The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype

Cell Cycle

Volumn 8, Issue 20, 2009, Pages 3274-3284

  Heddleston, John M ^a   Li, Zhizhong ^a   McLendon, Roger E ^a,b   Hjelmeland, Anita B ^a   Rich, Jeremy N ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Cancer stem cell; Glioblastoma; HIF2 ; Hypoxia; Hypoxia inducible factor

Indexed keywords

CD133 ANTIGEN; CELL MARKER; GLUCOSE TRANSPORTER 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PROTEIN SERPIN B9; SERINE PROTEINASE INHIBITOR; TRANSCRIPTION FACTOR NANOG; UNCLASSIFIED DRUG; VASCULOTROPIN; VON HIPPEL LINDAU PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; CANCER CELL; CANCER STEM CELL; CARCINOGENESIS; CELL POPULATION; CELL PROLIFERATION; CELL RENEWAL; CELL SURVIVAL; CONTROLLED STUDY; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; MOUSE; NONHUMAN; PHENOTYPE; PLASTICITY; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; TUMOR GROWTH; UPREGULATION;

EID: 70350225829     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.8.20.9701     Document Type: Review

References (73)

1. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, et al. Malignant astrocytic glioma: genetics, biology and paths to treatment. Genes Dev 2007; 21:2683-2710 (Pubitemid 350070717)
2. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005; 352:987-996 (Pubitemid 40349501)
3. Vredenburgh JJ, Desjardins A, Herndon JE, 2nd, Dowell JM, Reardon DA, Quinn JA, et al. Phase II trial of bevacizumab and irinotecan in recurrent malignant glioma. Clin Cancer Res 2007; 13:1253-1259
4. Vredenburgh JJ, Desjardins A, Herndon JE, 2nd, Marcello J, Reardon DA, Quinn JA, et al. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J Clin Oncol 2007; 25:4722-4729
5. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer and cancer stem cells. Nature 2001; 414:105-111
6. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994; 367:645-648 (Pubitemid 24067706)
7. Bonnet D, Dick J. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3:730-737 (Pubitemid 27298715)
8. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100:3983-3988 (Pubitemid 36418143)
9. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004; 64:7011-7021 (Pubitemid 39331011)
10. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 2003; 100:15178-15183 (Pubitemid 37518036)
11. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63:5821-5828 (Pubitemid 37187480)
12. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature 2004; 432:396-401. (Pubitemid 39551674)
13. Taylor MD, Poppleton H, Fuller C, Su X, Liu Y, Jensen P, et al. Radial glia cells are candidate stem cells of ependymoma. Cancer Cell 2005; 8:323-335 (Pubitemid 41443417)
14. Yuan X, Curtin J, Xiong Y, Liu G, Waschsmann- Hogiu S, Farkas DL, et al. Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 2004; 23:9392-9400 (Pubitemid 40069671)
15. Vescovi AL, Galli R, Reynolds BA. Brain tumour stem cells. Nat Rev Cancer 2006; 6:425-436
16. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444:756-760 (Pubitemid 44949604)
17. Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB, et al. Stem Cell-like Glioma Cells Promote Tumor Angiogenesis through Vascular Endothelial Growth Factor. Cancer Res 2006; 66:7843-7848 (Pubitemid 44299144)
18. Hambardzumyan D, Becher OJ, Rosenblum MK, Pandolfi PP, Manova-Todorova K, Holland EC. PI3K pathway regulates survival of cancer stem cells residing in the perivascular niche following radiation in medulloblastoma in vivo. Genes Dev 2008; 22:436-448 (Pubitemid 351272752)
19. Wulf GG, Wang RY, Kuehnle I, Weidner D, Marini F, Brenner MK, et al. A leukemic stem cell with intrinsic drug efflux capacity in acute myeloid leukemia. Blood 2001; 98:1166-1173
20. + cancer stem cells in glioblastoma. Mol Cancer 2006; 5:67.
21. Todaro M, Alea MP, Di Stefano AB, Cammareri P, Vermeulen L, Iovino F, et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 2007; 1:389-402. (Pubitemid 47506537)
22. Blazek ER, Foutch JL, Maki G. Daoy medulloblastoma cells that express CD133 are radioresistant relative to CD133-cells, and the CD133+ sector is enlarged by hypoxia. Int J Radiat Oncol Biol Phys 2007; 67:1-5. (Pubitemid 44959518)
23. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 2008; 100:672-679
24. Kiel MJ, Morrison SJ. Uncertainty in the niches that maintain haematopoietic stem cells. Nat Rev Immunol 2008; 8:290-301.
25. Gilbertson RJ, Rich JN. Making a tumour's bed: glioblastoma stem cells and the vascular niche. Nat Rev Cancer 2007; 7:733-736
26. Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, et al. A perivascular niche for brain tumor stem cells. Cancer Cell 2007; 11:69-82. (Pubitemid 46054518)
27. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, et al. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008; 3:289-300.
28. Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, et al. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008; 3:279-288
29. Yang ZJ, Wechsler-Reya RJ. Hit 'em where they live: targeting the cancer stem cell niche. Cancer Cell 2007; 11:3-5.
30. Silván U, Díez-Torre A, Arluzea J, Andrade R, Silió M, Aréchaga J. Hypoxia and pluripotency in embryonic and embryonal carcinoma stem cell biology. Differentiation 2009; Epub ahead of print.
31. Clarke L, van der Kooy D. Low oxygen enhances primitive and definitive neural stem cell colony Formation by inhibiting distinct cell death pathways. Stem Cells 2009; Epub ahead of print.
32. Simon MC, Keith B. The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 2008; 9:285-296
33. Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci USA 2007; 104:5431-5436 (Pubitemid 47175697)
34. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126:663-676 (Pubitemid 44233629)
35. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131:861-872 (Pubitemid 350138099)
36. Gangemi RM, Griffero F, Marubbi D, Perera M, Capra MC, Malatesta P, et al. SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells 2009; 27:40-48
37. Du Z, Jia D, Liu S, Wang F, Li G, Zhang Y, et al. Oct4 is expressed in human gliomas and promotes colony formation in glioma cells. Glia 2009; 57:724-733
38. Wang J, Wang H, Li Z, Wu Q, Lathia JD, McLendon RE, et al. c-Myc is required for maintenance of glioma cancer stem cells. PLoS One 2008; 3:3769.
39. Zheng H, Ying H, Yan H, Kimmelman AC, Hiller DJ, Chen AJ, et al. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 2008; 455:1129-1133
40. Hu G, Kim J, Xu Q, Leng Y, Orkin SH, Elledge SJ. A genome-wide RNAi screen identifies a new transcriptional module required for self-renewal. Genes Dev 2009; 23:837-848
41. Wong DJ, Liu H, Ridky TW, Cassarino D, Segal E, Chang HY. Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell 2008; 2:333-344
42. Liu R, Wang X, Chen GY, Dalerba P, Gurney A, Hoey T, et al. The prognostic role of a gene signature from tumorigenic breast-cancer cells. N Engl J Med 2007; 356:217-226 (Pubitemid 46143225)
43. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008; 40:499-507. (Pubitemid 351601215)
44. Bissell MJ, Kenny PA, Radisky DC. Microenvironmental regulators of tissue structure and function also regulate tumor induction and progression: the role of extracellular matrix and its degrading enzymes. Cold Spring Harb Symp Quant Biol 2005; 70:343-356
45. Jögi A, Øra I, Nilsson H, Lindeheim A, Makino Y, Poellinger L, et al. Hypoxia alters gene expression in human neuroblastoma cells toward an immature and neural crest-like phenotype. Proc Natl Acad Sci USA 2002; 99:7021-7026
46. Tavaluc RT, Hart LS, Dicker DT, El-Deiry WS. Effects of low confluency, serum starvation and hypoxia on the side population of cancer cell lines. Cell Cycle 2007; 6:2554-2562
47. Giuntoli S, Rovida E, Gozzini A, Barbetti V, Cipolleschi MG, Olivotto M, et al. Severe hypoxia defines heterogeneity and selects highly immature progenitors within clonal erythroleukemia cells. Stem Cells 2007; 25:1119-1125 (Pubitemid 46684871)
48. Das B, Tsuchida R, Malkin D, Koren G, Baruchel S, Yeger H. Hypoxia enhances tumor stemness by increasing the invasive and tumorigenic side population fraction. Stem Cells 2008; 26:1818-1830
49. + human glioblastoma cells in vitro. Mol Cancer Res 2009; 7:489-497
50. Li Z, Bao S, Wu Q, Wang H, Eyler C, Sathornsumetee S, et al. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 2009; 15:501-513
51. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature 2000; 407:249-257
52. Cárdenas-Navia LI, Mace D, Richardson RA, Wilson DF, Shan S, Dewhirst MW. The pervasive presence of fluctuating oxygenation in tumors. Cancer Res 2008; 68:5812-5819
53. Pan GJ, Pei DQ. Identification of two distinct transactivation domains in the pluripotency sustaining factor nanog. Cell Res 2003; 13:499-502.
54. Chambers I, Tomlinson SR. The transcriptional foundation of pluripotency. Development 2009; 136:2311-2322
55. Niwa H, Masui S, Chambers I, Smith AG, Miyazaki J. Phenotypic complementation establishes requirements for specific POU domain and generic transactivation function of Oct-3/4 in embryonic stem cells. Mol Cell Biol 2002; 22:1526-1536 (Pubitemid 34150788)
56. Covello KL, Kehler J, Yu H, Gordan JD, Arsham AM, Hu CJ, et al. HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development and tumor growth. Genes Dev 2006; 20:557-570 (Pubitemid 43345322)
57. Yan Q, Bartz S, Mao M, Li L, Kaelin WG Jr. The hypoxia-inducible factor 2alpha N-terminal and C-terminal transactivation domains cooperate to promote renal tumorigenesis in vivo. Mol Cell Biol 2007; 27:2092-2102 (Pubitemid 46418467)
58. Beier D, Hau P, Proescholdt M, Lohmeier A, Wischhusen J, Oefner PJ, et al. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res 2007; 67:4010-4015 (Pubitemid 46815044)
59. Jain RK, di Tomaso E, Duda DG, Loeffler JS, Sorensen AG, Batchelor TT. Angiogenesis in brain tumours. Nat Rev Neurosci 2007; 8:610-622
60. Batchelor TT, Sorensen AG, di Tomaso E, Zhang WT, Duda DG, Cohen KS, et al. AZD2171, a pan- VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 2007; 11:83-95. (Pubitemid 46075199)
61. Pàez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Viñals F, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009; 15:220-231
62. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009; 15:232-239
63. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133:704-715 (Pubitemid 351636299)
64. Kenny PA, Lee GY, Myers CA, Neve RM, Semeiks JR, Spellman PT, et al. The morphologies of breast cancer cell lines in three-dimensional assays correlate with their profiles of gene expression. Mol Oncol 2007; 1:84-96. (Pubitemid 46776616)
65. Fael Al-Mayhani TM, Ball SL, Zhao JW, Fawcett J, Ichimura K, Collins PV, et al. An efficient method for derivation and propagation of glioblastoma cell lines that conserves the molecular profile of their original tumours. J Neurosci Methods 2009; 176:192-199
66. Pollard SM, Yoshikawa K, Clarke ID, Danovi D, Stricker S, Russell R, et al. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 2009; 4:568-580
67. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, 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 2006; 9:391-403. (Pubitemid 43668737)
68. Zimmer M, Ebert BL, Neil C, Brenner K, Papaioannou I, Melas A, et al. Small-molecule inhibitors of HIF-2a translation link its 5'UTR iron-responsive element to oxygen sensing. Mol Cell 2008; 32:838-848
69. Gordan JD, Bertout JA, Hu CJ, Diehl JA, Simon MC. HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 2007; 11:335-347
70. Gustafsson MV, Zheng X, Pereira T, Gradin K, Jin S, Lundkvist J, et al. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 2005; 9:617-628 (Pubitemid 41555144)
71. Sahlgren C, Gustafsson MV, Jin S, Poellinger L, Lendahl U. Notch signaling mediates hypoxiainduced tumor cell migration and invasion. Proc Natl Acad Sci USA 2008; 105:6392-6397 (Pubitemid 351758356)
72. Pistollato F, Chen HL, Rood BR, Zhang HZ, D'Avella D, Denaro L, et al. Hypoxia and HIF1alpha repress the differentiative effects of BMPs in high-grade glioma. Stem Cells 2009; 27:7-17.
73. Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, Broggi G, et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006; 444:761-765 (Pubitemid 44949605)