CD133/CD15 defines distinct cell subpopulations with differential in vitro clonogenic activity and stem cell-related gene expression profile in in vitro propagated glioblastoma multiforme-derived cell line with a PNET-like component

Folia Neuropathologica

Volumn 50, Issue 4, 2012, Pages 357-368

  Kahlert, Ulf D ^a   Bender, Noemi O ^b   Maciaczyk, Donata ^a   Bogiel, Tomasz ^a,c   Bar, Eli E ^d   Eberhart, Charles G ^e   Nikkhah, Guido ^a   Maciaczyk, Jaroslaw ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c Military Clinical Hospital Bydgoszcz   (Poland)

^d CASE WESTERN RESERVE UNIVERSITY   (United States)

^e DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

Brain tumour stem like cell; CD133; Clonogenicity; GBM; PNET

Indexed keywords

CD133 ANTIGEN; CD15 ANTIGEN; CELL SURFACE MARKER; MESSENGER RNA; NESTIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

AGED; ARTICLE; CANCER STEM CELL; CARCINOGENICITY; CELL FRACTIONATION; CELL HETEROGENEITY; CELL SUBPOPULATION; CLONOGENESIS; CLONOGENIC ASSAY; GENE EXPRESSION; GENETIC DIFFERENCE; GIANT CELL; GLIOBLASTOMA; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO PROPAGATION; IN VITRO STUDY; MALE; NEUROECTODERM TUMOR; PARIETAL LOBE; PRIMARY TUMOR; PROTEIN EXPRESSION;

EID: 84873396727     PISSN: 16414640     EISSN: 1509572X     Source Type: Journal    
DOI: 10.5114/fn.2012.32365     Document Type: Article

References (50)

1. Ahn SM, Byun K, Kim D, Lee K, Yoo JS, Kim SU, Jho EH, Simpson RJ, Lee B. Olig2-induced neural stem cell differentiation involves down regulation of Wnt signaling and induction of Dickkopf-1 expression. PloS One 2008; 3: e3917.
2. Albayrak BS, Ismailoglu O, Tanriover G, Cetinalp EN, Demir N. The double immunostaining of CD133 and Ki-67 favours a significant co-localization pattern in fibroblastic subtype of meningiomas. Neurol Neurochir Pol 2011; 45: 467-473.
3. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. Glioma stem cells promote radio-resistance by preferential activation of the DNA damage response. Nature 2006; 444: 756-760.
4. Bar EE, Chaudhry A, Lin A, Fan X, Schreck K, Matsui W, Picci rillo S, Vescovi AL, DiMeco F, Olivi A, Eberhart CG. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells 2007; 25: 2524-2533.
5. Bar EE, Lin A, Mahairaki V, Matsui W, Eberhart CG. Hypoxia increases the expression of stem-cell markers and promotes clonogenicity in glioblastoma neurospheres. Am J Pathol 2010; 177: 1491-1502.
6. Beier D, Hau P, Proescholdt M, Lohmeier A, Wischhusen J, Oefner PJ, Aigner L, Brawanski A, Bogdahn U, Beier C P. CD133+ and CD133-Glioblastoma- Derived Cancer Stem Cells Show Differential Growth Characteristics and Molecular Profiles. Cancer Res 2007; 67: 4010-4015.
7. Bleau AM, Huse JT, Holland EC. The ABCG2 resistance network of glioblastoma. Cell Cycle 2009; 8: 2936-2944.
8. Chambers SM, Studer L. Cell fate plug and play: direct reprogramming and induced pluripotency. Cell 2011; 145: 827-830.
9. Chen J, McKay RM, Parada L F. Malignant glioma: lessons from genomics, mouse models, and stem cells. Cell 2012; 149: 36-47.
10. Chen R, Nishimura MC, Bumbaca SM, Kharbanda S, Forrest WF, Kasman IM, Greve JM, Soriano RH, Gilmour LL, Rivers CS, Modru san Z, Nacu S, Guerrero S, Edgar KA, Wallin JJ, Lamszus K, Westphal M, Heim S, James CD, VandenBerg SR, Costello JF, Moore field S, Cowdrey CJ, Prados M, Phillips HS et al. 2010. A hierarchy of self-renewing tumor-initiating cell types in glioblastoma. Cancer Cell 2010; 17: 362-375.
11. Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz i Altaba A. HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol 2007; 17: 165-172.
12. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006; 127: 469-480.
13. Delamarre E, Taboubi S, Mathieu S, Bérenguer C, Rigot V, Lissitzky JC, Figarella-Branger D, Ouafik L, Luis J. Expression of integrin alpha6beta1 enhances tumorigenesis in glioma cells. Am J Pathol 2009; 175: 844-855.
14. Fan X, Khaki L, Zhu TS, Soules ME, Talsma CE, Gul N, Koh C, Zhang J, Li YM, Maciaczyk J, Nikkhah G, Dimeco F, Piccirillo S, Vesco vi AL, Eberhart CG. NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neu-rospheres and xenografts. Stem Cells 2010; 28: 5-16.
15. Fan X, Matsui W, Khaki L, Stearns D, Chun J, Li Y-M, Eberhart CG. Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res 2006; 66: 7445-7452.
16. Gingras MC, Roussel E, Bruner JM, Branch CD, Moser R P. Comparison of cell adhesion molecule expression between glioblastoma multiforme and autologous normal brain tissue. J Neuroimmunol 1995; 57: 143-153.
17. Gustafsson MV, Zheng X, Pereira T, Gradin K, Jin S, Lundkvist J, Ruas JL, Poellinger L, Lendah, U, Bondesson M. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 2005; 9: 617-628.
18. Hall PE, Lathia JD, Miller NGA, Caldwell MA, Ffrench-Constant C. Integrins are markers of human neural stem cells. Stem Cells 2006; 24: 2078-2084.
19. Ishizawa K, Kan-nuki S, Kumaga H, Komori T, Hirose T. Lipomatous primitive neuroectodermal tumor with a glioblastoma component: a case report. Acta neuropathol 2002; 103: 193-198.
20. Jamal M, Rath BH, Tsang PS, Camphausen K, Tofilon PJ. The brain microenvironment preferentially enhances the radioresistance of CD133(+) glioblastoma stem-like cells. Neoplasia 2012; 14: 150-158.
21. Joo KM, Kim SY, Jin X, Song SY, Kong DS, Lee JI, Jeon JW, Kim MH, Kang BG, Jung Y, Jin J, Hong SC, Park WY, Lee DS, Kim H, Nam DH. Clinical and biological implications of CD133-positive and CD133-negative cells in glioblastomas. Lab Invest 2008; 88: 808-815.
22. Kahlert U, Maciaczyk D, Doostkam S, Orr BA, Simons B, Bogiel T, Reithmeier T, Prinz M, Schubert J, Niedermann G, Brabletz T, Eberhart CG, Nikkhah G, Maciaczyk J. Activation of canonical WNT/β-catenin signaling enhances in vitro motility of glioblastoma cells by activation of ZEB1 and other activators of epithelial-to-mesenchymal transition. Cancer Lett 2012; 325: 42-53.
23. Kalani MYS, Cheshier SH, Cord BJ, Bababeygy SR, Vogel H, Weissman IL, Palmer TD, Nusse R. Wnt-mediated self-renewal of neural stem/progenitor cells. Proc Nat Acad Sci USA 2008; 105: 16970-16975.
24. Kelly JJP, Stechishin O, Chojnacki A, Lun X, Sun B, Senger DL, Forsyth P, Auer RN, Dunn JF, Cairncross JG, Parney IF, Weiss S. Proliferation of human glioblastoma stem cells occurs independently of exogenous mitogens. Stem Cells 2009; 27: 1722-1733.
25. Lathia JD, Gallagher J, Heddleston JM, Wang J, Eyler CE, Macswords J, Wu Q, Vasanji A, McLendon RE, Hjelmeland AB, Rich JN. Integrin alpha 6 regulates glioblastoma stem cells. Cell stem cell 2010; 6: 421-432.
26. Lawrence YR, Mishra MV, Werner-Wasik M, Andrews DW, Showalter TN, Glass J, Shen X, Symon Z, Dicker A P. Improving prognosis of glioblastoma in the 21st century: Who has benefited most? Cancer 2011; 118: 4228-4234.
27. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007; 114: 97-109.
28. Maciaczyk J, Singec I, Maciaczyk D, Klein A, Nikkhah G. Restricted spontaneous in vitro differentiation and region-specific migration of long-term expanded fetal human neural precursor cells after transplantation into the adult rat brain. Stem Cells Dev 2009; 18: 1043-1058.
29. McLendon RE, Provenzale J. Glioneuronal tumors of the central nervous system. Brain Tumor Pathol 2002; 19: 51-58.
30. Merchant AA, Matsui W. Targeting Hedgehog - a cancer stem cell pathway. Clin Cancer Res 2010; 16: 3130-3140.
31. Mizrak D, Brittan M, Alison MR. CD133: molecule of the moment. J Pathol 2008; 214: 3-9.
32. Morton JP, Lewis BC. Shh signaling and pancreatic cancer: implications for therapy? Cell Cycle 2007; 6: 1553-1557.
33. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, Pan F, Pelloski CE, Sulman EP, Bhat KP, Verhaak RG, Hoadley KA, Hayes DN, Perou CM, Schmidt HK, Ding L, Wilson RK, Van Den Berg D, Shen H, Bengtsson H, Neuvial P, Cope LM, Buckley J, Herman JG, Baylin SB, Laird PW, Aldape K; Cancer Genome Atlas Research Network. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 2010; 17: 510-522.
34. Nusse R. Wnt signaling and stem cell control. Cell Res 2008; 18: 523-527.
35. - tumor-initiating cells in adult human gliomas. Neurosurgery 2008; 62: 505-515.
36. Orr BA, Bai H, Odia Y, Jain D, Anders RA, Eberhart CG. Yes-associated protein 1 is widely expressed in human brain tumors and promotes glioblastoma growth. J Neuropathol Exp Neurol 2011; 70: 568-577.
37. Perry A, Miller CR, Gujrati M, Scheithauer BW, Zambrano SC, Jost SC, Raghavan R, Qian J, Cochran EJ, Huse JT, Holland EC, Burger PC, Rosenblum MK. Malignant gliomas with primitive neu roectodermal tumor-like components: a clinicopathologic and genetic study of 53 cases. Brain Pathol 2009; 19: 81-90.
38. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD, Misra A, Nigro JM, Colman H, Soroceanu L, Williams PM, Modrusan Z, Feuerstein BG, Aldape K. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 2006; 9: 157-173.
39. Pruszak J, Ludwig W, Blak A, Alavian K, Isacson O. CD15, CD24, and CD29 define a surface biomarker code for neural lineage differentiation of stem cells. Stem Cells 2009; 27: 2928-2940.
40. Read T-A, Fogarty MP, Markant SL, McLendon RE, Wei Z, Ellison DW, Febbo PG, Wechsler-Reya RJ. Identification of CD15 as a marker for tumor-propagating cells in a mouse model of medulloblastoma. Cancer Cell 2009; 15: 135-147.
41. Reeves SA, Helman LJ, Allison A, Israel MA. Molecular cloning and primary structure of human glial fibrillary acidic protein. Proc Nat Acad Sci USA 1989; 86: 5178-5182.
42. Schreck KC, Taylo, P, Marchionni L, Gopalakrishnan V, Bar EE, Gaiano N, Eberhart CG. The Notch target Hes1 directly modulates Gli1 expression and Hedgehog signaling: a potential mechanism of therapeutic resistance. Clin Cancer Res 2010; 16: 6060-6070.
43. Sethi N, Kang Y. Notch signalling in cancer progression and bone metastasis. Br J Cancer 2011; 105: 1805-1810.
44. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. Identification of human brain tumour initiating cells. Nature 2004; 432: 396-401.
45. Son MJ, Woolard K, Nam D-H, Lee J, Fine HA. SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 2009; 4: 440-452.
46. Uchida N, Buck DW, He D, Reitsma MJ, Masek M, Phan TV, Tsukamoto AS, Gage FH, Weissman IL. Direct isolation of human central nervous system stem cells. Proc Nat Acad Sci USA 2000; 97: 14720-14725.
47. Varelas X, Miller BW, Sopko R, Song S, Gregorieff A, Fellouse FA, Sakuma R, Pawson T, Hunziker W, McNeill H, Wrana JL, Attisano L. The Hippo pathway regulates Wnt/beta-catenin signaling. Dev Cell 2010; 18: 579-591.
48. Vescovi AL, Galli R, Reynolds BA. Brain tumour stem cells. Nature Rev Cancer 2006; 6: 425-436.
49. Ward RJ, Lee L, Graham K, Satkunendran T, Yoshikawa K, Ling E, Harper L, Austin R, Nieuwenhuis E, Clarke ID, Hui C-C, Dirks PB. Multipotent CD15+ cancer stem cells in patched-1-deficient mouse medulloblastoma. Cancer Res 2009; 69: 4682-4690.
50. Wolańczyk M, Hułas-Bigoszewska K, Witusik-Perkowska M, Papierz W, Jaskólski D, Liberski PP, Rieske P. Imperfect oligodendrocytic and neuronal differentiation of glioblastoma cells. Folia Neuropathol 2010; 48: 27-34.