Skip to main content

Advertisement

SpringerLink
Log in

Decidua Parietalis-Derived Mesenchymal Stromal Cells Reside in a Vascular Niche Within the Choriodecidua

  • Original Articles
  • Published:
Reproductive Sciences Aims and scope Submit manuscript

Abstract

Mesenchymal stromal cells (MSCs) from gestational tissues represent promising cell populations with stem cell-like properties for use in regenerative medicine. Previously, we reported that MSCs in the chorionic villi of the human placenta reside in a vascular niche. However, the niche(s) in which MSCs reside in the fetal membranes, another rich source of MSCs, remains to be determined. The cell surface markers STRO-1 and 3G5 were previously employed to identify niches in a variety of tissues and here we use these markers to report the location of the MSC niche in the human decidua parietalis. The cultured decidua parietalis MSCs (DPMSCs) isolated from the choriodecidua component of the fetal membranes possessed stem cell-like properties such as adherence to plastic, colony forming ability, and multipotent differentiation potential. Fluorescence in situ hybridization analysis showed cultured DPMSCs were of maternal origin. Immunocytochemistry demonstrated that cultured DPMSCs stained positively with stem cell surface markers 3G5, CD105, CD106, STRO-1, CD146, CD49a, and α-SMA but were negative for hematopoietic markers (CD117, CD34) and vascular markers (CD34, von Willebrand factor [vWF]). Immunohistochemistry with antibodies to stem cell surface markers and the endothelial markers on term fetal membranes revealed a vascular niche for DPMSCs, which was confirmed by immunofluorescence analysis. Both STRO-1 and vWF fluorescence signals showed substantial overlap, while CD146 and vWF signals showed partial overlap. These observations were consistent with a vascular niche.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Yen BL, Huang HI, Chien CC, et al. Isolation of multipotent cells from human term placenta. Stem Cells. 2005;23(1):3–9.

    Article  CAS  PubMed  Google Scholar 

  2. Fukuchi Y, Nakajima H, Sugiyama D, Hirose I, Kitamura T, Tsuji K. Human placenta-derived cells have mesenchymal stem/progenitor cell potential. Stem Cells. 2004;22(5):649–658.

    Article  CAS  PubMed  Google Scholar 

  3. Miao Z, Jin J, Chen L, et al. Isolation of mesenchymal stem cells from human placenta: comparison with human bone marrow mesenchymal stem cells. Cell Biol Int. 2006;30(9):681–687.

    Article  CAS  PubMed  Google Scholar 

  4. In’t Anker PS, Scherjon SA, Kleijburg-van der Keur C, et al. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells. 2004;22(7):1338–1345.

    Article  Google Scholar 

  5. Fauza D. Amniotic fluid and placental stem cells. Best Pract Res Clin Obstet Gynaecol. 2004;18(6):877–891.

    Article  PubMed  Google Scholar 

  6. Ilancheran S, Moodley Y, Manuelpillai U. Human fetal membranes: a source of stem cells for tissue regeneration and repair? Placenta. 2009;30(1):2–10.

    Article  CAS  PubMed  Google Scholar 

  7. Manuelpillai U, Moodley Y, Borlongan CV, Parolini O. Amniotic membrane and amniotic cells: potential therapeutic tools to combat tissue inflammation and fibrosis? Placenta. 2011;32(suppl 4): S320–S325.

    Article  CAS  PubMed  Google Scholar 

  8. Pappa KI, Anagnou NP. Novel sources of fetal stem cells: where do they fit on the developmental continuum? Regen Med. 2009; 4(3):423–433.

    Article  PubMed  Google Scholar 

  9. Runic R, Lockwood CJ, LaChapelle L, et al. Apoptosis and Fas expression in human fetal membranes. J Clin Endocrinol Metab. 1998;83(2):660–666.

    CAS  PubMed  Google Scholar 

  10. Bourne G. The foetal membranes. A review of the anatomy of normal amnion and chorion and some aspects of their function. Postgrad Med J. 1962;38:193–201.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Parry S, Strauss JF, 3rd. Premature rupture of the fetal membranes. N Engl J Med. 1998;338(10):663–670.

    Article  CAS  PubMed  Google Scholar 

  12. Wolbank S, van Griensven M, Grillari-Voglauer R, Peterbauer-Scherb A. Alternative sources of adult stem cells: human amniotic membrane. Adv Biochem Eng Biotechnol. 2010;123:1–27.

    CAS  PubMed  Google Scholar 

  13. Magatti M, De Munari S, Vertua E, Gibelli L, Wengler GS, Parolini O. Human amnion mesenchyme harbors cells with allogeneic T-cell suppression and stimulation capabilities. Stem Cells. 2008;26(1):182–192.

    Article  CAS  PubMed  Google Scholar 

  14. Parolini O, Alviano F, Bagnara GP, et al. Concise review: isolation and characterization of cells from human term placenta: outcome of the first international Workshop on Placenta Derived Stem Cells. Stem Cells. 2008;26(2):300–311.

    Article  PubMed  Google Scholar 

  15. Goldschlager T, Ghosh P, Zannettino A, et al. A comparison of mesenchymal precursor cells and amnion epithelial cells for enhancing cervical interbody fusion in an ovine model. Neurosurgery. 2011;68(4):1025–1034; discussion 1034–1025.

    Article  PubMed  Google Scholar 

  16. Soncini M, Vertua E, Gibelli L, et al. Isolation and characterization of mesenchymal cells from human fetal membranes. J Tissue Eng Regen Med. 2007;1(4):296–305.

    Article  CAS  PubMed  Google Scholar 

  17. Bailo M, Soncini M, Vertua E, et al. Engraftment potential of human amnion and chorion cells derived from term placenta. Transplantation. 2004;78(10):1439–1448.

    Article  PubMed  Google Scholar 

  18. Portmann-Lanz CB, Schoeberlein A, Huber A, et al. Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregeneration. Am J Obstet Gynecol. 2006;194(3): 664–673.

    Article  CAS  PubMed  Google Scholar 

  19. Genbacev O, Donne M, Kapidzic M, et al. Establishment of human trophoblast progenitor cell lines from the chorion. Stem Cells. 2011;29(9):1427–1436.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Strakova Z, Livak M, Krezalek M, Ihnatovych I. Multipotent properties of myofibroblast cells derived from human placenta. Cell Tissue Res. 2008;332(3):479–488.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Kyurkchiev S, Shterev A, Dimitrov R. Assessment of presence and characteristics of multipotent stromal cells in human endometrium and decidua. Reprod Biomed Online. 2010;20(3): 305–313.

    Article  PubMed  Google Scholar 

  22. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999; 284(5411):143–147.

    Article  CAS  PubMed  Google Scholar 

  23. Kolf CM, Cho E, Tuan RS. Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: regulation of niche, selfrenewal and differentiation. Arthritis Res Ther. 2007;9(1):204.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Miki T, Mitamura K, Ross MA, Stolz DB, Strom SC. Identification of stem cell marker-positive cells by immunofluorescence in term human amnion. J Reprod Immunol. 2007;75(2):91–96.

    Article  CAS  PubMed  Google Scholar 

  25. Shi S, Gronthos S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res. 2003;18(4):696–704.

    Article  PubMed  Google Scholar 

  26. Miura M, Gronthos S, Zhao M, et al. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A. 2003;100(10):5807–5812.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Seo BM, Miura M, Gronthos S, et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet. 2004;364(9429):149–155.

    Article  CAS  PubMed  Google Scholar 

  28. Zannettino AC, Paton S, Arthur A, et al. Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol. 2008;214(2):413–421.

    Article  CAS  PubMed  Google Scholar 

  29. Garcia-Pacheco JM, Oliver C, Kimatrai M, Blanco FJ, Olivares EG. Human decidual stromal cells express CD34 and STRO-1 and are related to bone marrow stromal precursors. Mol Hum Reprod. 2001;7(12):1151–1157.

    Article  CAS  PubMed  Google Scholar 

  30. Zannettino AC, Paton S, Kortesidis A, Khor F, Itescu S, Gronthos S. Human mulipotential mesenchymal/stromal stem cells are derived from a discrete subpopulation of STRO-1bright/CD34/ CD45(-)/glycophorin-A-bone marrow cells. Haematologica. 2007;92(12):1707–1708.

    Article  PubMed  Google Scholar 

  31. Bensidhoum M, Chapel A, Francois S, et al. Homing of in vitro expanded Stro-1- or Stro-1+ human mesenchymal stem cells into the NOD/SCID mouse and their role in supporting human CD34 cell engraftment. Blood. 2004;103(9):3313–3319.

    Article  CAS  PubMed  Google Scholar 

  32. Simmons PJ, Torok-Storb B. Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood. 1991;78(1):55–62.

    Article  CAS  PubMed  Google Scholar 

  33. Rider DA, Nalathamby T, Nurcombe V, Cool SM. Selection using the alpha-1 integrin (CD49a) enhances the multipotentiality of the mesenchymal stem cell population from heterogeneous bone marrow stromal cells. J Mol Histol. 2007;38(5):449–458.

    Article  CAS  PubMed  Google Scholar 

  34. Owen M. Marrow stromal stem cells. J Cell Sci Suppl. 1988;10: 63–76.

    Article  CAS  PubMed  Google Scholar 

  35. Deschaseaux F, Gindraux F, Saadi R, Obert L, Chalmers D, Herve P. Direct selection of human bone marrow mesenchymal stem cells using an anti-CD49a antibody reveals their CD45med,low phenotype. Br J Haematol. 2003;122(3):506–517.

    Article  PubMed  Google Scholar 

  36. Castrechini NM, Murthi P, Gude NM, et al. Mesenchymal stem cells in human placental chorionic villi reside in a vascular Niche. Placenta. 2010;31(3):203–212.

    Article  CAS  PubMed  Google Scholar 

  37. Gronthos S, Zannettino AC, Hay SJ, et al. Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci. 2003;116(Pt 9):1827–1835.

    Article  CAS  PubMed  Google Scholar 

  38. Shukunami C, Shigeno C, Atsumi T, Ishizeki K, Suzuki F, Hiraki Y. Chondrogenic differentiation of clonal mouse embryonic cell line ATDC5 in vitro: differentiation-dependent gene expression of parathyroid hormone (PTH)/PTH-related peptide receptor. J Cell Biol. 1996;133(2):457–468.

    Article  CAS  PubMed  Google Scholar 

  39. Yoshimura K, Shigeura T, Matsumoto D, et al. Characterization of freshly isolated and cultured cells derived from the fatty and fluid portions of liposuction aspirates. J Cell Physiol. 2006; 208(1):64–76.

    Article  CAS  PubMed  Google Scholar 

  40. Ogawa R, Mizuno H, Watanabe A, Migita M, Shimada T, Hyakusoku H. Osteogenic and chondrogenic differentiation by adipose-derived stem cells harvested from GFP transgenic mice. Biochem Biophys Res Commun. 2004;313(4):871–877.

    Article  CAS  PubMed  Google Scholar 

  41. Zhao Y, Zou B, Shi Z, Wu Q, Chen GQ. The effect of 3-hydroxybutyrate on the in vitro differentiation of murine osteoblast MC3T3-E1 and in vivo bone formation in ovariectomized rats. Biomaterials. 2007;28(20):3063–3073.

    Article  CAS  PubMed  Google Scholar 

  42. Murthi P, So M, Gude NM, Doherty VL, Brennecke SP, Kalionis B. Homeobox genes are differentially expressed in macrovascular human umbilical vein endothelial cells and microvascular placental endothelial cells. Placenta. 2007;28(2–3):219–223.

    Article  CAS  PubMed  Google Scholar 

  43. Mueller UW, Hawes CS, Jones WR. Identification of extravillous trophoblast cells in human decidua using an apparently unique murine monoclonal antibody to trophoblast. Histochem J. 1987;19(5):288–296.

    Article  CAS  PubMed  Google Scholar 

  44. Hawes CS, Petropoulos A, Lopata A, Kalionis B, Jones WR. Reactivity of human trophoblast monoclonal antibodies with marmoset monkey trophoblast cultures. Hum Reprod. 1998;13(5):1169–1174.

    Article  CAS  PubMed  Google Scholar 

  45. Harper J, Wilton L. FISH and embryo sexing to avoid X-linked disease. In: Harper J, Delhanty J, Handyside A, eds. Preimplantation Genetic Diagnosis. UK: John Wiley & Sons; 2001:191–202.

    Chapter  Google Scholar 

  46. Murthi P, Kee MW, Gude NM, Brennecke SP, Kalionis B. Fetal growth restriction is associated with increased apoptosis in the chorionic trophoblast cells of human fetal membranes. Placenta. 2005;26(4):329–338.

    Article  CAS  PubMed  Google Scholar 

  47. Caplan AI. All MSCs are pericytes? Cell Stem Cell. 2008;3(3): 229–230.

    Article  CAS  PubMed  Google Scholar 

  48. da Silva Meirelles L, Caplan AI, Nardi NB. In search of the in vivo identity of mesenchymal stem cells. Stem Cells. 2008; 26(9):2287–2299.

    Article  PubMed  Google Scholar 

  49. Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315–317.

    Article  CAS  PubMed  Google Scholar 

  50. Lin G, Garcia M, Ning H, et al. Defining stem and progenitor cells within adipose tissue. Stem Cells Dev. 2008;17(6):1053–1063.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Lin G, Liu G, Banie L, et al. Tissue distribution of mesenchymal stem cell marker Stro-1. Stem Cells Dev. 2011;20(10):1747–1752.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Ning H, Lin G, Lue TF, Lin CS. Mesenchymal stem cell marker Stro-1 is a 75 kd endothelial antigen. Biochem Biophys Res Commun. 2011;413(2):353–357.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Szoke K, Beckstrom KJ, Brinchmann JE. Human adipose tissue as a source of cells with angiogenic potential [published online ahead of print June 7, 2011]. Cell Transplant. 2011.

  54. St Croix B, Rago C, Velculescu V, et al. Genes expressed in human tumor endothelium. Science. 2000;289(5482):1197–1202.

    Article  Google Scholar 

  55. Crisan M, Corselli M, Chen CW, Peault B. Multilineage stem cells in the adult: a perivascular legacy? Organogenesis. 2011;7(2): 101–104.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Crisan M, Yap S, Casteilla L, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3(3):301–313.

    Article  CAS  PubMed  Google Scholar 

  57. Diaz-Flores L, Gutierrez R, Madrid JF, et al. Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol. 2009;24(7):909–969.

    CAS  PubMed  Google Scholar 

  58. Slukvin II, Vodyanik M. Endothelial origin of mesenchymal stem cells. Cell Cycle. 2011;10(9):1370–1373.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Nayak RC, Berman AB, George KL, Eisenbarth GS, King GL. A monoclonal antibody (3G5)-defined ganglioside antigen is expressed on the cell surface of microvascular pericytes. J Exp Med. 1988;167(3):1003–1015.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Obstetrics and Gynaecology, Pregnancy Research Centre, Royal Women’s Hospital, University of Melbourne, Parkville, Victoria, Australia

    N. M. Castrechini PhD, P. Murthi PhD, S. Qin BSc(Hons), G. D. Kusuma BSc(Hons), N. M. Gude PhD, S. P. Brennecke DPhil(Oxon) & B. Kalionis PhD

  2. Department of Perinatal Medicine, Pregnancy Research Centre, Royal Women’s Hospital, University of Melbourne, Locked Bag 300, 3052, Parkville, Victoria, Australia

    N. M. Castrechini PhD, P. Murthi PhD, S. Qin BSc(Hons), G. D. Kusuma BSc(Hons), N. M. Gude PhD, S. P. Brennecke DPhil(Oxon) & B. Kalionis PhD

  3. Melbourne IVF, Victoria, Australia

    L. Wilton PhD

  4. King Abdullah International Medical Research Center, King Saud Bin Abdulaziz University for Health Sciences, King Abdulaziz Medical City, National Guard Health Affairs, Riyadh, Saudi Arabia

    M. Abumaree PhD

  5. Mesenchymal Stem Cell Group, Department of Haematology, SA Pathology/Centre for Stem Cell Research Robinson Institute/Discipline of Medicine, University of Adelaide, SA, Australia

    S. Gronthos PhD

  6. Department of Haematology, SA Pathology, Hanson Institute and Centre for Stem Cell Research, Robinson Institute, University of Adelaide, Adelaide, SA, Australia

    A. Zannettino PhD

Authors
  1. N. M. Castrechini PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Murthi PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Qin BSc(Hons)
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. G. D. Kusuma BSc(Hons)
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. L. Wilton PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Abumaree PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. S. Gronthos PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. A. Zannettino PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. N. M. Gude PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. S. P. Brennecke DPhil(Oxon)
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. B. Kalionis PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to B. Kalionis PhD.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Castrechini, N.M., Murthi, P., Qin, S. et al. Decidua Parietalis-Derived Mesenchymal Stromal Cells Reside in a Vascular Niche Within the Choriodecidua. Reprod. Sci. 19, 1302–1314 (2012). https://doi.org/10.1177/1933719112450334

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1177/1933719112450334

Keywords

Search

Navigation