Skip to main content

Advertisement

SpringerLink
Log in

Multiple roles of CD90 in cancer

  • Review
  • Published:
Tumor Biology

Abstract

THY1 (CD90) is a 25–37-kDa heavily N-glycosylated, glycophosphatidylinositol (GPI) anchored cell surface protein. It is usually expressed on thymocytes, mesenchymal stem cells, hematopoietic stem cells, natural killer cells, neurons, endothelial cells, renal glomerular mesangial cells, follicular dendritic cells, fibroblasts, and myofibroblasts. It has been found to regulate cell adhesion, migration, apoptosis, axon growth, cell-cell and cell-matrix interactions, T-cell activation, and fibrosis. Several reports have shown that CD90 has an important role in cancer in regulating cancer cell proliferation, metastasis, and angiogenesis. There are also evidences that CD90 is an important prognostic marker in many cancers. Consequently, therapies that target CD90 have great promise in treating many cancers. However, several studies also indicate a contradictory role for CD90, where it acts as a tumor suppressor. In this review, we summarize the expression, function of CD90 in different cancers and its possible use as a biomarker or a therapeutic target in cancer. The challenges and future prospects for the use of CD90 for clinical applications are also discussed in this review.

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

Similar content being viewed by others

References

  1. Barron DA, Rowley DR. The reactive stroma microenvironment and prostate cancer progression. Endocr Relat Cancer. 2012;19:R187–204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Karagiannis GS, Poutahidis T, Erdman SE, Kirsch R, Riddell RH, Diamandis EP. Cancer-associated fibroblasts drive the progression of metastasis through both paracrine and mechanical pressure on cancer tissue. Mol Cancer Res. 2012;10:1403–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Pascal LE, Ai J, Vencio RZ, Vencio EF, Zhou Y, Page LS, et al. Differential inductive signaling of cd90 prostate cancer-associated fibroblasts compared to normal tissue stromal mesenchyme cells. Cancer Microenviron. 2011;4:51–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Pascal LE, Goo YA, Vencio RZN, Page LS, Chambers AA, Liebeskind ES, et al. Gene expression down-regulation in cd90(+) prostate tumor-associated stromal cells involves potential organ-specific genes. BMC Cancer. 2009;9.

  5. True LD, Zhang H, Ye ML, Huang CY, Nelson PS, von Haller PD, et al. Cd90/thy1 is overexpressed in prostate cancer-associated fibroblasts and could serve as a cancer biomarker. Mod Pathol. 2010;23:1346–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ungefroren H, Sebens S, Seidl D, Lehnert H, Hass R. Interaction of tumor cells with the microenvironment. Cell Commun Signal. 2011;9.

  7. Chen WC, Chang YS, Hsu HP, Yen MC, Huang HL, Cho CY, et al. Therapeutics targeting cd90-integrin-ampk-cd133 signal axis in liver cancer. Oncotarget. 2015;6:42923–37.

    PubMed  PubMed Central  Google Scholar 

  8. Ho DWY, Yang ZF, Yi K, Lam CT, Ng MNP, Yu WC, et al. Gene expression profiling of liver cancer stem cells by RNA-sequencing. PLoS One. 2012;7.

  9. Jiang J, Zhang Y, Chuai S, Wang Z, Zheng D, Xu F, et al. Trastuzumab (herceptin) targets gastric cancer stem cells characterized by cd90 phenotype. Oncogene. 2012;31:671–82.

    Article  CAS  PubMed  Google Scholar 

  10. Sukowati CH, Anfuso B, Torre G, Francalanci P, Croce LS, Tiribelli C. The expression of CD90/Thy-1 in hepatocellular carcinoma: an in vivo and in vitro study. PLoS One. 2013;8:e76830.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Tang KH, Dai YD, Tong M, Chan YP, Kwan PS, Fu L, et al. A CD90(+) tumor-initiating cell population with an aggressive signature and metastatic capacity in esophageal cancer. Cancer Res. 2013;73:2322–32.

    Article  CAS  PubMed  Google Scholar 

  12. Yan XP, Luo H, Zhou XD, Zhu BJ, Wang YL, Bian XW. Identification of CD90 as a marker for lung cancer stem cells in A549 and H446 cell lines. Oncol Rep. 2013;30:2733–40.

    CAS  PubMed  Google Scholar 

  13. Zhu L, Zhang W, Wang J, Liu R. Evidence of CD90+CXCR4+ cells as circulating tumor stem cells in hepatocellular carcinoma. Tumour Biol. 2015;36:5353–60.

    Article  CAS  PubMed  Google Scholar 

  14. Lobba ARM, Forni MF, Carreira ACO, Sogayar MC. Differential expression of CD90 and CD14 stem cell markers in malignant breast cancer cell lines. Cytometry Part A. 2012;81A:1084–91.

    Article  CAS  Google Scholar 

  15. Zhu J, Thakolwiboon S, Liu X, Zhang M, Lubman DM. Overexpression of CD90 (Thy-1) in pancreatic adenocarcinoma present in the tumor microenvironment. PLoS One. 2014;9:e115507.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Abeysinghe HR, Pollock SJ, Guckert NL, Veyberman Y, Keng P, Halterman M, et al. The role of the THY1 gene in human ovarian cancer suppression based on transfection studies. Cancer Genet Cytogenet. 2004;149:1–10.

    Article  CAS  PubMed  Google Scholar 

  17. Cheng Y, Stanbridge EJ, Kong H, Bengtsson U, Lerman MI, Lung ML. A functional investigation of tumor suppressor gene activities in a nasopharyngeal carcinoma cell line HONE1 using a monochromosome transfer approach. Genes Chromosomes Cancer. 2000;28:82–91.

    Article  CAS  PubMed  Google Scholar 

  18. Zeng L, Peng Z, Zhang M. Construction of THY1 eukaryotic expression plasmid and its effects on growth of ovarian cancer SKOV3 cells. Sheng Wu Yi Xue Gong Cheng Xue Za Zhi. 2009;26:620–4.

    CAS  PubMed  Google Scholar 

  19. Crawford JM, Barton RW. Thy-1 glycoprotein: structure, distribution, and ontogeny. Lab Invest. 1986;54:122–35.

    CAS  PubMed  Google Scholar 

  20. Seki T, Spurr N, Obata F, Goyert S, Goodfellow P, Silver J. The human Thy-1 gene: structure and chromosomal location. Proc Natl Acad Sci U S A. 1985;82:6657–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Williams AF, Gagnon J. Neuronal cell thy-1 glycoprotein: homology with immunoglobulin. Science. 1982;216:696–703.

    Article  CAS  PubMed  Google Scholar 

  22. Haeryfar SM, Hoskin DW. Thy-1: more than a mouse pan-T cell marker. J Immunol. 2004;173:3581–8.

    Article  CAS  PubMed  Google Scholar 

  23. Pont S. Thy-1: a lymphoid cell subset marker capable of delivering an activation signal to mouse T lymphocytes. Biochimie. 1987;69:315–20.

    Article  CAS  PubMed  Google Scholar 

  24. Barboni E, Rivero BP, George AJT, Martin SR, Renouf DV, Hounsell EF, et al. The glycophosphatidylinositol anchor affects the conformation of Thy-1 protein. J Cell Sci. 1995;108:487–97.

    CAS  PubMed  Google Scholar 

  25. Kukulansky T, Abramovitch S, Hollander N. Cleavage of the glycosylphosphatidylinositol anchor affects the reactivity of thy-1 with antibodies. J Immunol. 1999;162:5993–7.

    CAS  PubMed  Google Scholar 

  26. Mayeux-Portas V, File SE, Stewart CL, Morris RJ. Mice lacking the cell adhesion molecule Thy-1 fail to use socially transmitted cues to direct their choice of food. Curr Biol. 2000;10:68–75.

    Article  CAS  PubMed  Google Scholar 

  27. Beissert S, He HT, Hueber AO, Lellouch AC, Metze D, Mehling A, et al. Impaired cutaneous immune responses in Thy-1-deficient mice. J Immunol. 1998;161:5296–302.

    CAS  PubMed  Google Scholar 

  28. Simon PD, McConnell J, Zurakowski D, Vorwerk CK, Naskar R, Grosskreutz CL, et al. Thy-1 is critical for normal retinal development. Dev Brain Res. 1999;117:219–23.

    Article  CAS  Google Scholar 

  29. Hagood JS, Prabhakaran P, Kumbla P, Salazar L, MacEwen MW, Barker TH, et al. Loss of fibroblast Thy-1 expression correlates with lung fibrogenesis. Am J Pathol. 2005;167:365–79.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Craig W, Kay R, Cutler RL, Lansdorp PM. Expression of Thy-1 on human hematopoietic progenitor cells. J Exp Med. 1993;177:1331–42.

    Article  CAS  PubMed  Google Scholar 

  31. Killeen N. T-cell regulation: Thy-1—hiding in full view. Curr Biol. 1997;7:R774–7.

    Article  CAS  PubMed  Google Scholar 

  32. Saalbach A, Kraft R, Herrmann K, Haustein UF, Anderegg U. The monoclonal antibody AS02 recognizes a protein on human fibroblasts being highly homologous to Thy-1. Arch Dermatol Res. 1998;290:360–6.

    Article  CAS  PubMed  Google Scholar 

  33. Saalbach A, Wetzig T, Haustein UF, Anderegg U. Detection of human soluble Thy-1 in serum by ELISA. Fibroblasts and activated endothelial cells are a possible source of soluble Thy-1 in serum. Cell Tissue Res. 1999;298:307–15.

    Article  CAS  PubMed  Google Scholar 

  34. Seeger RC, Danon YL, Rayner SA, Hoover F. Definition of a Thy-1 determinant on human neuroblastoma, glioma, sarcoma, and teratoma cells with a monoclonal antibody. J Immunol. 1982;128:983–9.

    CAS  PubMed  Google Scholar 

  35. Gunter KC, Germain RN, Kroczek RA, Saito T, Yokoyama WM, Chan C, et al. Thy-1-mediated T-cell activation requires co-expression of CD3/Ti complex. Nature. 1987;326:505–7.

    Article  CAS  PubMed  Google Scholar 

  36. Dreyer EB, Leifer D, Heng JE, McConnell JE, Gorla M, Levin LA, et al. An astrocytic binding site for neuronal Thy-1 and its effect on neurite outgrowth. Proc Natl Acad Sci U S A. 1995;92:11195–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Herrera-Molina R, Frischknecht R, Maldonado H, Seidenbecher CI, Gundelfinger ED, Hetz C, et al. Astrocytic alphavbeta3 integrin inhibits neurite outgrowth and promotes retraction of neuronal processes by clustering Thy-1. PLoS One. 2012;7:e34295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Seki M, Nawa H, Morioka T, Fukuchi T, Oite T, Abe H, et al. Establishment of a novel enzyme-linked immunosorbent assay for Thy-1; quantitative assessment of neuronal degeneration. Neurosci Lett. 2002;329:185–8.

    Article  CAS  PubMed  Google Scholar 

  39. Fujita N, Kato Y, Naito M, Tsuruo T. A novel anti-Thy-1 (CD90) monoclonal antibody induces apoptosis in mouse malignant T-lymphoma cells in spite of inducing bcl-2 expression. Int J Cancer. 1996;66:544–50.

    Article  CAS  PubMed  Google Scholar 

  40. Fujita N, Kodama N, Kato Y, Lee SH, Tsuruo T. Aggregation of Thy-1 glycoprotein induces thymocyte apoptosis through activation of CPP32-like proteases. Exp Cell Res. 1997;232:400–6.

    Article  CAS  PubMed  Google Scholar 

  41. Hueber AO, Raposo G, Pierres M, He HT. Thy-1 triggers mouse thymocyte apoptosis through a bcl-2-resistant mechanism. J Exp Med. 1994;179:785–96.

    Article  CAS  PubMed  Google Scholar 

  42. Narisawa-Saito M, Kimura S, Fujiwara N, Oite T, Shimoji K, Shimizu F. Thy-1-mediated phosphatidylinositol turnover in cultured rat glomerular mesangial cell. J Cell Physiol. 1996;168:705–10.

    Article  CAS  PubMed  Google Scholar 

  43. Sato T, van Dixhoorn MG, Schroeijers WE, van Es LA, Daha MR. Efficient induction of apoptosis in cultured rat glomerular mesangial cells by dimeric monoclonal IgA anti-Thy-1 antibodies. Kidney Int. 1997;51:173–81.

    Article  CAS  PubMed  Google Scholar 

  44. Rege TA, Hagood JS. Thy-1 as a regulator of cell-cell and cell-matrix interactions in axon regeneration, apoptosis, adhesion, migration, cancer, and fibrosis. FASEB J. 2006;20:1045–54.

    Article  CAS  PubMed  Google Scholar 

  45. Rege TA, Hagood JS. Thy-1, a versatile modulator of signaling affecting cellular adhesion, proliferation, survival, and cytokine/growth factor responses. Biochim Biophys Acta. 1763;2006:991–9.

    Google Scholar 

  46. Saalbach A, Haustein UF, Anderegg U. A ligand of human Thy-1 is localized on polymorphonuclear leukocytes and monocytes and mediates the binding to activated Thy-1-positive microvascular endothelial cells and fibroblasts. J Invest Dermatol. 2000;115:882–8.

    Article  CAS  PubMed  Google Scholar 

  47. Saalbach A, Hildebrandt G, Haustein UF, Anderegg U. The Thy-1/Thy-1 ligand interaction is involved in binding of melanoma cells to activated Thy-1-positive microvascular endothelial cells. Microvasc Res. 2002;64:86–93.

    Article  CAS  PubMed  Google Scholar 

  48. Rege TA, Pallero MA, Gomez C, Grenett HE, Murphy-Ullrich JE, Hagood JS. Thy-1, via its GPI anchor, modulates Src family kinase and focal adhesion kinase phosphorylation and subcellular localization, and fibroblast migration, in response to thrombospondin-1/hep I. Exp Cell Res. 2006;312:3752–67.

    Article  CAS  PubMed  Google Scholar 

  49. Barker TH, Hagood JS. Getting a grip on Thy-1 signaling. Biochim Biophys Acta. 1793;2009:921–3.

    Google Scholar 

  50. Gabra H, Watson JE, Taylor KJ, Mackay J, Leonard RC, Steel CM, et al. Definition and refinement of a region of loss of heterozygosity at 11q23.3–q24.3 in epithelial ovarian cancer associated with poor prognosis. Cancer Res. 1996;56:950–4.

    CAS  PubMed  Google Scholar 

  51. Abeysinghe HR, Cao Q, Xu J, Pollock S, Veyberman Y, Guckert NL, et al. Thy1 expression is associated with tumor suppression of human ovarian cancer. Cancer Genet Cytogenet. 2003;143:125–32.

    Article  CAS  PubMed  Google Scholar 

  52. Cao Q, Abeysinghe H, Chow O, Xu J, Kaung HL, Fong CT, et al. Suppression of tumorigenicity in human ovarian carcinoma cell line SKOV-3 by microcell-mediated transfer of chromosome 11. Cancer Genet Cytogenet. 2001;129:131–7.

    Article  CAS  PubMed  Google Scholar 

  53. Abeysinghe HR, Li LQ, Guckert NL, Reeder J, Wang N. Thy-1 induction is associated with up-regulation of fibronectin and thrombospondin-1 in human ovarian cancer. Cancer Genet Cytogenet. 2005;161:151–8.

    Article  CAS  PubMed  Google Scholar 

  54. Akiyama SK, Olden K, Yamada KM. Fibronectin and integrins in invasion and metastasis. Cancer Metastasis Rev. 1995;14:173–89.

    Article  CAS  PubMed  Google Scholar 

  55. Hsu SC, Volpert OV, Steck PA, Mikkelsen T, Polverini PJ, Rao S, et al. Inhibition of angiogenesis in human glioblastomas by chromosome 10 induction of thrombospondin-1. Cancer Res. 1996;56:5684–91.

    CAS  PubMed  Google Scholar 

  56. Zeng LQ, Peng ZL, Duan ZL. Expression of THY1 gene in epithelial ovarian cancer. Zhonghua Zhong Liu Za Zhi. 2009;31:118–20.

    CAS  PubMed  Google Scholar 

  57. Hui AB, Lo KW, Leung SF, Choi PH, Fong Y, Lee JC, et al. Loss of heterozygosity on the long arm of chromosome 11 in nasopharyngeal carcinoma. Cancer Res. 1996;56:3225–9.

    CAS  PubMed  Google Scholar 

  58. Mutirangura A, Tanunyutthawongese C, Pornthanakasem W, Kerekhanjanarong V, Sriuranpong V, Yenrudi S, et al. Genomic alterations in nasopharyngeal carcinoma: loss of heterozygosity and Epstein-Barr virus infection. Br J Cancer. 1997;76:770–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Lung HL, Bangarusamy DK, Xie D, Cheung AKL, Cheng Y, Kumaran MK, et al. Thy1 is a candidate tumour suppressor gene with decreased expression in metastatic nasopharyngeal carcinoma. Oncogene. 2005;24:6525–32.

    CAS  PubMed  Google Scholar 

  60. Lung HL, Cheung AKL, Cheng Y, Kwong FM, Lo PHY, Law EWL, et al. Functional characterization of THY1 as a tumor suppressor gene with antiinvasive activity in nasopharyngeal carcinoma. Int J Cancer. 2010;127:304–12.

    CAS  PubMed  Google Scholar 

  61. Weinstein JL, Katzenstein HM, Cohn SL. Advances in the diagnosis and treatment of neuroblastoma. Oncologist. 2003;8:278–92.

    Article  PubMed  Google Scholar 

  62. Fiegel HC, Kaifi JT, Quaas A, Varol E, Krickhahn A, Metzger R, et al. Lack of Thy1 (CD90) expression in neuroblastomas is correlated with impaired survival. Pediatr Surg Int. 2008;24:101–5.

    Article  PubMed  Google Scholar 

  63. Piper DR, Mujtaba T, Keyoung H, Roy NS, Goldman SA, Rao MS, et al. Identification and characterization of neuronal precursors and their progeny from human fetal tissue. J Neurosci Res. 2001;66:356–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Uchida N, Buck DW, He DP, Reitsma MJ, Masek M, Phan TV, et al. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci U S A. 2000;97:14720–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Nava S, Westgren M, Jaksch M, Tibell A, Broome U, Ericzon BG, et al. Characterization of cells in the developing human liver. Differentiation. 2005;73:249–60.

    Article  CAS  PubMed  Google Scholar 

  66. Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, Ngai P, et al. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell. 2008;13:153–66.

    Article  CAS  PubMed  Google Scholar 

  67. Ceafalan L, Vidulescu C, Radu E, Regalia T, Popescu I, Pana M, et al. Expression of stem cell markers on fetal and tumoral human liver cells in primary culture. Rev Med Chir Soc Med Nat Iasi. 2005;109:96–104.

    CAS  PubMed  Google Scholar 

  68. Cheng BQ, Jiang Y, Li DL, Fan JJ, Ma M. Up-regulation of Thy-1 promotes invasion and metastasis of hepatocarcinomas. Asian Pac J Cancer Prev. 2012;13:1349–53.

    Article  PubMed  Google Scholar 

  69. Lingala S, Cui YY, Chen XL, Ruebner BH, Qian XF, Zern MA, et al. Immunohistochemical staining of cancer stem cell markers in hepatocellular carcinoma. Exp Mol Pathol. 2010;89:27–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Lu JW, Chang JG, Yeh KT, Chen RM, Tsai JJP, Hu RM. Overexpression of Thy1/CD90 in human hepatocellular carcinoma is associated with HBV infection and poor prognosis. Acta Histochem. 2011;113:833–8.

    Article  CAS  PubMed  Google Scholar 

  71. Yu XH, Xu LB, Liu C, Zhang R, Wang J. Clinicopathological characteristics of 20 cases of hepatocellular carcinoma with bile duct tumor thrombi. Dig Dis Sci. 2011;56:252–9.

    Article  PubMed  Google Scholar 

  72. Yamashita T, Honda M, Nakamoto Y, Baba M, Nio K, Hara Y, et al. Discrete nature of EpCAM+ and CD90+cancer stem cells in human hepatocellular carcinoma. Hepatology. 2013;57:1484–97.

    Article  CAS  PubMed  Google Scholar 

  73. Yang ZF, Ngai P, Ho DW, Yu WC, Ng MNP, Lau CK, et al. Identification of local and circulating cancer stem cells in human liver cancer. Hepatology. 2008;47:919–28.

    Article  CAS  PubMed  Google Scholar 

  74. Cheng BQ, Jiang Y, Zhu Q, Lin WG. Wnt/beta-catenin aids in regulating the proliferation of hepG2 cells mediated by thy-1. Genet Mol Res. 2014;13:5115–27.

    Article  CAS  PubMed  Google Scholar 

  75. Jia Q, Zhang XL, Deng T, Gao J. Positive correlation of Oct4 and ABCG2 to chemotherapeutic resistance in CD90(+)CD133(+) liver cancer stem cells. Cell Reprogram. 2013;15:143–50.

    CAS  PubMed  Google Scholar 

  76. Bahnassy AA, Fawzy M, El-Wakil M, Zekri AR, Abdel-Sayed A, Sheta M. Aberrant expression of cancer stem cell markers (CD44, CD90, and CD133) contributes to disease progression and reduced survival in hepatoblastoma patients: 4-year survival data. Transl Res. 2014;165:396–406.

    Article  PubMed  CAS  Google Scholar 

  77. Furlan A, Vercamer C, Desbiens X, Pourtier A. Ets-1 triggers and orchestrates the malignant phenotype of mammary cancer cells within their matrix environment. J Cell Physiol. 2008;215:782–93.

    Article  CAS  PubMed  Google Scholar 

  78. Taki M, Verschueren K, Yokoyama K, Nagayama M, Kamata N. Involvement of Ets-1 transcription factor in inducing matrix metalloproteinase-2 expression by epithelial-mesenchymal transition in human squamous carcinoma cells. Int J Oncol. 2006;28:487–96.

    CAS  PubMed  Google Scholar 

  79. Chen JF, Zhang LJ, Zhao AL, Wang Y, Wu N, Xiong HC, et al. [Abnormal expression of Thy-1 as a novel tumor marker in lung cancer and its prognostic significance]. Zhonghua Yi Xue Za Zhi. 2005;85:1921–5.

    CAS  PubMed  Google Scholar 

  80. Jacob M, Male H, Diaz E, Huang C, Farassati F. CD90 (thy1) as a potential cancer stem cell markers and therapeutic target in non-small cell lung cancer. http://wwwatsjournalsorg/doi/abs/101164/ajrccm-conference20111831_MeetingAbstractsA5070 2011

  81. Hong X, Chedid K, Kalkanis SN. Glioblastoma cell line-derived spheres in serum-containing medium versus serum-free medium: a comparison of cancer stem cell properties. Int J Oncol. 2012;41:1693–700.

    CAS  PubMed  Google Scholar 

  82. Chen YC, Hsu HS, Chen YW, Tsai TH, How CK, Wang CY, et al. Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS One. 2008;3.

  83. Xiang R, Liao D, Cheng T, Zhou H, Shi Q, Chuang TS, et al. Downregulation of transcription factor SOX2 in cancer stem cells suppresses growth and metastasis of lung cancer. Br J Cancer. 2011;104:1410–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Kawamura K, Hiroshima K, Suzuki T, Chai K, Yamaguchi N, Shingyoji M, et al. CD90 is a diagnostic marker to differentiate between malignant pleural mesothelioma and lung carcinoma with immunohistochemistry. Am J Clin Pathol. 2013;140:544–9.

    Article  PubMed  Google Scholar 

  85. Ziegler A, Cerciello F, Bigosch C, Bausch-Fluck D, Felley-Bosco E, Ossola R, et al. Proteomic surfaceome analysis of mesothelioma. Lung Cancer. 2012;75:189–96.

    Article  PubMed  Google Scholar 

  86. Melotti A, Daga A, Marubbi D, Zunino A, Mutti L, Corte G. In vitro and in vivo characterization of highly purified human mesothelioma derived cells. BMC Cancer. 2010;10.

  87. Frei C, Opitz I, Soltermann A, Fischer B, Moura U, Rehrauer H, et al. Pleural mesothelioma side populations have a precursor phenotype. Carcinogenesis. 2011;32:1324–32.

    Article  CAS  PubMed  Google Scholar 

  88. He JT, Liu YS, Zhu T, Zhu JH, DiMeco F, Vescovi AL, et al. CD90 is identified as a candidate marker for cancer stem cells in primary high-grade gliomas using tissue microarrays. Mol Cell Proteomics. 2012;11.

  89. Parry PV, Engh JA. CD90 is identified as a marker for cancer stem cells in high-grade gliomas using tissue microarrays. Neurosurgery. 2012;70:N23–4.

    Article  PubMed  Google Scholar 

  90. He J, Liu Y, Zhu T, Zhu J, Dimeco F, Vescovi AL, et al. CD90 is identified as a candidate marker for cancer stem cells in primary high-grade gliomas using tissue microarrays. Mol Cell Proteomics. 2011;11:M111 010744.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Woo SR, Oh YT, An JY, Kang BG, Nam DH, Joo KM. Glioblastoma specific antigens, GD2 and CD90, are not involved in cancer stemness. Anat Cell Biol. 2015;48:44–53.

    Article  PubMed  PubMed Central  Google Scholar 

  92. Scognamiglio G, D’Antonio A, Rossi G, Cavazza A, Camerlingo R, Pirozzi G, et al. CD90 expression in atypical meningiomas and meningioma metastasis. Am J Clin Pathol. 2014;141:841–9.

    Article  PubMed  Google Scholar 

  93. Fabi A, Nuzzo C, Vidiri A, Ciccarese M, Felici A, Cattani F, et al. Bone and lung metastases from intracranial meningioma. Anticancer Res. 2006;26:3835–7.

    PubMed  Google Scholar 

  94. Notta F, Doulatov S, Laurenti E, Poeppl A, Jurisica I, Dick JE. Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment. Science. 2011;333:218–21.

    Article  CAS  PubMed  Google Scholar 

  95. Kozii R, Wilson J, Persichetti J, Phelps V, Ball SEB, Ball ED. Thy-1 expression on blast cells from adult patients with acute myeloid leukemia. Leuk Res. 1997;21:381–5.

    Article  CAS  PubMed  Google Scholar 

  96. Campos L, Guyotat D. Expression of Thy-1 antigen (CDw90) on adult acute leukemia blast cells. Blood. 1996;87:413–4.

    CAS  PubMed  Google Scholar 

  97. Petrovici K, Graf M, Reif S, Hecht K, Schmetzer H. Expression profile of the progenitor cell markers CD34, CD38 and CD90 in acute myeloid leukemia and their prognostic significance. J Cancer Mol. 2010;5:79–86.

    CAS  Google Scholar 

  98. Buccisano F, Rossi FM, Venditti A, Del Poeta G, Cox MC, Abbruzzese E, et al. CD90/Thy-1 is preferentially expressed on blast cells of high risk acute myeloid leukaemias. Br J Haematol. 2004;125:203–12.

    Article  CAS  PubMed  Google Scholar 

  99. Blair A, Hogge DE, Ailles LE, Lansdorp PM, Sutherland HJ. Lack of expression of Thy-1 (CD90) on acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo. Blood. 1997;89:3104–12.

    CAS  PubMed  Google Scholar 

  100. Cascavilla N, Melillo L, D’Arena G, Greco MM, Carella AM, Sajeva MR, et al. Minimally differentiated acute myeloid leukemia (AML M0): clinico-biological findings of 29 cases. Leuk Lymphoma. 2000;37:105–13.

    Article  CAS  PubMed  Google Scholar 

  101. Dohner K, Brown J, Hehmann U, Hetzel C, Stewart J, Lowther G, et al. Molecular cytogenetic characterization of a critical region in bands 7q35–q36 commonly deleted in malignant myeloid disorders. Blood. 1998;92:4031–5.

    CAS  PubMed  Google Scholar 

  102. Holden JT, Geller RB, Farhi DC, Holland HK, Stempora LL, Phillips CN, et al. Characterization of Thy-1 (CDw90) expression in CD34(+) acute-leukemia. Blood. 1995;86:60–5.

    CAS  PubMed  Google Scholar 

  103. Wuchter C, Ratei R, Spahn G, Schoch C, Harbott J, Schnittger S, et al. Impact of CD133 (AC133) and CD90 expression analysis for acute leukemia immunophenotyping. Haematologica. 2001;86:154–61.

    CAS  PubMed  Google Scholar 

  104. Inaba T, Shimazaki C, Sumikuma T, Shimura K, Takahashi R, Hirai H, et al. Flow cytometric analysis of Thy-1 expression in myelodysplastic syndrome. Int J Hematol. 1998;68:403–10.

    Article  CAS  PubMed  Google Scholar 

  105. Will B, Zhou L, Vogler TO, Ben-Neriah S, Schinke C, Tamari R, et al. Stem and progenitor cells in myelodysplastic syndromes show aberrant stage-specific expansion and harbor genetic and epigenetic alterations. Blood. 2012;120:2076–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Takahashi T, Mizutani M, Miwa H, Katayama N, Nishii K, Shikami M, et al. Frequent expression of human Thy-1 antigen on pre-b cell acute lymphoblastic leukemia with t(9;22). Int J Hematol. 1998;67:369–78.

    Article  CAS  PubMed  Google Scholar 

  107. Ishiura Y, Kotani N, Yamashita R, Yamamoto H, Kozutsumi Y, Honke K. Anomalous expression of Thy1 (CD90) in B-cell lymphoma cells and proliferation inhibition by anti-Thy1 antibody treatment. Biochem Biophys Res Commun. 2010;396:329–34.

    Article  CAS  PubMed  Google Scholar 

  108. Yamazaki H, Nishida H, Iwata S, Dang NH, Morimoto C. CD90 and CD110 correlate with cancer stem cell potentials in human T-acute lymphoblastic leukemia cells. Biochem Biophys Res Commun. 2009;383:172–7.

    Article  CAS  PubMed  Google Scholar 

  109. Wang X, Liu Y, Zhou K, Zhang G, Wang F, Ren J. Isolation and characterization of CD105+/CD90+ subpopulation in breast cancer MDA-MB-231 cell line. Int J Clin Exp Pathol. 2015;8:5105–12.

    PubMed  PubMed Central  Google Scholar 

  110. Donnenberg VS, Donnenberg AD, Zimmerlin L, Landreneau RJ, Bhargava R, Wetzel RA, et al. Localization of CD44 and CD90 positive cells to the invasive front of breast tumors. Cytometry Part B-Clinical Cytometry. 2010;78B:287–301.

    Article  CAS  Google Scholar 

  111. Johansson I, Ringner M, Hedenfalk I. The landscape of candidate driver genes differs between male and female breast cancer. PLoS One. 2013;8.

  112. Jurisic G, Iolyeva M, Proulx ST, Halin C, Detmar M. Thymus cell antigen 1 (Thy1, CD90) is expressed by lymphatic vessels and mediates cell adhesion to lymphatic endothelium. Exp Cell Res. 2010;316:2982–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Schubert K, Gutknecht D, Koberle M, Anderegg U, Saalbach A. Melanoma cells use Thy-1 (CD90) on endothelial cells for metastasis formation. Am J Pathol. 2013;182:266–76.

    Article  CAS  PubMed  Google Scholar 

  114. Ishizu A, Ishikura H, Nakamaru Y, Kikuchi K, Koike T, Yoshiki T. Interleukin-1alpha regulates Thy-1 expression on rat vascular endothelial cells. Microvasc Res. 1997;53:73–8.

    Article  CAS  PubMed  Google Scholar 

  115. Ishizu A, Ishikura H, Nakamaru Y, Takeuchi E, Kimura C, Koike T, et al. Thy-1 induced on rat endothelium regulates vascular permeability at sites of inflammation. Int Immunol. 1995;7:1939–47.

    Article  CAS  PubMed  Google Scholar 

  116. Leyton L, Schneider P, Labra CV, Ruegg C, Hetz CA, Quest AF, et al. Thy-1 binds to integrin beta(3) on astrocytes and triggers formation of focal contact sites. Curr Biol. 2001;11:1028–38.

    Article  CAS  PubMed  Google Scholar 

  117. Saalbach A, Wetzel A, Haustein UF, Sticherling M, Simon JC, Anderegg U. Interaction of human Thy-1 (CD90) with the integrin alphavbeta3 (CD51/CD61): an important mechanism mediating melanoma cell adhesion to activated endothelium. Oncogene. 2005;24:4710–20.

    Article  CAS  PubMed  Google Scholar 

  118. Zhao HJ, Peehl DM. Tumor-promoting phenotype of CD90(hi) prostate cancer-associated fibroblasts. Prostate. 2009;69:991–1000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Tiveron MC, Nosten-Bertrand M, Jani H, Garnett D, Hirst EM, Grosveld F, et al. The mode of anchorage to the cell surface determines both the function and the membrane location of Thy-1 glycoprotein. J Cell Sci. 1994;107(Pt 7):1783–96.

    CAS  PubMed  Google Scholar 

  120. Narisawa-Saito M, Yamanashi Y, Morioka T, Oite T, Shimizu F. Thy-1 molecule associates with protein tyrosine kinase(s) in rat mesangial cells. Clin Exp Immunol. 1996;106:86–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Thomas PM, Samelson LE. The glycophosphatidylinositol-anchored Thy-1 molecule interacts with the p60fyn protein tyrosine kinase in T cells. J Biol Chem. 1992;267:12317–22.

    CAS  PubMed  Google Scholar 

  122. Haeryfar SM, Hoskin DW. Selective pharmacological inhibitors reveal differences between Thy-1- and T cell receptor-mediated signal transduction in mouse T lymphocytes. Int Immunopharmacol. 2001;1:689–98.

    Article  CAS  PubMed  Google Scholar 

  123. Koumas L, Phipps RP. Differential COX localization and pg release in Thy-1(+) and Thy-1(−) human female reproductive tract fibroblasts. Am J Physiol Cell Physiol. 2002;283:C599–608.

    Article  CAS  PubMed  Google Scholar 

  124. Ramakrishnan S, Houston LL. Prevention of growth of leukemia-cells in mice by monoclonal-antibodies directed against Thy-1.1 antigen disulfide linked to 2 ribosomal inhibitors—pokeweed antiviral protein or ricin-A chain. Cancer Res. 1984;44:1398–404.

    CAS  PubMed  Google Scholar 

  125. Colombatti M, Colombatti A, Blythman HE, Bron C. Thy 1.2+ leukemia-cells eradicated from in vitro leukemia-bone marrow cell mixtures by antibody-toxin conjugates. J Natl Cancer Inst. 1984;72:1095–9.

    CAS  PubMed  Google Scholar 

  126. Badger CC, Krohn KA, Peterson AV, Shulman H, Bernstein ID. Experimental radiotherapy of murine lymphoma with I-131-labeled anti-Thy 1.1 monoclonal-antibody. Cancer Res. 1985;45:1536–44.

    CAS  PubMed  Google Scholar 

  127. Cheng R, Weissman I, Jones P: Characterization of CD90 as a therapeutic antibody target on cancer stem cells. Stanford Digital Repository 2015

  128. Qu Z, Goldenberg DM, Cardillo TM, Shi V, Hansen HJ, Chang CH. Bispecific anti-CD20/22 antibodies inhibit B-cell lymphoma proliferation by a unique mechanism of action. Blood. 2008;111:2211–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Vidal M, Morris R, Grosveld F, Spanopoulou E. Tissue-specific control elements of the Thy-1 gene. EMBO J. 1990;9:833–40.

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Bradley JS, Ramirez G, Hagood JS. Roles and regulation of Thy-1, a context-dependent modulator of cell phenotype. Biofactors. 2009;35:258–65.

    Article  CAS  PubMed  Google Scholar 

  131. Jaganathan BG, Tisato V, Vulliamy T, Dokal I, Marsh J, Dazzi F, et al. Effects of MSC co-injection on the reconstitution of aplastic anemia patient following hematopoietic stem cell transplantation. Leukemia. 2010;24:1791–5.

    Article  CAS  PubMed  Google Scholar 

  132. Almqvist P, Carlsson SR. Characterization of a hydrophilic form of Thy-1 purified from human cerebrospinal fluid. J Biol Chem. 1988;263:12709–15.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

AK is supported by fellowship from MHRD (Ministry of Human Resource and Development), Govt. of India.

Authors’ contributions

AK, AB, JB, and BGJ wrote the manuscript and approved the final version of the manuscript.

Author information

Author notes

    Authors and Affiliations

    1. Stem Cell and Cancer Biology Group, Department of Biosciences and Bioengineering, Indian Institute of Technology Guwahati, Guwahati, Assam, India

      Atul Kumar, Anshuman Bhanja & Bithiah Grace Jaganathan

    2. Department of Hematology, Gauhati Medical College Hospital, Guwahati, Assam, India

      Jina Bhattacharyya

    Authors
    1. Atul Kumar
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Anshuman Bhanja
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Jina Bhattacharyya
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Bithiah Grace Jaganathan
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Bithiah Grace Jaganathan.

    Ethics declarations

    Conflicts of interest

    None

    Additional information

    Atul Kumar and Anshuman Bhanja contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Kumar, A., Bhanja, A., Bhattacharyya, J. et al. Multiple roles of CD90 in cancer. Tumor Biol. 37, 11611–11622 (2016). https://doi.org/10.1007/s13277-016-5112-0

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s13277-016-5112-0

    Keywords

    Search

    Navigation