CD133 glycosylation is enhanced by hypoxiain cultured glioma stem cells

International Journal of Oncology

Volumn 42, Issue 3, 2013, Pages 1011-1017

  Lehnus, Kristina S ^a   Donovan, Laura K ^a   Huang, Xiaowei ^b   Zhao, Ninghui ^c   Warr, Tracy J ^d   Pilkington, Geoffrey J ^a   An, Qian ^a  

^a UNIVERSITY OF PORTSMOUTH   (United Kingdom)

^b YUNNAN UNIVERSITY   (China)

^c KUNMING MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF WOLVERHAMPTON   (United Kingdom)

Author keywords

Cancer stem cell; CD133; Glioma; Glycosylation; Hypoxia

Indexed keywords

CD133 ANTIGEN;

ANTIGEN BINDING; ANTIGEN DETECTION; ANTIGEN EXPRESSION; ARTICLE; CANCER STEM CELL; CELL SELECTION; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE; GLIOBLASTOMA; GLIOMA CELL; HYPOXIA; IMMUNOCYTOCHEMISTRY; INCUBATION TIME; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD; APOPTOSIS; BRAIN NEOPLASMS; CELL HYPOXIA; CELL LINE, TUMOR; GLIOMA; GLYCOPROTEINS; GLYCOSYLATION; HUMANS; NEOPLASTIC STEM CELLS; PEPTIDES;

EID: 84873671800     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2013.1787     Document Type: Article

References (44)

1. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J and Dirks PB: Identification of a cancer stem cell in human brain tumours. Cancer Res 63: 5821-5828, 2003. (Pubitemid 37187480)
2. Wang J, Sakariassen PØ, Tsinkalovsky O, Immervoll H, Bøe SO, Svendsen A, Prestegarden L, Røsland G, Thorsen F, Stuhr L, Molven A, Bjerkvig R and Enger PØ: CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int J Cancer 122: 761-768, 2008.
3. Clément V, Dutoit V, Marino D, Dietrich PY and Radovanovic I: Limits of CD133 as a marker of glioma self-renewing cells. Int J Cancer 125: 244-248, 2009.
4. Mizrak D, Brittan M and Alison MR: CD133: molecule of the moment. J Pathol 214: 3-9, 2008.
5. Cheng JX, Liu BL and Zhang X: How powerful is CD133 as a cancer stem cell marker in brain tumors? Cancer Treat Rev 35: 403-408, 2009.
6. Campos B and Herold-Mende CC: Insight into the complex regulation of CD133 in glioma. Int J Cancer 128: 501-510, 2011.
7. Sun Y, Kong W, Falk A, Hu J, Zhou L, Pollard S and Smith A: CD133 (prominin) negative human neural stem cells are clonogenic and tripotent. PLoS One 4: 1-10, 2009.
8. Fargeas CA, Huttner WB and Corbeil D: Nomenclature of prominin-1 (CD133) splice variants - an update. Tissue Antigens 69: 602-606, 2007. (Pubitemid 46733679)
9. Osmond TL, Broadley KW and McConnell MJ: Glioblastoma cells negative for the anti-CD133 antibody AC133 express a truncated variant of the CD133 protein. Int J Mol Med 25: 883-888, 2010.
10. 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: 1025-1032, 2008.
11. Oliver L, Olivier C, Marhuenda FB, Campone M and Vallette FM: Hypoxia and the malignant glioma microenvironment: regulation and implications for therapy. Curr Mol Pharmacol 2: 263-284, 2009.
12. Evans SM, Judy KD, Dunphy I, Jenkins WT, Hwang WT, Nelson PT, Lustig RA, Jenkins K, Magarelli DP, Hahn SM, Collins RA, Grady MS and Koch CJ: Hypoxia is important in the biology and aggression of human glial brain tumors. Clin Cancer Res 10: 8177-8184, 2004. (Pubitemid 40053376)
13. Amberger-Murphy V: Hypoxia helps glioma to fight therapy. Curr Cancer Drug Targets 9: 381-390, 2009.
14. Donovan LK, Potter NE, Warr T and Pilkington GJ: A Prominin-1-rich paediatric glioblastoma: biological behaviour is determined by oxygen tension modulated CD133 expression but not accompanied by underlying molecular profiles. Transl Oncol 5: 141-154, 2012.
15. McCord AM, Jamal M, Shankavaram UT, Lang FF, Camphausen K and Tofilon PJ: Physiologic oxygen concentration enhances the stem-like properties of CD133+ human glioblastoma cells in vitro. Mol Cancer Res 7: 489-497, 2009.
16. Griguer CE, Oliva CR, Gobin E, Marcorelles P, Benos DJ, Lancaster JR Jr and Gillespie GY: CD133 is a marker of bioenergetic stress in human glioma. PLoS One 3: e3655, 2008.
17. Platet N, Liu SY, Atifi ME, Oliver L, Vallette FM, Berger F and Wion D: Influence of oxygen tension on CD133 phenotype in human glioma cell cultures. Cancer Lett 258: 286-290, 2007. (Pubitemid 350110377)
18. Iida H, Suzuki M, Goitsuka R and Ueno H: Hypoxia induces CD133 expression in human lung cancer cells by up-regulation of OCT3/4 and SOX2. Int J Oncol 40: 71-79, 2012.
19. Hermansen SK, Christensen KG, Jensen SS and Kristensen BW: Inconsistent immunohistochemical expression patterns of four different CD133 antibody clones in glioblastoma. J Histochem Cytochem 59: 391-407, 2011.
20. Günther HS, Schmidt NO, Phillips HS, Kemming D, Kharbanda S, Soriano R, Modrusan Z, Meissner H, Westphal M and Lamszus K: Glioblastoma-derived stem cell-enriched cultures form distinct subgroups according to molecular and phenotypic criteria. Oncogene 27: 2897-2909, 2008. (Pubitemid 351620450)
21. An Q, Burke GA, Dainton M, Harrison CJ, Kempski H, Konn Z, Myooren W, Stewart A, Taj M, Webb D, Strefford JC and Martineau M: Haploinsufficiency of the MLL and TOB2 genes in lymphoid malignancy. Leukemia 24: 649-652, 2010.
22. Fargeas CA, Fonseca A, Huttner WB and Corbeil D: Prominin-1 (CD133): from progenitor cells to human diseases. Future Lipidology 1: 213-255, 2006.
23. Kemper K, Sprick MR, De Bree M, Vermeulen L, Hoek M, Zeilstra J, Pals ST, Mehmet H, Stassi G and Medema JP: The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res 70: 719-729, 2010.
24. Gahmber CG and Tolvanen M: Why mammalian cell surface proteins are glycoproteins. Trends Biochem Sci 21: 308-311, 1996. (Pubitemid 26281034)
25. Taïeb N, Maresca M, Guo X, Garmy N, Fatini J and Yahi N: The first extracellular domain of the tumour stem cell marker CD133 contains an antigenic ganglioside-binding motif. Cancer Lett 278: 164-173, 2009.
26. Birks SM, Danquah JO, King L, Vlasak R, Gorecki DC and Pilkington GJ: Targeting the GD3 acetylation pathway selectively induces apoptosis in glioblastoma. Neuro Oncol 13: 950-960, 2011.
27. Bar EE, Lin A, Bar EE, Lin A, Mahairaki V, Matsui W and Eberhart CG: Hypoxia increases the expression of stem-cell markers and promotes clonogenicity in glioblastoma neurospheres. Am J Pathol 177: 1491-1502, 2010.
28. Ruan K, Song G and Ouyang G: Role of hypoxia in the hallmarks of human cancer. J Cell Biochem 107: 1053-1062, 2009.
29. Lu X and Kang Y: Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clin Cancer Res 16: 5928-5935, 2010.
30. Fujiwara S, Nakagawa K, Harada H, Nagato S, Furukawa K, Teraoka M, Seno T, Oka K, Iwata S and Ohnishi T: Silencing hypoxia-inducible factor-1alpha inhibits cell migration and invasion under hypoxic environment in malignant gliomas. Int J Oncol 30: 793-802, 2007.
31. Hashimoto O, Shimizu K, Semba S, Chiba S, Ku Y, Yokozaki H and Hori Y: Hypoxia induces tumor aggressiveness and the expansion of CD133-positive cells in a hypoxia-inducible factor-1a-dependent manner in pancreatic cancer cells. Pathobiology 78: 181-192, 2011.
32. Lee HC and Wei YH: Mitochondrial DNA instability and metabolic shift in human cancers. Int J Mol Sci 10: 674-701, 2009.
33. Gogvadze V, Zhivotovsky B and Orrenius S: The Warburg effect and mitochondrial stability in cancer cells. Mol Aspects Med 31: 60-74, 2010.
34. Grandemange S, Herzig S and Martinou JC: Mitochondrial dynamics and cancer. Semin Cancer Biol 19: 50-56, 2009.
35. Ishikawa K and Hayashi J: A novel function of mtDNA: its involvement in metastasis. Ann NY Acad Sci 1201: 40-43, 2010.
36. Denko NC: Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat Rev Cancer 8: 705-713, 2008.
37. Semenza GL: Regulation of cancer cell metabolism by hypoxia-inducible factor 1. Semin Cancer Biol 19: 12-16, 2009.
38. Chiche J, Rouleau M, Gounon P, Brahimi-Horn MC, Pouysségur J and Mazure NM: Hypoxic enlarged mitochondria protect cancer cells from apoptotic stimuli. J Cell Physiol 222: 648-657, 2010.
39. Klimova T and Chandel NS: Mitochondrial complex III regulates hypoxic activation of HIF. Cell Death Differ 15: 660-666, 2008. (Pubitemid 351405069)
40. De Haan C, Habibi-Nazhad B, Yan E, Salloum N, Parliament M and Allalunis-Turner J: Mutation in mitochondrial complex I ND6 subunit is associated with defective response to hypoxia in human glioma cells. Mol Cancer 3: 19, 2004.
41. Soeda A, Park M, Lee D, Mintz A, Androutsellis-Theotokis A, McKay RD, Engh J, Iwama T, Kunisada T, Kassam AB, Pollack IF and Park DM: Hypoxia promotes expansion of the CD133-positive glioma stem cells through activation of HIF-1alpha. Oncogene 28: 3949-3959, 2009.
42. Lluis JM, Llacuna L, von Montfort C, Bárcena C, Enrich C, Morales A and Fernandez-Checa JC: GD3 synthase overexpression sensitizes hepatocarcinoma cells to hypoxia and reduces tumor growth by suppressing the cSrc/NF-kappaB survival pathway. PLoS One 4: e8059, 2009.
43. Kolenda J, Jensen SS, Aaberg-Jessen C, Christensen K, Andersen C, Brünner N and Kristensen BW: Effects of hypoxia on expression of a panel of stem cell and chemoresistance markers in glioblastoma-derived spheroids. J Neurooncol 103: 43-58, 2011.
44. Cortes-Dericks L, Carboni GL, Schmid RA and Karoubi G: Putative cancer stem cells in malignant pleural mesothelioma show resistance to cisplatin and pemetrexed. Int J Oncol 37: 437-444, 2010.