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

Molecular and Cellular Biology

Volumn 24, Issue 7, 2004, Pages 2875-2889

  Erler, Janine T ^a,b   Cawthorne, Christopher J ^a,b   Williams, Kaye J ^b   Koritzinsky, Marianne ^c   Wouters, Bradley G ^c   Wilson, Clare ^a   Miller, Crispin ^a   Demonacos, Costas ^b   Stratford, Ian J ^b   Dive, Caroline ^a,b,d  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d CHRISTIE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; DNA TOPOISOMERASE INHIBITOR; ETOPOSIDE; HYPOXIA INDUCIBLE FACTOR 1; OXYGEN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER; CANCER CELL; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CANCER RESISTANCE; COLON CANCER; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; FEMALE; HUMAN; HUMAN CELL; HYPOXIA; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; SOLID TUMOR;

ANIMALS; ANOXIA; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CARRIER PROTEINS; CELL LINE, TUMOR; DNA-BINDING PROTEINS; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; ETOPOSIDE; FEMALE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MICE, NUDE; NEOPLASMS; NUCLEAR PROTEINS; NUCLEIC ACID SYNTHESIS INHIBITORS; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; TRANSCRIPTION FACTORS; TRANSPLANTATION, HETEROLOGOUS;

ANIMALIA;

EID: 12144287046     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.7.2875-2889.2004     Document Type: Article

References (62)

1. Adams, J. M., and S. Cory. 1998. The Bcl-2 protein family: arbiters of cell survival. Science 281:1322-1326.
2. Akakura, N., M. Kobayashi, I. Horiuchi, A. Suzuki, J. Wang, J. Chen, H. Niizeki, K. Kawamura, M. Hosokawa, and M. Asaka. 2001. Constitutive expression of hypoxia-inducible factor-1α renders pancreatic cancer cells resistant to apoptosis induced by hypoxia and nutrient deprivation. Cancer Res. 61:6548-6554.
3. Baek, J. H., J. E. Jang, C. M. Kang, H. Y. Chung, N. D. Kim, and K. W. Kim. 2000. Hypoxia-induced VEGF enhances tumor survivability via suppression of serum deprivation-induced apoptosis. Oncogene 19:4621-4631.
4. Birner, P., M. Schindl, A. Obermair, G. Breitenecker, and G. Oberhuber. 2001. Expression of hypoxia-inducible factor 1α in epithelial ovarian tumors: its impact on prognosis and response to chemotherapy. Clin. Cancer Res. 7:1661-1668.
5. Bos, R., H. Zhong, C. F. Hanrahan, E. C. Mommers, G. L. Semenza, H. M. Pinedo, M. D. Abeloff, J. W. Simons, P. J. van Diest, and E. van der Wall. 2001. Levels of hypoxia-inducible factor-1 alpha during breast carcinogenesis. J. Natl. Cancer Inst. 93:309-314.
6. Brown, J. M., and B. Wouters. 2001. Apoptosis: mediator or mode of cell killing by anticancer drugs? Drug Resist. Updates 4:135-136.
7. Bruick, R. K. 2000. Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc. Natl. Acad. Sci. USA 97:9082-9087.
8. Carmeliet, P., Y. Dor, J. M. Herbert, D. Fukumura, K. Brusselmans, M. Dewerchin, M. Neeman, F. Bono, R. Abramovitch, P. Maxwell, C. J. Koch, P. Ratcliffe, L. Moons, R. K. Jain, D. Collen, E. Keshert, and E. Keshet. 1998. Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394:485-490.
9. Cheng, E. H., M. C. Wei, S. Weiler, R. A. Flavell, T. W. Mak, T. Lindsten, and S. J. Korsmeyer. 2001. BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol. Cell 8:705-711.
10. Degli Esposti, M., J. T. Erler, J. A. Hickman, and C. Dive. 2001. Bid, a widely expressed proapoptotic protein of the Bcl-2 family, displays lipid transfer activity. Mol. Cell. Biol. 21:7268-7276.
11. DePreter, K., F. Speleman, V. Combaret, J. Lunec, G. Lautreys, B. H. Eussen, N. Francotte, J. Board, A. D. Pearson, A. De Paepe, N. Van Roy, and J. Vandesompele. 2002. Quantification of MYCN, DDX1 and NAG gene copy number in neuroblastoma using real time quantitative PCR assay. Mod. Pathol. 15:59-66.
12. Dive, C., and J. A. Hickman. 1991. Drug target interactions: only the first step in the commitment of a cell to a programmed cell death. Br. J. Cancer 64:192-196.
13. Dong, Z., M. A. Venkatachalam, J. Wang, Y. Patel, P. Saikumar, G. L. Semenza, T. Force, and J. Nishiyana. 2001. Up-regulation of apoptosis inhibitory protein IAP-2 by hypoxia. HIF-1-independent mechanisms. J. Biol. Chem. 276:18702-18709.
14. Eskes, R., S. Desagher, B. Antonsson, and J.-C. Martinou. 2000. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol. Cell. Biol. 20:929-935.
15. Graeber, T. G., C. Osmanian, T. Jacks, D. E. Housman, S. J. Koch, S. W. Lowe, and A. J. Giaccia. 1996. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379:88-91.
16. Griffiths, J. R., P. M. McSheehy, S. P. Robinson, H. Troy, Y. L. Chung, R. D. Leek, K. J. Williams, I. J. Stratford, A. L. Harris, and M. Stubbs. 2002. Metabolic changes detected by in vivo magnetic resonance studies of HEPA-1 wild-type tumors and tumors deficient in hypoxia-inducible factor-1beta (HIF-1beta): evidence of an anabolic role for the HIF-1 pathway. Cancer 62:688-695.
17. Guo, K., G. Searfossm, D. Krolikowskim, M. Pagnoni, C. Granksm, K. Clark, K. T. Yu, M. Jaye, and Y. Ivashchenko. 2001. Hypoxia induces the expression of the pro-apoptotic gene BNIP3. Cell Death Differ. 8:367-376.
18. Hopfl, G., R. H. Wenger, U. Ziegler, T. Stallmach, O. Gardelle, R. Achermann, M. Wergin, B. Kaser-Hotz, H. M. Saunders, K. Williams, I. Stratford, M. Gassman, and I. Desbaillets. 2002. Rescue of hypoxia-inducible factor-1alpha-deficient tumor growth by wild-type cells is independent of vascular endothelial growth factor. Cancer Res. 62:2962-2970.
19. Jiang, B. H., F. Agani, A. Passaniti, and G. L. Semenza. 1997. V-Src induces expression of hypoxia-inducible factor 1 (HIF-1) and transcription of genes encoding vascular endothelial growth factor and enolase 1: involvement of HIF-1 in tumour progression. Cancer Res. 57:5328-5335.
20. Johnstone, R. W., A. A. Ruefi, and S. W. Lowe. 2002. Apoptosis: a link between cancer genetics and chemotherapy. Cell 108:153-164.
21. Kalra, R., A.-M. Jones, J. Kirk, G. E. Adams, and I. J. Stratford. 1993. The effect of hypoxia on acquired drug resistance and response to epidermal growth factor in Chinese hamster lung fibroblasts and human breast cancer cells in vitro. Int. J. Cancer 54:650-655.
22. Kinoshita, M., D. L. Johnson, C. H. Shatney, Y. L. Lee, and H. Mochizuki. 2001. Cancer cells surviving hypoxia obtain hypoxia resistance and maintain anti-apoptotic potential under reoxygenation. Int. J. Cancer 91:322-326.
23. Koumenis, C., C. Naczki, M. Koritzinsky, S. Rastani, A. Diehl, N. Sonenberg, A. Koromilas, and B. G. Wouters. 2002. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2α. Mol. Cell. Biol. 22:7405-7416.
24. LeBlanc, H., D. Lawrence, E. Varfolomeev, K. Totpal, J. Morlan, P. Schow, S. Fong, R. Schwall, D. Sinicropi, and A. Ashkenazi. 2002. Tumor-cell resistance to death receptor-induced apoptosis through mutational inactivation of the proapoptotic Bcl-2 homolog Bax. Nat. Med. 8:274-281.
25. Letai, A., M. C. Bassik, L. D. Walensky, M. D. Sorcinelli, S. Weiler, and J. Korsmeyer. 2002. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2:183-192.
26. Makin, G., and C. Dive. 2001. Apoptosis and cancer chemotherapy. Trends Cell Biol. 11:S22-S26.
27. Maxwell, P. H., G. U. Dachs, J. M. Gleadle, L. G. Nicholls, A. L. Harris, I. J. Stratford, O. Hankinson, C. W. Pugh, and P. Ratcliffe. 1997. Hypoxia-inducible factor-1 modulates gene expression in solid tumours and influences both angiogenesis and tumour growth. Proc. Natl. Acad. Sci. USA 94:8104-8109.
28. McClintock, D. S., M. T. Santore, V. Y. Lee, J. Brunelle, G. R. Scott Bidinger, W.-X. Zong, C. B. Thompson, N. Hay, and N. S. Chandel. 2002. Bcl-2 family members and functional electron transport chain regulate oxygen deprivation-induced cell death. Mol. Cell. Biol. 22:94-104.
29. Narravula, S., and S. P. Colgan. 2001. Hypoxia-inducible factor 1-mediated inhibition of peroxisome proliferator-activated receptor α expression during hypoxia. J. Immunol. 166:7543-7548.
30. Park, S. Y., T. R. Billiar, and D. W. Seol. 2002. Hypoxia inhibition of apoptosis induced by tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). Biochem. Biophys. Res. Commun. 291:150-153.
31. Raleigh, J. A., S. C. Chou, G. E. Arteel, and M. R. Horsman. 1999. Comparisons among pimonidazole binding, oxygen electrode measurements, and radiation response in C3H mouse tumors. Radiat. Res. 151:580-589.
32. Rampino, N., H. Yamamoto, Y. Ionov, Y. Li, H. Sawai, J. C. Reed, and M. Perucho. 1997. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science 275:967-969.
33. Ryan, H. E., J. Lo, and R. S. Johnson. 1998. HIF-1α is required for solid tumor formation and embryonic vascularization. EMBO J. 17:3005-3015.
34. Ryan, H. E., M. Poloni, W. McNutty, D. Elson, M. Grassmann, J. M. Arbeit, and R. S. Johnson. 2000. Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res. 60:4010-4015.
35. Sax, J. K., P. Fei, M. E. Murphy, E. Bernhard, S. J. Korsmeyer, and W. S. El-Deiry. 2002. BID regulation by p53 contributes to chemosensitivity. Nat. Cell Biol. 4:842-849.
36. Scaffidi, C., I. Schmitz, J. Zha, S. J. Korsmeyer, P. H. Krammer, and M. E. Peter. 1999. Differential modulation of apoptosis sensitivity in CD95 type I and type II cells. J. Biol. Chem. 6:22532-22538.
37. Schmitt, C. A., and S. W. Lowe. 2001. Apoptosis is critical for drug response in vivo. Drug Resist. Updates 4:132-134.
38. Semenza, G. L., B. H. Jiang, S. W. Leung, R. Passantino, J. P. Concordet, P. Maire, and A. Giallongo. 1996. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J. Biol. Chem. 271:32529-32537.
39. Semenza, G. L. 2002. HIF-1 and tumour progression: pathophysiology and therapeutics. Trends Mol. Med. 8:S62-S67.
40. Smith, E., I. J. Stratford, and G. E. Adams. 1980. Cytotoxicity of adriamycin on aerobic and hypoxic Chinese hamster V79 cells in vitro. Br. J. Cancer 41:568-573.
41. Sowter, H. S., P. J. Ratcliffe, P. Watson, A. H. Greenberg, and A. L. Harris. 2001. HIF-1-dependent regulation of hypoxic induction of cell death factors BNIP3 and NIX in human tumors. Cancer Res. 61:6669-6673.
42. Stratford, I. J., A. V. Patterson, G. U. Dachs, B. Telfer, and K. Williams. 1999. Hypoxia-mediated gene expression, p. 107-113. In P. Vaupel and D. K. Kelleher (ed.), Tumour hypoxia: pathophysiology, clinical significance and therapeutic perspectives. Wissenchaftliche Verlagsgeselschaft GmbH, Stuttgart, Germany.
43. Sui, G., C. Soohoo, E. B. Affar, F. Gay, Y. Shi, W. C. Forrester, and Y. Shi. 2002. A DNA vector-based RNAi technology to suppress gene expression in mammalian cells. Proc. Natl. Acad. Sci. USA 99:5515-5520.
44. Swanson, H. I. 2002. DNA binding and protein interactions of the AHR/ ARNT heterodimer that facilitate gene activation. Chem.-Biol. Interact. 141:63-76.
45. Teicher, B. A. 1994. Hypoxia and drug resistance. Cancer Metastasis Rev. 13:139-168.
46. Theodorakis, P., E. Lomonosova, and D. Chinnadurai. 2002. Critical requirement of BAX for manifestation of apoptosis induced by multiple stimuli in human epithelial cancer cells. Cancer Res. 62:3373-3376.
47. Thomas, D. A., L. Scorrano, G. V. Putcha, S. J. Korsmeyer, and T. J. Ley. 2001. Granzyme B can cause mitochondrial depolarisation and cell death in the absence of BID, BAX and BAK. Proc. Natl. Acad. Sci. USA 98:14985-14990.
48. Violette, S., L. Poulain, E. Dussaulx, D. Pepin, A. M. Faussat, J. Chambaz, J. M. Lacorte, C. Staedel, and T. Lesuffieur. 2002. Resistance of colon cancer cells to long-term 5-fluorouracil exposure is correlated to the relative level of Bcl-2, Bcl-xl in addition to BAX and p53 status. Int. J. Cancer 98:498-504.
49. Wang, G. 1995. Hypoxia-inducible factor 1 is a basic helix-loop-helix-PAS heterodimer regulated by cellular oxygen tension. Proc. Natl. Acad. Sci. USA 92:5510-5514.
50. Wei, M. C., T. Lindsten, V. K. Mootha, S. Weiler, A. Gross, M. Ashiya, C. B. Thompson, and S. J. Korsmeyer. 2000. tBid, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 14:2060-2071.
51. Wei, M. C., W. X. Zong, E. H. Cheng, T. Lindsten, V. Panoutsakopoulou, A. J. Ross, K. A. Roth, G. R. MacGregor, C. B. Thompson, and S. J. Korsmeyer. 2001. Pro-apoptotic Bax and Bak: a requisite gateway to mitochondrial dysfunction and death. Science 292:727-730.
52. Wenger, R. H., and M. Gassman. 1997. Oxygen(es) and the hypoxia-inducible factor-1. Biol. Chem. 378:609-616.
53. West, C., I. J. Stratford, N. Barrass, and E. Smith. 1981. A comparison of adriamycin and mAMSA in vitro: cell lethality and sister chromatid exchange studies. Br. J. Cancer 44:798-809.
54. Williams, K. J., B. A. Telfer, R. E. Airley, H. P. Peters, M. R. Sheridan, A. J. van der Kogel, A. L. Harris, and I. J. Stratford. 2002. A protective role for HIF-1 in response to redox manipulation and glucose deprivation: implications for tumorigenesis. Oncogene 21:282-290.
55. Wood, S. M., M. S. Wiesener, K. M. Yeates, N. Okada, C. W. Pugh, P. H. Maxwell, and P. J. Ratcliffe. 1998. Selection and analysis of a mutant cell line defective in the hypoxia-inducible factor-1α-subunit (HIF-1α). J. Biol. Chem. 273:8360-8368.
56. Wykoff, C. C., N. J. Beasley, P. H. Watson, K. J. Turner, J. Pastorek, A. Sibtain, G. D. Wilson, H. Turley, K. L. Talks, P. H. Maxwell, C. W. Pugh, P. J. Ratcliffe, and A. L. Harris. 2000. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res. 60:7075-7083.
57. Wykoff, C. C., C. W. Pugh, A. L. Harris, P. H. Maxwell, and P. J. Ratcliffe. 2001. The HIF pathway: implications for patterns of gene expression in cancer. Novartis Found. Symp. 240:212-225.
58. Yang, E., J. Zha, J. Jockel, L. H. Boise, C. B. Thompson, and S. J. Korsmeyer. 1995. Bad, a heterodimeric partner for Bcl-xL and Bcl-2, displaces Bax and promotes cell death. Cell 80:285-291.
59. Zhang, L., J. Yu, B. H. Park, K. W. Kinzler, and B. Vogelstein. 2000. Role of BAX in the apoptotic response to anticancer agents. Science 290:989-992.
60. Zhong, H., F. Agani, A. A. Baccala, E. Laughner, N. Rioseco-Camacho, W. B. Isaacs, J. W. Simons, and G. L. Semenza. 1998. Increased expression of hypoxia-inducible factor-1α in rat and human prostate cancer. Cancer Res. 58:5280-5284.
61. Zhong, H., A. M. De Marzom, E. Laughnerm, M. Lim, D. A. Hilton, D. Zagzag, P. Buechler, W. B. Isaacs, G. L. Semenza, and J. W. Simons. 1999. Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res. 59:5830-5835.
62. Zhong, H., and J. W. Simons. 1999. Direct comparison of GAPDH, beta-actin, cyclophilin, and 28S rRNA as internal standards for quantifying RNA levels under hypoxia. Biochem. Biophys. Res. Commun. 259:523-526.