Physiologic oxygen concentration enhances the stem-like properties of CD133+ human glioblastoma cells in vitro

Molecular Cancer Research

Volumn 7, Issue 4, 2009, Pages 489-497

  McCord, Amy M ^a   Jamal, Muhammad ^a   Shankavarum, Uma T ^b   Lang, Frederick F ^c   Camphausen, Kevin ^b   Tofilon, Philip J ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD133 ANTIGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; OCTAMER TRANSCRIPTION FACTOR 4; OXYGEN; TRANSCRIPTION FACTOR SOX2; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN CONTAINING PROTEIN 1; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; PEPTIDE; SMALL INTERFERING RNA; TUMOR MARKER;

ARTICLE; CANCER STEM CELL; CELL PROLIFERATION; CELL RENEWAL; CLONOGENESIS; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GLIA CELL; GLIOBLASTOMA; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; OXYGEN CONCENTRATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; BRAIN TUMOR; CELL DIFFERENTIATION; DNA MICROARRAY; DRUG SCREENING; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOBLOTTING; IN VITRO STUDY; METABOLISM; PATHOLOGY; TUMOR CELL CULTURE;

ANTIGENS, CD; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL PROLIFERATION; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; GLYCOPROTEINS; HUMANS; IMMUNOBLOTTING; NEOPLASTIC STEM CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXYGEN; PEPTIDES; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL; TUMOR STEM CELL ASSAY;

EID: 65549150903     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-08-0360     Document Type: Article

References (50)

1. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352: 987-996
2. Galli R, Binda E, Orfanelli U, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004; 64:7011-7021
3. Hemmati HD, Nakano I, Lazareff JA, et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 2003;100:15178-15183
4. Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature 2004;432:396-401.
5. Singh SK, Clarke ID, Terasaki M, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003;63:5821-5828
6. Kakarala M, Wicha MS. Cancer stem cells: implications for cancer treatment and prevention. Cancer J 2007;13:271-275
7. Bao S, Wu Q, Sathornsumetee S, et al. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 2006; 66:7843-7848
8. Lee J, Kotliarova S, Kotliarov Y, 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.
9. Piccirillo SG, Reynolds BA, Zanetti N, et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006;444:761-765
10. + cancer stem cells in glioblastoma. Mol Cancer 2006;5:67.
11. Bao S, Wu Q, McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006;444: 756-760
12. Guyton AC, Hall JE. Textbook of medical physiology. Philadelphia: Elsevier Saunders; 2006.
13. Evans SM, Judy KD, Dunphy I, et al. Hypoxia is important in the biology and aggression of human glial brain tumors. Clin Cancer Res 2004;10:8177-8184
14. Dings J, Meixensberger J, Jager A, Roosen K. Clinical experience with 118 brain tissue oxygen partial pressure catheter probes. Neurosurgery 1998; 43:1082-1095 (Pubitemid 128723302)
15. Pouyssegur J, Dayan F, Mazure NM. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 2006;441:437-443 (Pubitemid 44050138)
16. Gordan JD, Simon MC. Hypoxia-inducible factors: central regulators of the tumor phenotype. Curr Opin Genet Dev 2007;17:71-77 (Pubitemid 46109295)
17. Ivanovic Z, Hermitte F, Brunet de la Grange P, et al. Simultaneous maintenance of human cord blood SCID-repopulating cells and expansion of committed progenitors at low O2 concentration (3%). Stem Cells 2004;22:716-724
18. 2 concentration (1%) synergize to improve the maintenance of hematopoietic stem cells (pre-CFC). J Cell Physiol 2007;212:68-75.
19. Studer L, Csete M, Lee SH, et al. Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J Neurosci 2000;20:7377-7383
20. Zhang CP, Zhu LL, Zhao T, et al. Characteristics of neural stem cells expanded in lowered oxygen and the potential role of hypoxia-inducible factor-1α. Neurosignals 2006;15:259-265
21. Evans SM, Judy KD, Dunphy I, et al. Comparative measurements of hypoxia in human brain tumors using needle electrodes and EF5 binding. Cancer Res 2004;64:1886-1892.
22. Jiang H, Gomez-Manzano C, Aoki H, et al. Examination of the therapeutic potential of Delta-24-RGD in brain tumor stem cells: role of autophagic cell death. J Natl Cancer Inst 2007;99:1410-1414
23. Beier D, Hau P, Proescholdt M, et al. CD133(+) and CD133(-) glioblastomaderived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res 2007;67:4010-4015
24. Davis JM. Basic cell culture: a practical approach. In: Rickwood D, Homes BD, editors. Oxford (NY): Oxford University Press; 1994.
25. Zhang QB, Ji XY, Huang Q, et al. Differentiation profile of brain tumor stem cells: a comparative study with neural stem cells. Cell Res 2006;16:909-915
26. Eyler CE, Rich JN. Survival of the fittest: cancer stem cells in therapeutic resistance and angiogenesis. J Clin Oncol 2008;26:2839-2845
27. Covello KL, Kehler J, Yu H, et al. HIF-2α regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev 2006;20:557-570
28. Avilion AA, Nicolis SK, Pevny LH, et al. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003;17:126-140
29. Tomioka M, Nishimoto M, Miyagi S, et al. Identification of Sox-2 regulatory region which is under the control of Oct-3/4-Sox-2 complex. Nucleic Acids Res 2002;30:3202-3213
30. Clark PA, Treisman DM, Ebben J, Kuo JS. Developmental signaling pathways in brain tumor-derived stem-like cells. Dev Dyn 2007;236:3297-3308 (Pubitemid 350276387)
31. Miki J, Furusato B, Li H, et al. Identification of putative stem cell markers, CD133 and CXCR4, in hTERT-immortalized primary nonmalignant and malignant tumor-derived human prostate epithelial cell lines and in prostate cancer specimens. Cancer Res 2007;67:3153-3161
32. Monzani E, Facchetti F, Galmozzi E, et al. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer 2007; 43:935-946
33. Grayson WL, Zhao F, Bunnell B, Ma T. Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun 2007;358:948-953 (Pubitemid 46802482)
34. Pistollato F, Chen HL, Schwartz PH, Basso G, Panchision DM. Oxygen tension controls the expansion of human CNS precursors and the generation of astrocytes and oligodendrocytes. Mol Cell Neurosci 2007;35:424-435 (Pubitemid 46992832)
35. Platet N, Liu SY, Atifi ME, et al. Influence of oxygen tension on CD133 phenotype in human glioma cell cultures. Cancer Lett 2007;258:286-290
36. Danilov CA, Fiskum G. Hyperoxia promotes astrocyte cell death after oxygen and glucose deprivation. Glia 2008;56:801-808
37. Lendahl U, Zimmerman LB, McKay RD. CNS stem cells express a new class of intermediate filament protein. Cell 1990;60:585-595 (Pubitemid 20083815)
38. 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)
39. Niwa H, Miyazaki J, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 2000;24: 372-376 (Pubitemid 30187435)
40. Nichols J, Zevnik B, Anastassiadis K, et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998;95:379-391
41. Keith B, Simon MC. Hypoxia-inducible factors, stem cells, and cancer. Cell 2007;129:465-472 (Pubitemid 46660978)
42. Calabrese C, Poppleton H, Kocak M, et al. A perivascular niche for brain tumor stem cells. Cancer Cell 2007;11:69-82.
43. Woodward WA, Chen MS, Behbod F, et al. WNT/β-catenin mediates radiation resistance of mouse mammary progenitor cells. Proc Natl Acad Sci U S A 2007;104:618-623
44. Dote H, Burgan WE, Camphausen K, Tofilon PJ. Inhibition of hsp90 compromises the DNA damage response to radiation. Cancer Res 2006;66:9211-9220 (Pubitemid 44521142)
45. Van Gelder RN, von Zastrow ME, Yool A, et al. Amplified RNA synthesized from limited quantities of heterogeneous cDNA. Proc Natl Acad Sci U S A 1990; 87:1663-1667
46. Warrington JA, Nair A, Mahadevappa M, Tsyganskaya M. Comparison of human adult and fetal expression and identification of 535 housekeeping/maintenance genes. Physiol Genomics 2000;2:143-147
47. Gentleman RC, Carey VJ, Bates DM, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004; 5:R80.
48. Irizarry RA, Hobbs B, Collin F, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003; 4:249-264
49. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001;98:5116-5121 (Pubitemid 32397092)
50. Efron B, Tibshirani R. On testing the significance of sets of genes. Annals of Applied Statistics 2007;1:107-129