CD133: Holy of grail of neuro-oncology or promiscuous red-herring?

Cell Proliferation

Volumn 45, Issue 6, 2012, Pages 527-537

  Donovan, L K ^a   Pilkington, G J ^a  

^a UNIVERSITY OF PORTSMOUTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD133 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; NOTCH RECEPTOR; VASCULOTROPIN;

ANGIOGENESIS; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; BRAIN TUMOR; CANCER STEM CELL; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CELL HYPOXIA; GLIOBLASTOMA; HUMAN; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION;

ANIMALS; ANOXIA; ANTIGENS, CD; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOPROTEINS; HUMANS; NEOPLASMS; NEOPLASTIC STEM CELLS; PEPTIDES; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL;

CLUPEIDAE;

EID: 84868130835     PISSN: 09607722     EISSN: 13652184     Source Type: Journal    
DOI: 10.1111/j.1365-2184.2012.00842.x     Document Type: Article

References (95)

1. Corbeil D, Röper K, Fargeas CA, Joester A, Huttner WB (2001) Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic 2, 82-91.
2. Miraglia S, Godfrey W, Yin AH, Atkins K, Warnke R, Holden JT et al. (1997) A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood 90, 5013-5021.
3. Boivin D, Labbé D, Fontaine N, Lamy S, Beaulieu E, Gingras D et al. (2009) The stem cell marker CD133 (prominin-1) is phosphorylated on cytoplasmic tyrosine-828 and tyrosine-852 by Src and Fyn tyrosine kinases. Biochemistry 48, 3998-4007.
4. Mizrak D, Brittan M, Alison MR (2008) CD133: molecule of the moment. J. Pathol. 214, 3-9.
5. Weigmann A, Corbeil D, Hellwig A, Huttner WB (1997) Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc. Natl. Acad. Sci. USA 94, 12425-12430.
6. Corbeil D, Roper K, Hellwig A, Tavian M, Miraglia S, Watt SM et al. (2000) The human AC133 hematopoietic stem cell antigen is also expressed in epithelial cells and targeted to plasma membrane protrusions. J. Biol. Chem. 275, 5512-5520.
7. Roper K, Corbeil D, Huttner WB (2000) Retention of prominin in microvilli reveals distinct cholesterol-based lipid microdomains in the apical plasma membrane. Nat. Cell Biol. 2, 582-592.
8. Giebel B, Corbeil D, Beckmann J, Hohn J, Freund D, Giesen K et al. (2004) Segregation of lipid raft markers including CD133 in polarized human haematopoietic stem and progenitor cells. Blood 104, 2332-2338.
9. Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG et al. (1997) AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 90, 5002-5012.
10. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J et al. (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res. 63, 5821-5828.
11. Singh SK, Hawkins C, Clarke ID, Squire JA, Bavani J, Hide T et al. (2004) Identification of human brain tumour initiating cells. Nature 18, 396-401.
12. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hielmeland AB et al. (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444, 756-760.
13. Zeppernick F, Ahmadi R, Campos B, Dictus C, Helmke BM, Becker N et al. (2008) Stem cell marker CD133 affects clinical outcome in glioma patients. Clin. Cancer Res. 14, 123-129.
14. Bauer N, Fonseca A, Florek M, Freund D, Jászai J, Bornhäuser M et al. (2008) New insights into the cell biology of haematopoietic progenitors by studying prominin-1 (CD133). Cells Tissues Organs 188, 127-138.
15. Yu Y, Flint A, Dvorin EL, Bischoff J (2002) AC133-2, a novel isoform of human AC133 stem cell antigen. J. Biol. Chem. 277, 20711-20716.
16. Campos B, Zeng L, Daotrong PH, Eckstein V, Unterberg A, Mairbaurl H et al. (2011) Expression and regulation of AC133 and CD133 in glioblastoma. Glia 59, 1974-1986.
17. Donovan LK, Potter NE, Warr T, Pilkington GJ (2012) A Prominin-1-rich paediatric glioblastoma: biological behaviour is determined by oxygen tension modulated CD133 expression but no accompanied by underlying molecular profiles. Transl. Oncol. 5, 141-154.
18. Ardebili SY, Zajc I, Gole B, Campos B, Herold-Mende C, Drmota S et al. (2011) CD133/prominin1 is prognostic for GBM patient's survival, but inversely correlated with cysteine cathepsin's expression in glioblastoma derived spheroids. Radiol. Oncol. 45, 102-115.
19. Prestegarden L, Svendsen A, Wang J, Sleire L, Skaftnesmo KO, Bjerkvig R et al. (2010) Glioma cell populations grouped by different cell type markers drive brain tumour growth. Cancer Res. 70, 4274-4279.
20. Levicar N, Nuttall RK, Lah TT (2003) Proteases in brain tumour progression. Acta Neurochir. (Wien) 145, 825-838.
21. Vranic A (2010) Antigenic expression on recurrent meningioma cells. Radiol. Oncol. 44, 107-112.
22. Lah T, Obermajer N, Duran-Alonso MB, Kos J (2008) Cysteine, cathepsins and cystatins as cancer biomarkers. In: Edwards DR, ed. The Cancer Degradome Proteases and Cancer Biology, pp. 587-625. New York: Springer.
23. Berquin LM, Sloane BF (1996) Cathepsin B expression in human tumours. Adv. Exp. Med. Biol. 389, 281-294.
24. Beier D, Hau P, Proescholdt M, Lohmeier A, Wischhusen J, Oefner PJ et al. (2007) CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 67, 4010-4015.
25. Wang J, Sakariassen PO, Tsinkalovsky O, Immervoll H, Boe SO, Svendsen A et al. (2008) CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int. J. Cancer 122, 761-768.
26. Keith B, Simon MC (2007) Hypoxia-inducible factors, stem cells, and cancer. Cell 129, 465-472.
27. Hockel M, Vorndran B, Schlenger K, Baussmann E, Knapstein PG (1993) Tumor oxygenation: a new predictive parameter in locally advanced cancer of the uterine cervix. Gynecol. Oncol. 51, 141-149.
28. Qing G, Simon MC (2009) Hypoxia inducible factor 2α: a critical mediator of aggressive tumour phenotypes. Curr. Opin. Genet. Dev. 19, 60-66.
29. Scheuermann TH, Yang J, Zhang L, Gardner KH, Bruick RK (2007) Hypoxia-inducible factors Per/ARNT/Sim domains: structure and function. Methods Enzymol. 435, 3-24.
30. Gordon JD, Simon MC (2007) Hypoxia-inducible factors: central regulators of the tumour phenotype. Curr. Opin. Genet. Dev. 17, 71-77.
31. Lendahl U, Lee KL, Yang H, Poellinger L (2009) Generating specificity and diversity in the transcriptional response to hypoxia. Nat. Rev. Genet. 10, 821-832.
32. Raval RR, Lau KW, Tran MG, Sowter HM, Mandroita SJ, Li JL et al. (2005) Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol. Cell. Biol. 25, 5675-5686.
33. Patel SA, Simon MC (2008) Biology of hypoxia inducible factor 2α in development and disease. Cell Death Diff. 15, 628-634.
34. Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC (2003) Differential roles of hypoxia-inducible factor 1α (HIF-1α) and HIF2α in hypoxic gene regulation. Mol. Cell. Biol. 23, 9361-9374.
35. Wang V, Davis DA, Haque M, Huang LE, Yarchoan R (2005) Differential gene up-regulation by hypoxia-inducible factor 1-α and hypoxia-inducible factor 2α in HEK293T cells. Cancer Res. 65, 3299-3306.
36. Gradmaier K, A de Weijert MC, Verhaegh GW, Schalken JA, Oosterwijk E (2004) Strict regulation of CAIX(G250/MN) by HIF-1alpha in clear cell renal cell carcinoma. Oncogene 23, 5624-5631.
37. Warnecke C, Zaborowska Z, Kurreck J, Erdmann VA, Frei U, Wiesener M et al. (2004) Differentiating the functional role of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha (EPAS-1) by the use of RNA interference: erythropoietin is a HIF-2alpha target gene in Hep3B and Kelly cells. FASEB J. 18, 1462-1464.
38. Baba M, Hirai S, Yamada-Okabe H, Hamada K, Tabuchi H, Kobayashi K et al. (2003) Loss of von Hippel-Lindau protein causes cell density dependent deregulation of CyclinD1 expression through hypoxia-inducible factor. Oncogene 22, 2728-2738.
39. Covello KL, Kehler J, Yu H, Gordan JD, Arsham AM, Hu CJ et al. (2006) HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev. 20, 557-570.
40. Gort EH, Van Haaften G, Verlaan I, Groot AJ, Plasterk RH, Shvarts A et al. (2008) The TWIST1 oncogene is a direct target of hypoxia-inducible factor-2alpha. Oncogene 27, 1501-1511.
41. Wiesener MS, Jurgensen JS, Rosenberger C, Scholze CK, Horstrup JH, Warnecke C et al. (2003) Widespread hypoxia-inducible expression of HIF-2alpha in distinct cell populations of different organs. FASEB J. 17, 271-273.
42. Holmquist-Mengelbier L, Fredlund E, Lofstedt T, Noguera R, Navarro S, Nilsson H et al. (2006) Recruitment of HIF-1alpha and HIF-2alpha to common target genes is differentially regulated in neuroblastoma: HIF-2alpha promotes an aggressive phenotype. Cancer Cell 10, 413-423.
43. Li Z, Bao S, Wu Q, Wang H, Eyler C, Sathornsumetee S et al. (2009) Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 15, 501-513.
44. Zheng X, Shen G, Yang X, Liu W (2007) Most C6 cells are cancer stem cells: evidence from clonal and population analyses. Cancer Res. 67, 3691-3697.
45. Griguer CE, Oliva CR, Gobin E, Marcorelles P, Benos DJ, Lancaster JR Jr et al. (2008) CD133 is a marker of bioenergetic stress in human glioma. PLoS ONE 3, e3655.
46. Jin J, Davis J, Zhu D, Kashima DT, Leroueil M, Pan C et al. (2007) Identification of novel proteins affected by rotenone in mitochondria of dopaminergic cells. BMC Neurosci. 8, 67.
47. King MP, Attardi G (1989) Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science 246, 500-503.
48. Gillies RJ, Gatenby RA (2007) Adaptive landscapes and emergent phenotypes: why do cancers have high glycolysis? J. Bioenerg. Biomembr. 39, 251-257.
49. Charles NA, Holland EC, Gilbertson R, Glass R, Kettenmann H (2011) The brain tumour microenvironment. Glia 59, 1169-1180.
50. Persano L, Rampazzo E, Della Puppa A, Pistollato F, Basso G (2011) The three-layer concentric model of glioblastoma: cancer stem cells, microenvironmental regulation, and therapeutic implications. ScientificWorldJournal 11, 1829-1841.
51. 2 distributions in the bone marrow haematopoietic compartment II Modified Kroghian models. Biophys. J. 81, 685-696.
52. 2 distributions in the bone marrow haematopoietic compartment I Krogh's model. Biophys. J. 81, 675-684.
53. Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD (2007) Distribution of haematopoietic stem cells in the bone marrow according to regional hypoxia. Proc. Natl. Acad. Sci. USA 104, 5431-5436.
54. Iida H, Suzuki M, Goitsuka R, Ueno H (2012) Hypoxia induces CD133 expression in human lung cancer cells by up-regulation of OCT3/4 and SOX2. Int. J. Oncol. 40, 71-79.
55. McCord AM, Jamal M, Shankavaram UT, Lang FF, Camphausen K, Tofilon PJ (2009) Physiologic oxygen concentration enhances the stem-like properties of CD133+ human glioblastoma cells in vitro. Mol. Cancer Res. 7, 489-497.
56. Zhu TS, Costello MA, Talsma CE, Flack CG, Crowley JG, Hamm LL et al. (2011) Endothelial cells create a stem cell niche in glioblastoma by providing NOTCH ligands that nurture self-renewal of cancer stem-like cells. Cancer Res. 71, 6061-6072.
57. Gustafsson MV, Zheng X, Pereira T, Gradin K, Jin S, Lundkvist J et al. (2005) Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev. Cell 9, 617-628.
58. Bray SJ (2006) Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7, 678-689.
59. Murata K, Hattori M, Hirai N, Shinozuka Y, Hirata H, Kageyama R et al. (2005) Hes1 directly controls cell proliferation through the transcriptional repression of p27Kip1. Mol. Cell. Biol. 25, 4262-4271.
60. Mao XG, Yan M, Xue XY, Zhang X, Ren HG, Guo G et al. (2011) Overexpression of ZNF217 in glioblastoma contributes to the maintenance of glioma stem cells regulated by hypoxia-inducible factors. Lab. Invest. 91, 1068-1078.
61. Pilkington GJ (1994) Tumour cell migration in the central nervous system. Brain Pathol. 4, 157-166.
62. Bolteus AJ, Berens ME, Pilkington GJ (2001) Migration and invasion in brain neoplasms. Curr. Neurol. Neurosci. Rep. 1, 225-232.
63. Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, Invernici G, Cenci T et al. (2010) Tumour vascularisation via endothelial differentiation of glioblastoma stem-like cells. Nature 468, 824-828.
64. Kukk E, Lymboussaki A, Taira S, Kaipainen A, Jeltsh M, Joukov V et al. (1996) VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development 122, 3829-3837.
65. Zagzag D, Lukyanov Y, Lan L, Ali MA, Esencay M, Mendez O et al. (2006) Hypoxia-inducible factor 1 and VEGF upregulate CXCR4 in glioblastoma: implications for angiogenesis and glioma cell invasion. Lab. Invest. 86, 1221-1232.
66. Burger JA, Kipps TJ (2006) CXCR4: a key receptor in the cross talk between tumour cells and their microenvironment. Blood 107, 1761-1767.
67. Su L, Zhang J, Xu H, Wang Y, Chu Y, Liu R et al. (2005) Differential expression of CXCR4 is associated with the metastatic potential of human non-small cell lung cancer cell. Clin. Cancer Res. 11, 8273-8280.
68. Saur D, Seidler B, Schneider G, Algül H, Beck R, Senekowitsch-Schmidtke R et al. (2005) CXCR4 expression increases liver and lung metastasis in a mouse model of pancreatic cancer. Gastroenterology 129, 1237-1250.
69. Kang H, Watkins G, Douglas-Jones A, Mansel RE, Jiang WG (2005) The elevated levels of CXCR4 is correlated with nodal metastasis of human breast cancer. Breast 14, 360-367.
70. Cabioglu N, Sahin A, Doucet M, Yavuz E, Igci AO, Yildirim E et al. (2005) Chemokine receptor CXCR4 expression in breast cancer as a potential predictive marker of isolated tumours in bone marrow. Clin. Exp. Metast. 22, 39-46.
71. Rempel SA, Dudas S, Ge S, Gutiérrez JA (2000) Identification and localisation of the cytokine SDF1 and its receptor, CXCR4, to regions of necrosis and angiogenesis in human glioblastoma. Clin. Cancer Res. 6, 102-111.
72. Oh JW, Drabik K, Kutsch O, Choi C, Tousson A, Benveniste EN (2001) CXCR4 expression and function in human astroglioma cells. J. Immunol. 166, 2695-2704.
73. Zhou Y, Larsen PH, Hao C, Yong VW (2002) CXCR4 is a major chemokine receptor on glioma cells and mediates their survival. J. Biol. Chem. 277, 49481-49487.
74. Woerner BM, Warrington NM, Kung AL, Perry A, Rubin JB (2005) Widespread CXCR4 activation in astrocytomas revealed by phospho-CXCR4-specific antibodies. Cancer Res. 65, 11392-11399.
75. Hong X, Jiang F, Kalkanis SN, Zhang ZG, Zhang XP, DeCarvalho AC et al. (2006) SDF-1 and CXCR4 are up-regulated by VEGF and contribute to glioma cell invasion. Cancer Lett. 236, 39-45.
76. Jensen RL (2009) Brain tumor hypoxia: tumorigenesis, angiogenesis, imaging, pseudoprogression, and as a therapeutic target. J. Neurooncol. 92, 317-335.
77. Oliver L, Olivier C, Marhuenda FB, Campone M, Vallette FM (2009) Hypoxia and the malignant glioma microenvironment: regulation and implications for therapy. Curr. Mol. Pharmacol. 2, 263-284.
78. Peichev M, Naiyer AJ, Pereira D, Zhu Z, Lane WJ, Williams M et al. (2000) Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 95, 952-958.
79. Torrente Y, Belicchi M, Mamchaoui K, Pellegrino MA, Furling D, Mouly V et al. (2004) Human circulating AC133(+) stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J. Clin. Invest. 114, 182-195.
80. Richardson GD, Robson CN, Lang SH, Neal DE, Maitland NJ, Collins AT (2004) CD133, a novel marker for human prostatic epithelial stem cells. J. Cell Sci. 117, 3539-3545.
81. Ono M, Hakomori S (2004) Glycosylation defining cancer cell motility and invasiveness. Glycoconj. J. 20, 71-78.
82. Taieb N, Maresca M, Guo XJ, Garmy N, Fantini J, Yahi N (2009) The first extracellular domain of the tumour stem cell marker CD133 contains an antigenic ganglioside-binding motif. Cancer Lett. 278, 164-173.
83. Kemper K, Sprick MR, De Bree M, Scopelliti A, Vermeulen L, Hoek M et al. (2010) The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res. 70, 719-729.
84. Hakomori S (1996) Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res. 56, 5309-5318.
85. Zheng M, Fang H, Tsuruoka T, Tsuji T, Sasaki T, Hakomori S (1993) Regulatory role of GM3 ganglioside in alpha 5 beta 1 integrin receptor for fibronectin-mediated adhesion of FUA169 cells. J. Biol. Chem. 268, 2217-2222.
86. Ohkawa Y, Miyazaki S, Miyata M, Hamamura K, Furukawa K (2008) Essential roles of integrin-mediated signaling for the enhancement of malignant properties of melanomas based on the expression of GD3. Biochem. Biophys. Res. Commun. 373, 14-19.
87. Birks SM, Danquah JO, King L, Vlasak R, Gorecki DC, Pilkington GJ (2011) Targeting the GD3 acetylation pathway selectively induces apoptosis in glioblastoma. Neuro Oncol. 13, 950-960.
88. Rutella S, Bonanno G, Procoli A, Mariotti A, Corallo M, Prisco MG et al. (2009) Cells with characteristics of cancer stem/progenitor cells express the CD133 antigen in human endometrial tumours. Clin. Cancer Res. 15, 4299-4311.
89. Ma B, Lei X, Guan Y, Mou LS, Yuan YF, Yue H et al. (2011) Maintenance of retinal cancer stem cell-like properties through long-term serum-free culture from human retinoblastoma. Oncol. Rep. 26, 135-143.
90. Karbanová J, Missol-Kolka E, Fonseca AV, Lorra C, Janich P, Hollerová H et al. (2008) The stem cell marker CD133 (Prominin-1) is expressed in various human glandular epithelia. J. Histochem. Cytochem. 56, 977-993.
91. Florek M, Haase M, Marzesco A, Freud D, Ehninger G, Huttner WB et al. (2005) Prominin-1/CD133, a neural and haematopoietic stem cell marker, is expressed in adult human differentiated cells and certain types of kidney cancer. Cell Tissue Res. 319, 15-26.
92. Mak AB, Blakely KM, Williams RA, Penttilä PA, Shukalyuk AI, Osman KT et al. (2011) CD133 protein N-glycosylation processing contributes to cell surface recognition of the primitive cell marker AC133 epitope. J. Biol. Chem. 286, 41046-41056.
93. Rappa G, Fodstad O, Lorico A (2008) The stem cell-associated antigen CD133 (Prominin-1) is a molecular therapeutic target for metastatic melanoma. Stem Cells 26, 3008-3017.
94. Bar EE (2011) Glioblastoma, cancer stem cells and hypoxia. Brain Pathol. 21, 119-129.
95. Soltysova A, Altanerova V, Altaner C (2005) Cancer stem cells. Neoplasm 52, 435-440.