Skip to main content

Advertisement

SpringerLink
Log in

The bone marrow metastasis niche in retinoblastoma

  • Review
  • Published:
Cellular Oncology Aims and scope Submit manuscript

Abstract

Background

Retinoblastoma (Rb) is a progressive cancer which mainly occurs in children, and which is caused by different genetic or epigenetic alterations that lead to inactivation of both alleles of the RB1 gene. Hereditary and non-hereditary forms of Rb do exist, and the hereditary form is associated with an increased risk of secondary malignancies. Metastasis to distant organs is a critical feature of many tumors, and may be caused by various molecular alterations at different stages. Recognition of these alterations and, thus, insight into the processes underlying the development of metastases may result in novel preventive as well as effective targeted treatment options. Rb is associated with metastases to various organs and tissues, including the bone marrow (BM).

Methods

Here, we provide an overview of mutations and other molecular changes known to be involved in Rb development and metastasis to the BM. This overview is based on a literature search ranging from 1990 to 2015.

Conclusions

The various BM metastasis-related molecular changes identified to date may be instrumental for a better diagnosis, prognosis and classification of Rb patients, as well as for the development of novel comprehensive (targeted) therapies.

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

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

VEGF:

Vascular endothelial growth factor

VEGF-R:

Vascular endothelial growth factor receptor

FGF:

Fibroblast growth factor

KIF14:

Kinesin family member 14

MYCN:

V-myc myelocytomatosis viral oncogene neuroblastoma-derived homolog

KiSS1:

KiSS-1 metastasis suppressor

FGF-R:

Fibroblast growth factor receptor

N-cadherin:

Neural-cadherin

ECM:

Extracellular matrix

MMPs:

Matrix metalloproteinases

LOX:

Lysyl oxidase.

References

  1. M. Kuruva, B.R. Mittal, R. Kashyap, A. Bhattacharya, R.K. Marwaha, Bilateral retinoblastoma presenting as metastases to forearm bones four years after the initial treatment. Indian J. Nucl. Med. 26, 115–116 (2011)

    Article  PubMed Central  PubMed  Google Scholar 

  2. M.J. Ali, S.G. Honavar, V.A. Reddy, Distant metastatic retinoblastoma without central nervous system involvement. Indian J. Ophthalmol. 61, 357–159 (2013)

    Article  PubMed Central  PubMed  Google Scholar 

  3. S.N. Zafar, S.Q. Ahmad, N. Zafar, Retinoblastoma in an adult. BMC Res. Notes. 6, 1–3 (2013)

    Article  Google Scholar 

  4. J. Yun, Y. Li, C.-T. Xu, B.-R. Pan, Epidemiology and Rb1 gene of retinoblastoma. Int. J. Ophthalmol. 4, 103–109 (2011)

    PubMed Central  PubMed  Google Scholar 

  5. G.L. Chantada and I.J. Dunkel, in Retinoblastoma, ed. by C. Rodriguez-Galindo and M.W. Wilson (Springer US, 2010), p. 103–114

  6. G.L. Chantada, C. Sampor, A. Bosaleh, V. Solernou, A. Fandiño, M.T. de Dávila, Comparison of staging systems for extraocular retinoblastoma: analysis of 533 patients. JAMA Ophthalmol. 131, 1127–1134 (2013)

    Article  PubMed  Google Scholar 

  7. Y. Tabe, M. Konopleva, Advances in understanding the leukaemia microenvironment. Br. J. Haematol. 164, 767–778 (2014)

    Article  PubMed Central  PubMed  Google Scholar 

  8. S. Azizidoost, S. Babashah, F. Rahim, M. Shahjahani, N. Saki, Bone marrow neoplastic niche in leukemia. Hematology 19, 232–238 (2014)

    Article  CAS  PubMed  Google Scholar 

  9. V.B.F. Vallone, H. Choi, V. Labovsky, L.M. Martinez, V. Milovic, G. Jaimovich, E. Batagelj, F. Dimase, A.R. Villafañe, N.A. Chasseing, Bone marrow mesenchymal stem cells: pre-metastatic niche for breast cancer. Blood 122, 4859–4859 (2013)

    Google Scholar 

  10. P.T. Finger, J.W. Harbour, Z.A. Karcioglu, Risk factors for metastasis in retinoblastoma. Surv. Ophthalmol. 47, 1–16 (2002)

    Article  PubMed  Google Scholar 

  11. A. Ray, D.S. Gombos, Retinoblastoma: an overview. Indian J. Pediatr. 79, 916–921 (2012)

    Article  PubMed  Google Scholar 

  12. G. Bunin, M. Orjuela et al., in Clinical Ophthalmic Oncology, ed. by A.D. Singh, A.L. Murphree, B.E. Damato (Springer, Berlin, 2015), pp. 39–50

    Google Scholar 

  13. L. Castéra, C. Dehainault, D. Michaux, L. Lumbroso-Le Rouic, I. Aerts, F. Doz, A. Pelet, J. Couturier, D. Stoppa-Lyonnet, M. Gauthier-Villars, Fine mapping of whole RB1 gene deletions in retinoblastoma patients confirms PCDH8 as a candidate gene for psychomotor delay. Eur. J. Med. Gen. 21, 460–464 (2013)

    Google Scholar 

  14. M.-y. He, Y. An, Y.-j. Gao, X.-w. Qian, G. Li, J. Qian, Screening of RB1 gene mutations in Chinese patients with retinoblastoma and preliminary exploration of genotype–phenotype correlations. Mol. Vis. 20, 545–552 (2014)

    PubMed Central  PubMed  Google Scholar 

  15. M. Sabir, R.M. Baig, K. Ali, I. Mahjabeen, M. Saeed, M.A. Kayani, Retinoblastoma (RB1) pocket domain mutations and promoter hyper-methylation in head and neck cancer. Cell. Oncol. 37, 203–213 (2014)

    Article  CAS  Google Scholar 

  16. J. Sage, The retinoblastoma tumor suppressor and stem cell biology. Genes Dev. 26, 1409–1420 (2012)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. S.L. Anwar, T. Krech, B. Hasemeier, E. Schipper, N. Schweitzer, A. Vogel, H. Kreipe, U. Lehmann, Deregulation of RB1 expression by loss of imprinting in human hepatocellular carcinoma. J. Pathol. 233, 392–401 (2014)

    Article  CAS  PubMed  Google Scholar 

  18. C. Marouf, A. Tazzite, B. Diakité, H. Jouhadi, A. Benider, S. Nadifi, Association of TP53 PIN3 polymorphism with breast cancer in Moroccan population. Tumour Biol. 35, 12403–12408 (2014)

    Article  CAS  PubMed  Google Scholar 

  19. M. Wade, Y.-C. Li, G.M. Wahl, MDM2, MDMX and p53 in oncogenesis and cancer therapy. Nat. Rev. Cancer 13, 83–96 (2013)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. A. Agrawal, J. Yang, R.F. Murphy, D.K. Agrawal, Regulation of the p14ARF-Mdm2-p53 pathway: an overview in breast cancer. Exp. Mol. Pathol. 81, 115–122 (2006)

    Article  CAS  PubMed  Google Scholar 

  21. N.A. Laurie, S.L. Donovan, C.-S. Shih, J. Zhang, N. Mills, C. Fuller, A. Teunisse, S. Lam, Y. Ramos, A. Mohan, Inactivation of the p53 pathway in retinoblastoma. Nature 444, 61–66 (2006)

    Article  CAS  PubMed  Google Scholar 

  22. N.A. Laurie, M.A. Dyer, Targeting MDM2 and MDMX in retinoblastoma. Curr. Cancer Drug Targets 7, 689–695 (2007)

    Article  CAS  PubMed  Google Scholar 

  23. B.L. Thériault, H. Dimaras, B.L. Gallie, T.W. Corson, The genomic landscape of retinoblastoma: a review. Clin. Exp. Ophthalmol. 42, 33–52 (2014)

    Article  Google Scholar 

  24. J.-Y. Choe, J.Y. Yun, Y.K. Jeon, S.H. Kim, H.-K. Choung, S. Oh, M. Park, J.E. Kim, Sonic hedgehog signalling proteins are frequently expressed in retinoblastoma and are associated with aggressive clinicopathological features. J. Clin. Pathol. 68, 6–11 (2015)

    Article  PubMed  Google Scholar 

  25. S. Siffroi-Fernandez, A. Cinaroglu, V. Fuhrmann-Panfalone, G. Normand, K. Bugra, J. Sahel, D. Hicks, Acidic fibroblast growth factor (FGF-1) and FGF receptor 1 signaling in human Y79 retinoblastoma. Arch. Ophthalmol. 123, 368–376 (2005)

    Article  CAS  PubMed  Google Scholar 

  26. N. Sethi, Y. Kang, Unravelling the complexity of metastasis—molecular understanding and targeted therapies. Nat. Rev. Cancer 11, 735–748 (2011)

    Article  CAS  PubMed  Google Scholar 

  27. A. Geurts van Kessel, The cancer genome: from structure to function. Cell. Oncol. 37, 155–165 (2014)

    Article  Google Scholar 

  28. A.C. Chiang, J. Massagué, Molecular basis of metastasis. N. Engl. J. Med. 359, 2814–2823 (2008)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. J.H. Tsai, J. Yang, Epithelial–mesenchymal plasticity in carcinoma metastasis. Genes Dev. 27, 2192–2206 (2013)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. E.Y. Lee, W.J. Muller, Oncogenes and tumor suppressor genes. Cold Spring Harb. Perspect. Biol. 2, a003236 (2010)

    CAS  PubMed Central  PubMed  Google Scholar 

  31. C.G.A. Network, Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330–337 (2012)

    Article  Google Scholar 

  32. C.Q. Lin, J. Singh, K. Murata, Y. Itahana, S. Parrinello, S.H. Liang, C.E. Gillett, J. Campisi, P.-Y. Desprez, A role for Id-1 in the aggressive phenotype and steroid hormone response of human breast cancer cells. Cancer Res. 60, 1332–1340 (2000)

    CAS  PubMed  Google Scholar 

  33. Z. Shengbing, L. Jing Feng, W. Bin, G. Lingyun, H. Aimin, Expression of KiSS‐1 gene and its role in invasion and metastasis of human hepatocellular carcinoma. Anat. Rec. (Hoboken). 292, 1128–1134 (2009)

    Article  PubMed  Google Scholar 

  34. D. Nie, J. Nemeth, Y. Qiao, A. Zacharek, L. Li, K. Hanna, K. Tang, G.G. Hillman, M.L. Cher, D.J. Grignon, Increased metastatic potential in human prostate carcinoma cells by overexpression of arachidonate 12-lipoxygenase. Clin. Exp. Metastasis 20, 657–663 (2003)

    Article  CAS  PubMed  Google Scholar 

  35. J. Liu, W. Wei, W. Tang, Y. Jiang, H. Yang, J. Li, Mechanism of lysyl oxidase (LOX) in breast cancer invasion and metastasis. Zhonghua Yi Xue Za Zhi 92, 1379–1383 (2012)

    CAS  PubMed  Google Scholar 

  36. D.X. Nguyen, P.D. Bos, J. Massagué, Metastasis: from dissemination to organ-specific colonization. Nat. Rev. Cancer 9, 274–284 (2009)

    Article  CAS  PubMed  Google Scholar 

  37. D. Maret, E. Gruzglin, M.S. Sadr, V. Siu, W. Shan, A.W. Koch, N.G. Seidah, R.F. Del Maestro, D.R. Colman, Surface expression of precursor N-cadherin promotes tumor cell invasion. Neoplasia 12, 1066–1038 (2010)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. E. Haÿ, E. Laplantine, V. Geoffroy, M. Frain, T. Kohler, R. Müller, P.J. Marie, N-cadherin interacts with axin and LRP5 to negatively regulate Wnt/β-catenin signaling, osteoblast function, and bone formation. Mol. Cell. Biol. 29, 953–964 (2009)

    Article  PubMed Central  PubMed  Google Scholar 

  39. M.E. Diamond, L. Sun, A.J. Ottaviano, M.J. Joseph, H.G. Munshi, Differential growth factor regulation of N-cadherin expression and motility in normal and malignant oral epithelium. J. Cell Sci. 121, 2197–2207 (2008)

    Article  CAS  PubMed  Google Scholar 

  40. H. Zhuo, K. Jiang, L. Dong, Y. Zhu, L. Lü, Y. Lü, Y. Zhang, H. Zhang, Y. Ye, S. Wang, Overexpression of N-cadherin is correlated with metastasis and worse survival in colorectal cancer patients. Chin. Sci. Bull. 58, 3529–3534 (2013)

    Article  CAS  Google Scholar 

  41. E.H. Van Aken, P. Papeleu, P. De Potter, E. Bruyneel, J. Philippé, S. Seregard, A. Kvanta, J.-J. De Laey, M.M. Mareel, Structure and function of the N-cadherin/catenin complex in retinoblastoma. Invest. Ophthalmol. Vis. Sci. 43, 595–602 (2002)

    PubMed  Google Scholar 

  42. J. Schiffman, G. Grunwald, Differential cell adhesion and expression of N-cadherin among retinoblastoma cell lines. Invest. Ophthalmol. Vis. Sci. 33, 1568–1574 (1992)

    CAS  PubMed  Google Scholar 

  43. A. Kvanta, B. Steen, S. Seregard, Expression of vascular endothelial growth factor (VEGF) in retinoblastoma but not in posterior uveal melanoma. Exp. Eye Res. 63, 511–518 (1996)

    Article  CAS  PubMed  Google Scholar 

  44. C. Gialeli, A.D. Theocharis, N.K. Karamanos, Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J. 278, 16–27 (2011)

    Article  CAS  PubMed  Google Scholar 

  45. M. Kandalam, M. Mitra, K. Subramanian, J. Biswas, Molecular pathology of retinoblastoma. Middle East Afr. J. Ophthalmol. 17, 217–223 (2010)

    Article  PubMed Central  PubMed  Google Scholar 

  46. C. Martins, B. Fernandes, E. Antecka, S. Di Cesare, J. Mansure, J. Marshall, M. Burnier, Expression of the metastasis suppressor gene KISS1 in uveal melanoma. Eye (Lond). 22, 707–711 (2008)

    Article  CAS  PubMed  Google Scholar 

  47. F.-S. Wang, H. Chen, Z.-Y. Wu, J.-H. Lin, KISS1 expression in osteosarcoma: high in chinese clinical cases, but lower in cell lines. Asian Pac. J. Cancer Prev. 12, 3229–3234 (2011)

    PubMed  Google Scholar 

  48. K.T. Nash, P.A. Phadke, J.-M. Navenot, D.R. Hurst, M.A. Accavitti-Loper, E. Sztul, K.S. Vaidya, A.R. Frost, J.C. Kappes, S.C. Peiper, Requirement of KISS1 secretion for multiple organ metastasis suppression and maintenance of tumor dormancy. J. Natl. Cancer Inst. 99, 309–321 (2007)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  49. M. Sanchez-Carbayo, P. Capodieci, C. Cordon-Cardo, Tumor suppressor role of KiSS-1 in bladder cancer: loss of KiSS-1 expression is associated with bladder cancer progression and clinical outcome. Am. J. Pathol. 162, 609–617 (2003)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  50. T.M. Goto, Y. Arima, O. Nagano, H. Saya, Lysyl oxidase is induced by cell density-mediated cell cycle suppression via RB-E2F1-HIF-1α axis. Cell Struct. Funct. 38, 9–14 (2013)

    Article  CAS  PubMed  Google Scholar 

  51. J.J. Park, S.J. Hwang, J.-H. Park, H.-J. Lee, Chlorogenic acid inhibits hypoxia-induced angiogenesis via down-regulation of the HIF-1α/AKT pathway. Cell. Oncol. 38, 1–8 (2015)

    Article  Google Scholar 

  52. Z. Lu, F. Bauzon, H. Fu, J. Cui, H. Zhao, K. Nakayama, K.I. Nakayama and L. Zhu, Skp2 suppresses apoptosis in Rb1-deficient tumours by limiting E2F1 activity. Nat Commun. 5, 3463 (2014) doi: 10.1038/ncomms4463

  53. H.-G. Kopp, S.T. Avecilla, A.T. Hooper, S. Rafii, The bone marrow vascular niche: home of HSC differentiation and mobilization. Physiology (Bethesda) 20, 349–356 (2005)

    Article  CAS  Google Scholar 

  54. B. Furusato, A. Mohamed, M. Uhlén, J.S. Rhim, CXCR4 and cancer. Pathol. Int. 60, 497–505 (2010)

    Article  CAS  PubMed  Google Scholar 

  55. M.M. Balla, G.K. Vemuganti, C. Kannabiran, S.G. Honavar, R. Murthy, Phenotypic characterization of retinoblastoma for the presence of putative cancer stem-like cell markers by flow cytometry. Invest. Ophthalmol. Vis. Sci. 50, 1506–1514 (2009)

    Article  PubMed  Google Scholar 

  56. C. Salinas-Souza, R. De Oliveira, M.T.D.S. Alves, R.J. Garcia Filho, A.S. Petrilli, S.R.C. Toledo, The metastatic behavior of osteosarcoma by gene expression and cytogenetic analyses. Hum. Pathol. 44, 2188–2198 (2013)

    Article  CAS  PubMed  Google Scholar 

  57. G.D. Roodman, Genes associate with abnormal bone cell activity in bone metastasis. Cancer Metastasis Rev. 31, 569–578 (2012)

    Article  CAS  PubMed  Google Scholar 

  58. F. Navid, V.M. Santana, R.C. Barfield, Anti-GD2 antibody therapy for GD2-expressing tumors. Curr. Cancer Drug Targets 10, 200–209 (2010)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  59. D. Dávila, Optimization of molecular detection of GD2 synthase mRNA in retinoblastoma. Mol. Med. Rep. 3, 253–259 (2010)

    PubMed  Google Scholar 

  60. J. Di, T. Duiveman-de Boer, P.L. Zusterzeel, C.G. Figdor, L.F.G. Massuger, R. Torensma, The stem cell markers Oct4A, Nanog and c-Myc are expressed in ascites cells and tumor tissue of ovarian cancer patients. Cell. Oncol. 36, 363–374 (2013)

    Article  CAS  Google Scholar 

  61. T. Hiraga, S. Ito, H. Nakamura, Cancer stem–like cell marker CD44 promotes bone metastases by enhancing tumorigenicity, cell motility, and hyaluronan production. Cancer Res. 73, 4112–4122 (2013)

    Article  CAS  PubMed  Google Scholar 

  62. F. Rahim, S. Hajizamani, E. Mortaz, A. Ahmadzadeh, M. Shahjahani, S. Shahrabi, N. Saki, Molecular regulation of bone marrow metastasis in prostate and breast cancer. Bone Marrow Res. 2014, 1–13 (2014)

    Article  Google Scholar 

  63. P. Massoner, T. Thomm, B. Mack, G. Untergasser, A. Martowicz, K. Bobowski, H. Klocker, O. Gires, M. Puhr, EpCAM is overexpressed in local and metastatic prostate cancer, suppressed by chemotherapy and modulated by MET-associated miRNA-200c/205. Br. J. Cancer 111, 955–964 (2014). doi:10.1038/bjc.2014.366

    Article  CAS  PubMed  Google Scholar 

  64. S. Krishnakumar, A. Mohan, K. Mallikarjuna, N. Venkatesan, J. Biswas, M.P. Shanmugam, L. Ren-Heidenreich, EpCAM expression in retinoblastoma: a novel molecular target for therapy. Invest. Ophthalmol. Vis. Sci. 45, 4247–4250 (2004)

    Article  PubMed  Google Scholar 

  65. B. Ell and Y. Kang, MicroRNAs as regulators of bone homeostasis and bone metastasis . Bonekey Rep. 3, 1608 (2014) doi: 10.1038/bonekey.2014.44

  66. C. Salazar, R. Nagadia, P. Pandit, J. Cooper-White, N. Banerjee, N. Dimitrova, W.B. Coman, C. Punyadeera, A novel saliva-based microRNA biomarker panel to detect head and neck cancers. Cell. Oncol. 37, 331–338 (2014)

    Article  CAS  Google Scholar 

  67. C. Yu, M. Wang, Z. Li, J. Xiao, F. Peng, X. Guo, Y. Deng, J. Jiang, C. Sun, MicroRNA-138-5p regulates pancreatic cancer cell growth through targeting FOXC1. Cell. Oncol. 38, 1–9 (2015)

    Article  Google Scholar 

  68. H. Zhang, Y. Li, M. Lai, The microRNA network and tumor metastasis. Oncogene 29, 937–948 (2009)

    Article  PubMed  Google Scholar 

  69. Y. Bai, X. Bai, Z. Wang, X. Zhang, C. Ruan, J. Miao, MicroRNA-126 inhibits ischemia-induced retinal neovascularization via regulating angiogenic growth factors. Exp. Mol. Pathol. 91, 471–477 (2011)

    Article  CAS  PubMed  Google Scholar 

  70. S.F. Tavazoie, C. Alarcón, T. Oskarsson, D. Padua, Q. Wang, P.D. Bos, W.L. Gerald, J. Massagué, Endogenous human microRNAs that suppress breast cancer metastasis. Nature 451, 147–152 (2008)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  71. N. Venkatesan, P. Deepa, M. Vasudevan, V. Khetan, A.M. Reddy, S. Krishnakumar, Integrated analysis of dysregulated miRNA-gene expression in HMGA2-silenced retinoblastoma cells. Bioinform. Biol. Insights. 8, 177–191 (2014)

    CAS  PubMed Central  PubMed  Google Scholar 

  72. M. Scarola, S. Schoeftner, C. Schneider, R. Benetti, miR-335 directly targets Rb1 (pRb/p105) in a proximal connection to p53-dependent stress response. Cancer Res. 70, 6925–6933 (2010)

    Article  CAS  PubMed  Google Scholar 

  73. G. Gabriely, T. Wurdinger, S. Kesari, C.C. Esau, J. Burchard, P.S. Linsley, A.M. Krichevsky, MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol. Cell. Biol. 28, 5369–5380 (2008)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. L.-X. Yan, X.-F. Huang, Q. Shao, M.-Y. Huang, L. Deng, Q.-L. Wu, Y.-X. Zeng, J.-Y. Shao, MicroRNA miR-21 overexpression in human breast cancer is associated with advaanced clinical stage, lymph node metastasis and patient poor prognosis. RNA 14, 2348–2360 (2008)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  75. M. Bullock, K. Pickard, B.S. Nielsen, A.E. Sayan, V. Jenei, M. Mellone, J. Primrose, G. Thomas, G. Packham, A. Mirnezami, Deregulated stromal microRNA-21 and promotion of metastatic progression in colorectal cancer. Lancet 383, S30 (2014)

    Article  Google Scholar 

  76. E.C. Connolly, K. Van Doorslaer, L.E. Rogler, C.E. Rogler, Overexpression of miR-21 promotes an in vitro metastatic phenotype by targeting the tumor suppressor RHOB. Mol. Cancer Res. 8, 691–700 (2010)

    Article  CAS  PubMed  Google Scholar 

  77. F. Shen, M.-H. Mo, L. Chen, S. An, X. Tan, Y. Fu, K. Rezaei, Z. Wang, L. Zhang, S.W. Fu, MicroRNA-21 down-regulates Rb1 expression by targeting PDCD4 in retinoblastoma. J. Cancer. 5, 804–812 (2014)

    Article  PubMed Central  PubMed  Google Scholar 

  78. B. Psaila, D. Lyden, The metastatic niche: adapting the foreign soil. Nat. Rev. Cancer 9, 285–293 (2009)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  79. S. Wan, Y. Liu, Y. Weng, W. Wang, W. Ren, C. Fei, Y. Chen, Z. Zhang, T. Wang, J. Wang, BMP9 regulates cross-talk between breast cancer cells and bone marrow-derived mesenchymal stem cells. Cell. Oncol. 37, 363–375 (2014)

    Article  CAS  Google Scholar 

  80. S. Shahrabi, S. Azizidoost, M. Shahjahani, F. Rahim, A. Ahmadzadeh, N. Saki, New insights in cellular and molecular aspects of BM niche in chronic myelogenous leukemia. Tumour Biol. 35, 10627–10633 (2014)

    Article  CAS  PubMed  Google Scholar 

  81. C.F. Chantrain, O. Feron, E. Marbaix, Y.A. DeClerck, Bone marrow microenvironment and tumor progression. Cancer Microenviron. 1, 23–35 (2008)

    Article  PubMed Central  PubMed  Google Scholar 

  82. A. Ganguly, C.L. Shields, Differential gene expression profile of retinoblastoma compared to normal retina. Mol. Vis. 16, 1292–1303 (2010)

    CAS  PubMed Central  PubMed  Google Scholar 

  83. A.M. Roccaro, A. Sacco, W.G. Purschke, M. Moschetta, K. Buchner, C. Maasch, D. Zboralski, S. Zöllner, S. Vonhoff, Y. Mishima, SDF-1 inhibition targets the bone marrow niche for cancer therapy. Cell Rep. 9, 118–128 (2014)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  84. P. Bianco, M. Riminucci, S. Gronthos, P.G. Robey, Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19, 180–192 (2001)

    Article  CAS  PubMed  Google Scholar 

  85. S.-P. Lin, F.-Y. Chiu, Y. Wang, M.-L. Yen, S.-Y. Kao and S.-C. Hung, RB Maintains Quiescence and Prevents Premature Senescence through Upregulation of DNMT1 in Mesenchymal Stromal Cells. Stem Cell Rep. 3, 975–986 (2014) doi: 10.1016/j.stemcr.2014.10.002

  86. C.R. Walkley, J.M. Shea, N.A. Sims, L.E. Purton, S.H. Orkin, Rb regulates interactions between hematopoietic stem cells and their bone marrow microenvironment. Cell 129, 1081–1095 (2007)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  87. G.B. Adams, D.T. Scadden, The hematopoietic stem cell in its place. Nat. Immunol. 7, 333–337 (2006)

    Article  CAS  PubMed  Google Scholar 

  88. S. Flowers, G.R. Beck, E. Moran, Transcriptional activation by pRB and its coordination with SWI/SNF recruitment. Cancer Res. 70, 8282–8287 (2010)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  89. G. Kapatai, M.A. Brundler, H. Jenkinson, P. Kearns, M. Parulekar, A.C. Peet, C.M. McConville, Gene expression profiling identifies different sub-types of retinoblastoma. Br. J. Cancer 109, 512–525 (2013). doi:10.1038/bjc.2013.283

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  90. N. Erez, Cancer: opening LOX to metastasis. Nature (2015). doi:10.1038/nature14529

    PubMed  Google Scholar 

  91. F. Dillmann, M.R. Veldwijk, S. Laufs, M. Sperandio, G. Calandra, F. Wenz, W.J. Zeller, S. Fruehauf, F. Dillmann, M.R. Veldwijk, Plerixafor inhibits chemotaxis toward SDF-1 and CXCR4-mediated stroma contact in a dose-dependent manner resulting in increased susceptibility of BCR-ABL+ cell to Imatinib and Nilotinib. Leuk. Lymphoma 50, 1676–1686 (2009)

    Article  CAS  PubMed  Google Scholar 

  92. S. Stefanovic, F. Schuetz, C. Sohn, P. Beckhove, C. Domschke, Bone marrow microenvironment in cancer patients: immunological aspects and clinical implications. Cancer Metastasis Rev. 32, 163–178 (2013)

    Article  CAS  PubMed  Google Scholar 

  93. K. Grymula, M. Tarnowski, M. Wysoczynski, J. Drukala, F.G. Barr, J. Ratajczak, M. Kucia, M.Z. Ratajczak, Overlapping and distinct role of CXCR7-SDF-1/ITAC and CXCR4-SDF-1 axes in regulating metastatic behavior of human rhabdomyosarcomas. Int. J. Cancer 127, 2554–2568 (2010)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  94. J.-J. Zhao, J. Yang, J. Lin, N. Yao, Y. Zhu, J. Zheng, J. Xu, J.Q. Cheng, J.-Y. Lin, X. Ma, Identification of miRNAs associated with tumorigenesis of retinoblastoma by miRNA microarray analysis. Childs Nerv. Syst. 25, 13–20 (2009)

    Article  PubMed  Google Scholar 

  95. W. Tang, Y. Zhu, J. Gao, J. Fu, C. Liu, Y. Liu, C. Song, S. Zhu, Y. Leng, G. Wang, MicroRNA-29a promotes colorectal cancer metastasis by regulating matrix metalloproteinase 2 and E-cadherin via KLF4. Br. J. Cancer 110, 450–458 (2013)

    Article  PubMed Central  PubMed  Google Scholar 

  96. K. Conkrite, M. Sundby, S. Mukai, J.M. Thomson, D. Mu, S.M. Hammond, D. MacPherson, miR-17 ∼ 92 cooperates with RB pathway mutations to promote retinoblastoma. Genes Dev. 25, 1734–1745 (2011)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  97. Y. Fan, S. Yin, Y. Hao, J. Yang, H. Zhang, C. Sun, M. Ma, Q. Chang, J.J. Xi, miR-19b promotes tumor growth and metastasis via targeting TP53. RNA 20, 765–772 (2014)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  98. S. Lu, Q. Zhu, Y. Zhang, W. Song, M.J. Wilson, P. Liu, Dual‐functions of miR‐373 and miR‐520c by differently regulating the activities of MMP2 and MMP9. J. Cell. Physiol. 230, 1862–1870 (2015). doi:10.1002/jcp.24914

    Article  CAS  PubMed  Google Scholar 

  99. M.Y. Shah, G.A. Calin, MicroRNAs miR-221 and miR-222: a new level of regulation in aggressive breast cancer. Genome. Med. 3, 56 (2011)

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We appreciate the contributions of all our colleagues in the Health Research Institute, Research Center of Thalassemia & Hemoglobinopathy. We thank Dr. Courtney Schaal for her help in the writing and the proofreading of the manuscript.

Authors’ contributions

Najmaldin Saki conceived the manuscript and revised it. Abbas Khosravi, Saeid Shahrabi and Mohammad Shahjahani wrote the manuscript and prepared the figures and the table.

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Hematology, Allied Medical School, Tehran University of Medical Sciences, Tehran, Iran

    Abbas Khosravi

  2. Department of Biochemistry and Hematology, Faculty of Medicine, Semnan University of Medical Sciences, Semnan, Iran

    Saeid Shahrabi

  3. Health Research Institute, Research Center of Thalassemia & Hemoglobinopathy, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

    Mohammad Shahjahani & Najmaldin Saki

Authors
  1. Abbas Khosravi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saeid Shahrabi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohammad Shahjahani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Najmaldin Saki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Najmaldin Saki.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khosravi, A., Shahrabi, S., Shahjahani, M. et al. The bone marrow metastasis niche in retinoblastoma. Cell Oncol. 38, 253–263 (2015). https://doi.org/10.1007/s13402-015-0232-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13402-015-0232-x

Keywords

Search

Navigation