Scholar 

  167. Kulesa, P. M., Bailey, C. M., Kasemeier-Kulesa, J. C., & McLennan R. (2010). Cranial neural crest migration: new rules for an old road. Developmental Biology, doi:10.1016/j.ydbio.2010.04.010.

  168. Kurihara, Y., Kurihara, H., Suzuki, H., et al. (1994). Elevated blood pressure and craniofacial abnormalities in mice deficient in endothelin-1. Nature, 368, 703–710.

    Article  CAS  PubMed  Google Scholar 

  169. Yanagisawa, H., Yanagisawa, M., Kapur, R. P., et al. (1998). Dual genetic pathways of endothelin-mediated intercellular signaling revealed by targeted disruption of endothelin converting enzyme-1 gene. Development, 125, 825–836.

    CAS  PubMed  Google Scholar 

  170. Clouthier, D. E., Hosoda, K., Richardson, J. A., et al. (1998). Cranial and cardiac neural crest defects in endothelin-A receptor-deficient mice. Development, 125, 813–824.

    CAS  PubMed  Google Scholar 

  171. Ruest, L. B., & Clouthier, D. E. (2009). Elucidating timing and function of endothelin-A receptor signaling during craniofacial development using neural crest cell-specific gene deletion and receptor antagonism. Developmental Biology, 328, 94–108.

    Article  CAS  PubMed  Google Scholar 

  172. Ruest, L. B., Xiang, X., Lim, K. C., Levi, G., & Clouthier, D. E. (2004). Endothelin-A receptor-dependent and -independent signaling pathways in establishing mandibular identity. Development, 131, 4413–4423.

    Article  CAS  PubMed  Google Scholar 

  173. Ozeki, H., Kurihara, Y., Tonami, K., Watatani, S., & Kurihara, H. (2004). Endothelin-1 regulates the dorsoventral branchial arch patterning in mice. Mechanisms of Development, 121, 387–395.

    Article  CAS  PubMed  Google Scholar 

  174. Abe, M., Ruest, L. B., & Clouthier, D. E. (2007). Fate of cranial neural crest cells during craniofacial development in endothelin-A receptor-deficient mice. The International Journal of Developmental Biology, 51, 97–105.

    Article  CAS  PubMed  Google Scholar 

  175. Zuniga, E., Stellabotte, F., & Crump, J. G. (2010). Jagged-Notch signaling ensures dorsal skeletal identity in the vertebrate face. Development, 137, 1843–1852.

    Article  CAS  PubMed  Google Scholar 

  176. Heanue, T. A., & Pachnis, V. (2007). Enteric nervous system development and Hirschsprung’s disease: advances in genetic and stem cell studies. Nature Reviews. Neuroscience, 8, 466–479.

    Article  CAS  PubMed  Google Scholar 

  177. Gammill, L. S., Roffers-Agarwal, J. (2010). Division of labor during trunk neural crest development. Developmental Biology, doi:10.1016/j.ydbio.2010.04.009.

  178. Brooks, A. S., Oostra, B. A., & Hofstra, R. M. (2005). Studying the genetics of Hirschsprung’s disease: unraveling an oligogenic disorder. Clinical Genetics, 67, 6–14.

    Article  CAS  PubMed  Google Scholar 

  179. Sanchez-Mejias, A., Fernandez, R. M., Lopez-Alonso, M., Antinolo, G., & Borrego, S. (2010). New roles of EDNRB and EDN3 in the pathogenesis of Hirschsprung disease. Genetics in Medicine, 12, 39–43.

    Article  CAS  PubMed  Google Scholar 

  180. Druckenbrod, N. R., Powers, P. A., Bartley, C. R., Walker, J. W., & Epstein, M. L. (2008). Targeting of endothelin receptor-B to the neural crest. Genesis, 46, 396–400.

    Article  CAS  PubMed  Google Scholar 

  181. Hosoda, K., Hammer, R. E., Richardson, J. A., et al. (1994). Targeted and natural (piebald-lethal) mutations of endothelin-B receptor gene produce megacolon associated with spotted coat color in mice. Cell, 79, 1267–1276.

    Article  CAS  PubMed  Google Scholar 

  182. Barlow, A., de Graaff, E., & Pachnis, V. (2003). Enteric nervous system progenitors are coordinately controlled by the G protein-coupled receptor EDNRB and the receptor tyrosine kinase RET. Neuron, 40, 905–916.

    Article  CAS  PubMed  Google Scholar 

  183. Lee, H. O., Levorse, J. M., & Shin, M. K. (2003). The endothelin receptor-B is required for the migration of neural crest-derived melanocyte and enteric neuron precursors. Developmental Biology, 259, 162–175.

    Article  CAS  PubMed  Google Scholar 

  184. Ro, S., Hwang, S. J., Muto, M., Jewett, W. K., & Spencer, N. J. (2006). Anatomic modifications in the enteric nervous system of piebald mice and physiological consequences to colonic motor activity. American Journal of Physiology. Gastrointestinal and Liver Physiology, 290, G710–G718.

    Article  CAS  PubMed  Google Scholar 

  185. Bondurand, N., Natarajan, D., Barlow, A., Thapar, N., & Pachnis, V. (2006). Maintenance of mammalian enteric nervous system progenitors by SOX10 and endothelin 3 signalling. Development, 133, 2075–2086.

    Article  CAS  PubMed  Google Scholar 

  186. Nagy, N., & Goldstein, A. M. (2006). Endothelin-3 regulates neural crest cell proliferation and differentiation in the hindgut enteric nervous system. Developmental Biology, 293, 203–217.

    Article  CAS  PubMed  Google Scholar 

  187. Carrasquillo, M. M., McCallion, A. S., Puffenberger, E. G., Kashuk, C. S., Nouri, N., & Chakravarti, A. (2002). Genome-wide association study and mouse model identify interaction between RET and EDNRB pathways in Hirschsprung disease. Nature Genetics, 32, 237–244.

    Article  CAS  PubMed  Google Scholar 

  188. Saldana-Caboverde, A., & Kos, L. (2010). Roles of endothelin signaling in melanocyte development and melanoma. Pigment Cell & Melanoma Research, 23, 160–170.

    CAS  Google Scholar 

  189. Lahav, R., Dupin, E., Lecoin, L., et al. (1998). Endothelin 3 selectively promotes survival and proliferation of neural crest-derived glial and melanocytic precursors in vitro. Proceedings of the National Academy of Sciences of the United States of America, 95, 14214–14219.

    Article  CAS  PubMed  Google Scholar 

  190. Real, C., Glavieux-Pardanaud, C., Le Douarin, N. M., & Dupin, E. (2006). Clonally cultured differentiated pigment cells can dedifferentiate and generate multipotent progenitors with self-renewing potential. Developmental Biology, 300, 656–669.

    Article  CAS  PubMed  Google Scholar 

  191. Hou, L., Pavan, W. J., Shin, M. K., & Arnheiter, H. (2004). Cell-autonomous and cell non-autonomous signaling through endothelin receptor B during melanocyte development. Development, 131, 3239–3247.

    Article  CAS  PubMed  Google Scholar 

  192. Ma, Q., Jones, D., Borghesani, P. R., et al. (1998). Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proceedings of the National Academy of Sciences of the United States of America, 95, 9448–9453.

    Article  CAS  PubMed  Google Scholar 

  193. Zou, Y. R., Kottmann, A. H., Kuroda, M., Taniuchi, I., & Littman, D. R. (1998). Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature, 393, 595–599.

    Article  CAS  PubMed  Google Scholar 

  194. Stumm, R. K., Zhou, C., Ara, T., et al. (2003). CXCR4 regulates interneuron migration in the developing neocortex. The Journal of Neuroscience, 23, 5123–5130.

    CAS  PubMed  Google Scholar 

  195. Tiveron, M. C., Rossel, M., Moepps, B., et al. (2006). Molecular interaction between projection neuron precursors and invading interneurons via stromal-derived factor 1 (CXCL12)/CXCR4 signaling in the cortical subventricular zone/intermediate zone. The Journal of Neuroscience, 26, 13273–13278.

    Article  CAS  PubMed  Google Scholar 

  196. Klein, R. S., & Rubin, J. B. (2004). Immune and nervous system CXCL12 and CXCR4: parallel roles in patterning and plasticity. Trends in Immunology, 25, 306–314.

    Article  CAS  PubMed  Google Scholar 

  197. Stumm, R., & Hollt, V. (2007). CXC chemokine receptor 4 regulates neuronal migration and axonal pathfinding in the developing nervous system: implications for neuronal regeneration in the adult brain. Journal of Molecular Endocrinology, 38, 377–382.

    Article  CAS  PubMed  Google Scholar 

  198. Garcia-Dominguez, M., Poquet, C., Garel, S., & Charnay, P. (2003). Ebf gene function is required for coupling neuronal differentiation and cell cycle exit. Development, 130, 6013–6025.

    Article  CAS  PubMed  Google Scholar 

  199. Borrell, V., Kaspar, B. K., Gage, F. H., & Callaway, E. M. (2006). In vivo evidence for radial migration of neurons by long-distance somal translocation in the developing ferret visual cortex. Cerebral Cortex, 16, 1571–1583.

    Article  PubMed  Google Scholar 

  200. Li, G., Kataoka, H., Coughlin, S. R., & Pleasure, S. J. (2009). Identification of a transient subpial neurogenic zone in the developing dentate gyrus and its regulation by Cxcl12 and reelin signaling. Development, 136, 327–335.

    Article  CAS  PubMed  Google Scholar 

  201. Lu, M., Grove, E. A., & Miller, R. J. (2002). Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor. Proceedings of the National Academy of Sciences of the United States of America, 99, 7090–7095.

    Article  CAS  PubMed  Google Scholar 

  202. Bagri, A., Gurney, T., He, X., et al. (2002). The chemokine SDF1 regulates migration of dentate granule cells. Development, 129, 4249–4260.

    CAS  PubMed  Google Scholar 

  203. Krathwohl, M. D., & Kaiser, J. L. (2004). Chemokines promote quiescence and survival of human neural progenitor cells. Stem Cells, 22, 109–118.

    Article  CAS  PubMed  Google Scholar 

  204. Wu, Y., Peng, H., Cui, M., Whitney, N. P., Huang, Y., & Zheng, J. C. (2009). CXCL12 increases human neural progenitor cell proliferation through Akt-1/FOXO3a signaling pathway. Journal of Neurochemistry, 109, 1157–1167.

    Article  CAS  PubMed  Google Scholar 

  205. Hagihara, K., Zhang, E. E., Ke, Y. H., et al. (2009). Shp2 acts downstream of SDF-1alpha/CXCR4 in guiding granule cell migration during cerebellar development. Developmental Biology, 334, 276–284.

    Article  CAS  PubMed  Google Scholar 

  206. Bhattacharyya, B. J., Banisadr, G., Jung, H., et al. (2008). The chemokine stromal cell-derived factor-1 regulates GABAergic inputs to neural progenitors in the postnatal dentate gyrus. The Journal of Neuroscience, 28, 6720–6730.

    Article  CAS  PubMed  Google Scholar 

  207. Kolodziej, A., Schulz, S., Guyon, A., et al. (2008). Tonic activation of CXC chemokine receptor 4 in immature granule cells supports neurogenesis in the adult dentate gyrus. The Journal of Neuroscience, 28, 4488–4500.

    Article  CAS  PubMed  Google Scholar 

  208. Tran, P. B., Banisadr, G., Ren, D., Chenn, A., & Miller, R. J. (2007). Chemokine receptor expression by neural progenitor cells in neurogenic regions of mouse brain. The Journal of Comparative Neurology, 500, 1007–1033.

    Article  CAS  PubMed  Google Scholar 

  209. Tozuka, Y., Fukuda, S., Namba, T., Seki, T., & Hisatsune, T. (2005). GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron, 47, 803–815.

    Article  CAS  PubMed  Google Scholar 

  210. Jagasia, R., Steib, K., Englberger, E., et al. (2009). GABA-cAMP response element-binding protein signaling regulates maturation and survival of newly generated neurons in the adult hippocampus. The Journal of Neuroscience, 29, 7966–7977.

    Article  CAS  PubMed  Google Scholar 

  211. Kiecker, C., & Niehrs, C. (2001). A morphogen gradient of Wnt/beta-catenin signalling regulates anteroposterior neural patterning in Xenopus. Development, 128, 4189–4201.

    CAS  PubMed  Google Scholar 

  212. Nordstrom, U., Jessell, T. M., & Edlund, T. (2002). Progressive induction of caudal neural character by graded Wnt signaling. Nature Neuroscience, 5, 525–532.

    Article  PubMed  Google Scholar 

  213. Houart, C., Caneparo, L., Heisenberg, C., Barth, K., Take-Uchi, M., & Wilson, S. (2002). Establishment of the telencephalon during gastrulation by local antagonism of Wnt signaling. Neuron, 35, 255–265.

    Article  CAS  PubMed  Google Scholar 

  214. Braun, M. M., Etheridge, A., Bernard, A., Robertson, C. P., & Roelink, H. (2003). Wnt signaling is required at distinct stages of development for the induction of the posterior forebrain. Development, 130, 5579–5587.

    Article  CAS  PubMed  Google Scholar 

  215. Lee, S. M., Tole, S., Grove, E., & McMahon, A. P. (2000). A local Wnt-3a signal is required for development of the mammalian hippocampus. Development, 127, 457–467.

    CAS  PubMed  Google Scholar 

  216. Danielian, P. S., & McMahon, A. P. (1996). Engrailed-1 as a target of the Wnt-1 signalling pathway in vertebrate midbrain development. Nature, 383, 332–334.

    Article  CAS  PubMed  Google Scholar 

  217. Jessell, T. M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nature Reviews. Genetics, 1, 20–29.

    Article  CAS  PubMed  Google Scholar 

  218. Hall, A. C., Lucas, F. R., & Salinas, P. C. (2000). Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell, 100, 525–535.

    Article  CAS  PubMed  Google Scholar 

  219. Lyuksyutova, A. I., Lu, C. C., Milanesio, N., et al. (2003). Anterior-posterior guidance of commissural axons by Wnt-frizzled signaling. Science, 302, 1984–1988.

    Article  CAS  PubMed  Google Scholar 

  220. Rosso, S. B., Sussman, D., Wynshaw-Boris, A., & Salinas, P. C. (2005). Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nature Neuroscience, 8, 34–42.

    Article  CAS  PubMed  Google Scholar 

  221. Packard, M., Koo, E. S., Gorczyca, M., Sharpe, J., Cumberledge, S., & Budnik, V. (2002). The Drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation. Cell, 111, 319–330.

    Article  CAS  PubMed  Google Scholar 

  222. Speese, S. D., & Budnik, V. (2007). Wnts: up-and-coming at the synapse. Trends in Neurosciences, 30, 268–275.

    Article  CAS  PubMed  Google Scholar 

  223. Ahmad-Annuar, A., Ciani, L., Simeonidis, I., et al. (2006). Signaling across the synapse: a role for Wnt and Dishevelled in presynaptic assembly and neurotransmitter release. The Journal of Cell Biology, 174, 127–139.

    Article  CAS  PubMed  Google Scholar 

  224. Ciani, L., & Salinas, P. C. (2005). WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nature Reviews. Neuroscience, 6, 351–362.

    Article  CAS  PubMed  Google Scholar 

  225. Stern, C. D. (2001). Initial patterning of the central nervous system: how many organizers? Nature Reviews. Neuroscience, 2, 92–98.

    Article  CAS  PubMed  Google Scholar 

  226. Daneman, R., Agalliu, D., Zhou, L., Kuhnert, F., Kuo, C. J., & Barres, B. A. (2009). Wnt/beta-catenin signaling is required for CNS, but not non-CNS, angiogenesis. Proceedings of the National Academy of Sciences of the United States of America, 106, 641–646.

    Article  CAS  PubMed  Google Scholar 

  227. Liebner, S., Corada, M., Bangsow, T., et al. (2008). Wnt/beta-catenin signaling controls development of the blood-brain barrier. The Journal of Cell Biology, 183, 409–417.

    Article  CAS  PubMed  Google Scholar 

  228. Stenman, J. M., Rajagopal, J., Carroll, T. J., Ishibashi, M., McMahon, J., & McMahon, A. P. (2008). Canonical Wnt signaling regulates organ-specific assembly and differentiation of CNS vasculature. Science, 322, 1247–1250.

    Article  CAS  PubMed  Google Scholar 

  229. Liebner, S., & Plate, K. H. (2010). Differentiation of the brain vasculature: the answer came blowing by the Wnt. Journal of Angiogenesis Research, 2, 1. doi:10.1186/2040-2384-2-1.

    Article  PubMed  CAS  Google Scholar 

  230. Lie, D. C., Colamarino, S. A., Song, H. J., et al. (2005). Wnt signalling regulates adult hippocampal neurogenesis. Nature, 437, 1370–1375.

    Article  CAS  PubMed  Google Scholar 

  231. Zhou, C. J., Zhao, C., & Pleasure, S. J. (2004). Wnt signaling mutants have decreased dentate granule cell production and radial glial scaffolding abnormalities. The Journal of Neuroscience, 24, 121–126.

    Article  CAS  PubMed  Google Scholar 

  232. Wexler, E. M., Paucer, A., Kornblum, H. I., Palmer, T. D., & Geschwind, D. H. (2009). Endogenous Wnt signaling maintains neural progenitor cell potency. Stem Cells, 27, 1130–1141.

    Article  CAS  PubMed  Google Scholar 

  233. Yu, J. M., Kim, J. H., Song, G. S., & Jung, J. S. (2006). Increase in proliferation and differentiation of neural progenitor cells isolated from postnatal and adult mice brain by Wnt-3a and Wnt-5a. Molecular and Cellular Biochemistry, 288, 17–28.

    Article  CAS  PubMed  Google Scholar 

  234. Inestrosa, N. C., & Arenas, E. (2010). Emerging roles of Wnts in the adult nervous system. Nature Reviews. Neuroscience, 11, 77–86.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by The O’Brien Foundation, The University of Melbourne, NHMRC/JDRF Programme Grant, Helen Macpherson Smith Trust and the Operational Infrastructure Support Scheme of the state of Victoria.

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The authors declare no potential conflicts of interest.

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Kobayashi, N.R., Hawes, S.M., Crook, J.M. et al. G-protein Coupled Receptors in Stem Cell Self-Renewal and Differentiation. Stem Cell Rev and Rep 6, 351–366 (2010). https://doi.org/10.1007/s12015-010-9167-9

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