Anoxia is necessary for tumor cell toxicity caused by a low-oxygen environment

Cancer Research

Volumn 65, Issue 8, 2005, Pages 3171-3178

  Papandreou, Ioanna ^a   Krishna, Chaya ^a   Kaper, Fiona ^a   Cai, Deli ^a   Giaccia, Amato J ^a   Denko, Nicholas C ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CCSR South   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; HYPOXIA INDUCIBLE FACTOR 1; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANOXIA; APOPTOSIS; ARTICLE; BNIP3 GENE; BNIP3L GENE; CELL DEATH; CELL GROWTH; CHROMATIN CONDENSATION; COLONY FORMATION; CONTROLLED STUDY; CYTOTOXICITY; EMBRYO; ENZYME ACTIVATION; FIBROBLAST; GENE; GENE FUNCTION; GENE INDUCTION; GENE OVEREXPRESSION; GENE TARGETING; GENOTOXICITY; HUMAN; HUMAN CELL; HYPOXIA; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; OXYGEN CONCENTRATION; PRIORITY JOURNAL; PROTEIN INDUCTION; TUMOR CELL;

EID: 17144416875     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-04-3395     Document Type: Article

References (44)

1. Vaupel P, Thews O, Hoeckel M. Treatment resistance of solid tumors: role of hypoxia and anemia. Med Oncol 2001;18:243-59.
2. Parrinello S, Samper E, Krtolica A, Goldstein J, Melov S, Campisi J. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat Cell Biol 2003;5:741-7.
3. Graeber TG, Osmanian C, Jacks T, et al. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 1996;379:88-91.
4. Yao KS, Clayton M, O'Dwyer PJ. Apoptosis in human adenocarcinoma HT29 cells induced by exposure to hypoxia. J Natl Cancer Inst 1995;87:117-22.
5. Hockel M, Schlenger K, Hockel S, Vaupel P. Hypoxic cervical cancers with low apoptotic index are highly aggressive. Cancer Res 1999;59:4525-8.
6. Brunelle JK, Santore MT, Budinger GR, et al. c-Myc sensitization to oxygen deprivation-induced cell death is dependent on Bax/Bak, but is independent of p53 and hypoxia-inducible factor-1. J Biol Chem 2004;279:4305-12.
7. Alarcon RM, Denko NC, Giaccia AJ. Genetic determinants that influence hypoxia-induced apoptosis. Novartis Found Symp 2001;240:115-28; discussion 128-32.
8. Soengas MS, Alarcon RM, Yoshida H, et al. Apaf-1 and caspase-9 in p53-dependent apoptosis and tumor inhibition. Science 1999;284:156-9.
9. Shimizu S, Eguchi Y, Kosaka H, Kamiike W, Matsuda H, Tsujimoto Y. Prevention of hypoxia-induced cell death by Bcl-2 and Bcl-xL. Nature 1995;374:811-3.
10. McClintock DS, Santore MT, Lee VY, et al. Bcl-2 family members and functional electron transport chain regulate oxygen deprivation-induced cell death. Mol Cell Biol 2002;22:94-104.
11. Yu J, Wang Z, Kinzler KW, Vogelstein B, Zhang L. PUMA mediates the apoptotic response to p53 in colorectal cancer cells. Proc Natl Acad Sci U S A 2003;100:1931-6.
12. Kim JY, Ahn HJ, Ryu JH, Suk K, Park JH. BH3-only protein noxa is a mediator of hypoxic cell death induced by hypoxia-inducible factor 1{α}. J Exp Med 2004;199:113-24.
13. Erler JT, Cawthorne CJ, Williams KJ, et al. Hypoxia-mediated down-regulation of Bid and Bax in tumors occurs via hypoxia-inducible factor 1-dependent and -independent mechanisms and contributes to drug resistance. Mol Cell Biol 2004;24:2875-89.
14. Ozawa K, Kuwabara K, Tamatani M, et al. 150-kDa oxygen-regulated protein (ORP150) suppresses hypoxia-induced apoptotic cell death. J Biol Chem 1999;274:6397-404.
15. Dong Z, Venkatachalam MA, Wang J, et al. Up-regulation of apoptosis inhibitory protein IAP-2 by hypoxia. Hif-1-independent mechanisms. J Biol Chem 2001;276:18702-9.
16. Bruick RK. Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc Natl Acad Sci U S A 2000;97:9082-7.
17. Kothari S, Cizeau J, McMillan-Ward E, et al. BNIP3 plays a role in hypoxic cell death in human epithelial cells that is inhibited by growth factors EGF and IGF. Oncogene 2003;22:4734-44.
18. Imazu T, Shimizu S, Tagami S, et al. Bcl-2/E1B 19 kDa-interacting protein 3-like protein (Bnip3L) interacts with bcl-2/Bcl-xL and induces apoptosis by altering mitochondrial membrane permeability. Oncogene 1999;18:4523-9.
19. Chen G, Cizeau J, Vande Velde C, et al. Nix and Nip3 form a subfamily of pro-apoptotic mitochondrial proteins. J Biol Chem 1999;274:7-10.
20. Chen G, Ray R, Dubik D, et al. The E1B 19K/Bcl-2-binding protein Nip3 is a dimeric mitochondrial protein that activates apoptosis. J Exp Med 1997;186:1975-83.
21. Kubasiak LA, Hernandez OM, Bishopric NH, Webster KA. Hypoxia and acidosis activate cardiac myocyte death through the Bcl-2 family protein BNIP3. Proc Natl Acad Sci U S A 2002;99:12825-30.
22. Matsushima M, Fujiwara T, Takahashi E, et al. Isolation, mapping, and functional analysis of a novel human cDNA (BNIP3L) encoding a protein homologous to human NIP3. Genes Chromosomes Cancer 1998;21:230-5.
23. Ohi N, Tokunaga A, Tsunoda H, et al. A novel adenovirus E1B19K-binding protein B5 inhibits apoptosis induced by Nip3 by forming a heterodimer through the C-terminal hydrophobic region. Cell Death Differ 1999;6:314-25.
24. Vande Velde C, Cizeau J, Dubik D, et al. BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol Cell Biol 2000;20:5454-68.
25. Yasuda M, Han JW, Dionne CA, Boyd JM, Chinnadurai G. BNIP3α: a human homolog of mitochondrial proapoptotic protein BNIP3. Cancer Res 1999;59:533-7.
26. Daido S, Kanzawa T, Yamamoto A, Takeuchi H, Kondo Y, Kondo S. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res 2004;64:4286-93.
27. Chan DA, Sutphin PD, Denko NC, Giaccia AJ. Role of prolyl hydroxylation in oncogenically stabilized hypoxia-inducible factor-1α. J Biol Chem 2002;277:40112-7.
28. Romero-Ramirez L, Cao H, Neison D, et al. XBP1 is essential for survival under hypoxic conditions and is required for tumor growth. Cancer Res 2004;64:5943-7.
29. Mazzarella RA, Green M. ERp99, an abundant, conserved glycoprotein of the endoplasmic reticulum, is homologous to the 90-kDa heat shock protein (hsp90) and the 94-kDa glucose regulated protein (GRP94). J Biol Chem 1987;262:8875-83.
30. Li F, Ambrosini G, Chu EY, et al. Control of apoptosis and mitotic spindle checkpoint by survivin. Nature 1998;396:580-4.
31. Masson N, Willam C, Maxwell PH, Pugh CW, Ratcliffe PJ. Independent function of two destruction domains in hypoxia-inducible factor-α chains activated by prolyl hydroxylation. EMBO J 2001;20:5197-206.
32. Mack FA, Rathmell WK, Arsham AM, Gnarra J, Keith B, Simon MC. Loss of pVHL is sufficient to cause HIF dysregulation in primary cells but does not promote tumor growth. Cancer Cell 2003;3:75-88.
33. Sowter HM, Ratcliffe PJ, Watson P, Greenberg AH, Harris AL. HIF-1-dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors. Cancer Res 2001;61:6669-73.
34. Lee MJ, Kim JY, Suk K, Park JH. Identification of the hypoxia-inducible factor 1 α-responsive HGTD-P gene as a mediator in the mitochondrial apoptotic pathway. Mol Cell Biol 2004;24:3918-27.
35. Yussman MG, Toyokawa T, Odley A, et al. 2nd Mitochondrial death protein Nix is induced in cardiac hypertrophy and triggers apoptotic cardiomyopathy. Nat Med 2002;8:725-30.
36. Zhou M, Gu L, Li F, Zhu Y, Woods WG, Findley HW. DNA damage induces a novel p53-survivin signaling pathway regulating cell cycle and apoptosis in acute lymphoblastic leukemia cells. J Pharmacol Exp Ther 2002;303:124-31.
37. Mirza A, McGuirk M, Hockenberry TN, et al. Human survivin is negatively regulated by wild-type p53 and participates in p53-dependent apoptotic pathway. Oncogene 2002;21:2613-22.
38. Lee AS. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem Sci 2001;26:504-10.
39. Reddy RK, Mao C, Baumeister P, Austin RC, Kaufman RJ, Lee AS. Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation. J Biol Chem 2003;278:20915-24.
40. Jamora C, Dennert G, Lee AS. Inhibition of tumor progression by suppression of stress protein GRP78/BiP induction in fibrosarcoma B/C10ME. Proc Natl Acad Sci U S A 1996;93:7690-4.
41. Koong AC, Chen EY, Lee AS, Brown JM, Giaccia AJ. Increased cytotoxicity of chronic hypoxic cells by molecular inhibition of GRP78 induction. Int J Radiat Oncol Biol Phys 1994;28:661-6.
42. Song MS, Park YK, Lee JH, Park K. Induction of glucose-regulated protein 78 by chronic hypoxia in human gastric tumor cells through a protein kinase C-epsilon/ERK/AP-1 signaling cascade. Cancer Res 2001;61:8322-30.
43. Evans SM, Hahn SM, Magarelli DP, Koch CJ. Hypoxic heterogeneity in human tumors: EF5 binding, vasculature, necrosis, and proliferation. Am J Clin Oncol 2001;34:467-72.
44. Vaupel P, Kallinowski F, Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res 1989;49:6449-65.