SSEA-1 Is an Enrichment Marker for Tumor-Initiating Cells in Human Glioblastoma

Cell Stem Cell

Volumn 4, Issue 5, 2009, Pages 440-452

  Son, Myung Jin ^a   Woolard, Kevin ^a   Nam, Do Hyun ^b   Lee, Jeongwu ^a   Fine, Howard A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b Sungkyunkwan University School of Medicine   (South Korea)

Author keywords

STEMCELL

Indexed keywords

STAGE SPECIFIC EMBRYO ANTIGEN 1; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CARCINOGENESIS; CELL CYCLE; CELL DIFFERENTIATION; CELL RENEWAL; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SCID MOUSE; TUMOR XENOGRAFT; WESTERN BLOTTING;

ANIMALS; ANTIGENS, CD15; CELL CYCLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; FEMALE; FLOW CYTOMETRY; GLIOBLASTOMA; HUMANS; MALE; MICE; MICE, SCID; NEOPLASTIC STEM CELLS; TUMOR CELLS, CULTURED;

EID: 65349115320     PISSN: 19345909     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stem.2009.03.003     Document Type: Article

References (53)

1. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., and Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444 (2006) 756-760
2. Bao S., Wu Q., Li Z., Sathornsumetee S., Wang H., McLendon R.E., Hjelmeland A.B., and Rich J.N. Targeting cancer stem cells through L1CAM suppresses glioma growth. Cancer Res. 68 (2008) 6043-6048
3. Beier D., Hau P., Proescholdt M., Lohmeier A., Wischhusen J., Oefner P.J., Aigner L., Brawanski A., Bogdahn U., and Beier C.P. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 67 (2007) 4010-4015
4. Bidlingmaier S., Zhu X., and Liu B. The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells. J. Mol. Med. 86 (2008) 1025-1032
5. Capela A., and Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35 (2002) 865-875
6. Capela A., and Temple S. LeX is expressed by principle progenitor cells in the embryonic nervous system, is secreted into their environment and binds Wnt-1. Dev. Biol. 291 (2006) 300-313
7. Chen H.L., Pistollato F., Hoeppner D.J., Ni H.T., McKay R.D., and Panchision D.M. Oxygen tension regulates survival and fate of mouse central nervous system precursors at multiple levels. Stem Cells 25 (2007) 2291-2301
8. Clarke M.F., Dick J.E., Dirks P.B., Eaves C.J., Jamieson C.H., Jones D.L., Visvader J., Weissman I.L., and Wahl G.M. Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 66 (2006) 9339-9344
9. Corbeil D., Roper K., Weigmann A., and Huttner W.B. AC133 hematopoietic stem cell antigen: human homologue of mouse kidney prominin or distinct member of a novel protein family?. Blood 91 (1998) 2625-2626
10. Coskun V., Wu H., Blanchi B., Tsao S., Kim K., Zhao J., Biancotti J.C., Hutnick L., Krueger Jr. R.C., Fan G., et al. CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc. Natl. Acad. Sci. USA 105 (2008) 1026-1031
11. Dalerba P., Dylla S.J., Park I.K., Liu R., Wang X., Cho R.W., Hoey T., Gurney A., Huang E.H., Simeone D.M., et al. Phenotypic characterization of human colorectal cancer stem cells. Proc. Natl. Acad. Sci. USA 104 (2007) 10158-10163
12. Dick J.E. Stem cell concepts renew cancer research. Blood 112 (2008) 4793-4807
13. Dirks P.B. Cancer: stem cells and brain tumours. Nature 444 (2006) 687-688
14. Galli R., Binda E., Orfanelli U., Cipelletti B., Gritti A., De Vitis S., Fiocco R., Foroni C., Dimeco F., and Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 64 (2004) 7011-7021
15. Griguer C.E., Oliva C.R., Gobin E., Marcorelles P., Benos D.J., Lancaster Jr. J.R., and Gillespie G.Y. CD133 is a marker of bioenergetic stress in human glioma. PLoS ONE 3 (2008) e3655 10.1371/journal.pone.0003655
16. Hall P.E., Lathia J.D., Miller N.G., Caldwell M.A., and ffrench-Constant C. Integrins are markers of human neural stem cells. Stem Cells 24 (2006) 2078-2084
17. Joo K.M., Kim S.Y., Jin X., Song S.Y., Kong D.S., Lee J.I., Jeon J.W., Kim M.H., Kang B.G., Jung Y., et al. Clinical and biological implications of CD133-positive and CD133-negative cells in glioblastomas. Lab Invest. 88 (2008) 808-815
18. Jordan C.T., Guzman M.L., and Noble M. Cancer stem cells. N. Engl. J. Med. 355 (2006) 1253-1261
19. Kelly P.N., Dakic A., Adams J.M., Nutt S.L., and Strasser A. Tumor growth need not be driven by rare cancer stem cells. Science 317 (2007) 337
20. Kim I., He S., Yilmaz O.H., Kiel M.J., and Morrison S.J. Enhanced purification of fetal liver hematopoietic stem cells using SLAM family receptors. Blood 108 (2006) 737-744
21. Kleihues P., Louis D.N., Scheithauer B.W., Rorke L.B., Reifenberger G., Burger P.C., and Cavenee W.K. The WHO classification of tumors of the nervous system. J. Neuropathol. Exp. Neurol. 61 (2002) 215-225
22. Lee J., Kotliarova S., Kotliarov Y., Li A., Su Q., Donin N.M., Pastorino S., Purow B.W., Christopher N., Zhang W., et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9 (2006) 391-403
23. Lee J., Son M.J., Woolard K., Donin N.M., Li A., Cheng C.H., Kotliarova S., Kotliarov Y., Walling J., Ahn S., et al. Epigenetic-mediated dysfunction of the bone morphogenetic protein pathway inhibits differentiation of glioblastoma-initiating cells. Cancer Cell 13 (2008) 69-80
24. Lendahl U., Zimmerman L.B., and McKay R.D. CNS stem cells express a new class of intermediate filament protein. Cell 60 (1990) 585-595
25. Lessard J., and Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 423 (2003) 255-260
26. Ligon K.L., Huillard E., Mehta S., Kesari S., Liu H., Alberta J.A., Bachoo R.M., Kane M., Louis D.N., Depinho R.A., et al. Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron 53 (2007) 503-517
27. Liu G., Yuan X., Zeng Z., Tunici P., Ng H., Abdulkadir I.R., Lu L., Irvin D., Black K.L., and Yu J.S. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol. Cancer 5 (2006) 67
28. Miraglia S., Godfrey W., Yin A.H., Atkins K., Warnke R., Holden J.T., Bray R.A., Waller E.K., and Buck D.W. A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood 90 (1997) 5013-5021
29. Mirzadeh Z., Merkle F.T., Soriano-Navarro M., Garcia-Verdugo J.M., and Alvarez-Buylla A. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3 (2008) 265-278
30. O'Brien C.A., Pollett A., Gallinger S., and Dick J.E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445 (2007) 106-110
31. Ogden A.T., Waziri A.E., Lochhead R.A., Fusco D., Lopez K., Ellis J.A., Kang J., Assanah M., McKhann G.M., Sisti M.B., et al. Identification of A2B5+CD133- tumor-initiating cells in adult human gliomas. Neurosurgery 62 (2008) 505-514
32. Patrawala L., Calhoun-Davis T., Schneider-Broussard R., and Tang D.G. Hierarchical organization of prostate cancer cells in xenograft tumors: the CD44+alpha2beta1+ cell population is enriched in tumor-initiating cells. Cancer Res. 67 (2007) 6796-6805
33. Pfenninger C.V., Roschupkina T., Hertwig F., Kottwitz D., Englund E., Bengzon J., Jacobsen S.E., and Nuber U.A. CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells. Cancer Res. 67 (2007) 5727-5736
34. Piccirillo S.G., Reynolds B.A., Zanetti N., Lamorte G., Binda E., Broggi G., Brem H., Olivi A., Dimeco F., and Vescovi A.L. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 444 (2006) 761-765
35. Potgens A.J., Schmitz U., Kaufmann P., and Frank H.G. Monoclonal antibody CD133-2 (AC141) against hematopoietic stem cell antigen CD133 shows crossreactivity with cytokeratin 18. J. Histochem. Cytochem. 50 (2002) 1131-1134
36. Quintana E., Shackleton M., Sabel M.S., Fullen D.R., Johnson T.M., and Morrison S.J. Efficient tumour formation by single human melanoma cells. Nature 456 (2008) 593-598
37. Read T.A., Fogarty M.P., Markant S.L., McLendon R.E., Wei Z., Ellison D.W., Febbo P.G., and Wechsler-Reya R.J. Identification of CD15 as a marker for tumor-propagating cells in a mouse model of medulloblastoma. Cancer Cell 15 (2009) 135-147
38. Reya T., Morrison S.J., Clarke M.F., and Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 414 (2001) 105-111
39. Ricci-Vitiani L., Lombardi D.G., Pilozzi E., Biffoni M., Todaro M., Peschle C., and De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature 445 (2007) 111-115
40. Richardson G.D., Robson C.N., Lang S.H., Neal D.E., Maitland N.J., and Collins A.T. CD133, a novel marker for human prostatic epithelial stem cells. J. Cell Sci. 117 (2004) 3539-3545
41. Shen X., Liu Y., Hsu Y.J., Fujiwara Y., Kim J., Mao X., Yuan G.C., and Orkin S.H. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol. Cell 32 (2008) 491-502
42. Sher F., Rossler R., Brouwer N., Balasubramaniyan V., Boddeke E., and Copray S. Differentiation of neural stem cells into oligodendrocytes: involvement of the polycomb group protein Ezh2. Stem Cells 26 (2008) 2875-2883
43. Shmelkov S.V., Butler J.M., Hooper A.T., Hormigo A., Kushner J., Milde T., St Clair R., Baljevic M., White I., Jin D.K., et al. CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J. Clin. Invest. 118 (2008) 2111-2120
44. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., and Dirks P.B. Identification of human brain tumour initiating cells. Nature 432 (2004) 396-401
45. Suh H., Consiglio A., Ray J., Sawai T., D'Amour K.A., and Gage F.H. In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell 1 (2007) 515-528
46. Trumpp A., and Wiestler O.D. Mechanisms of disease: cancer stem cells-targeting the evil twin. Nat. Clin. Pract. Oncol. 5 (2008) 337-347
47. Uchida N., Buck D.W., He D., Reitsma M.J., Masek M., Phan T.V., Tsukamoto A.S., Gage F.H., and Weissman I.L. Direct isolation of human central nervous system stem cells. Proc. Natl. Acad. Sci. USA 97 (2000) 14720-14725
48. Valk-Lingbeek M.E., Bruggeman S.W., and van Lohuizen M. Stem cells and cancer; the polycomb connection. Cell 118 (2004) 409-418
49. Vescovi A.L., Galli R., and Reynolds B.A. Brain tumour stem cells. Nat. Rev. Cancer 6 (2006) 425-436
50. Wang J., Sakariassen P.O., Tsinkalovsky O., Immervoll H., Boe S.O., Svendsen A., Prestegarden L., Rosland G., Thorsen F., Stuhr L., et al. CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int. J. Cancer 122 (2008) 761-768
51. Weissman I.L., Anderson D.J., and Gage F. Stem and progenitor cells: origins, phenotypes, lineage commitments, and transdifferentiations. Annu. Rev. Cell Dev. Biol. 17 (2001) 387-403
52. Yuan H., Corbi N., Basilico C., and Dailey L. Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev. 9 (1995) 2635-2645
53. Zhu L., Gibson P., Currle D.S., Tong Y., Richardson R.J., Bayazitov I.T., Poppleton H., Zakharenko S., Ellison D.W., and Gilbertson R.J. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature 457 (2009) 603-607