Hypoxia inducible factor-1α inactivation unveils a link between tumor cell metabolism and hypoxia-induced cell death

American Journal of Pathology

Volumn 173, Issue 4, 2008, Pages 1186-1201

  Favaro, Elena ^a   Nardo, Giorgia ^a   Persano, Luca ^a   Masiero, Massimo ^a   Moserle, Lidia ^a   Zamarchi, Rita ^b   Rossi, Elisabetta ^a   Esposito, Giovanni ^b   Plebani, Mario ^a,b   Sattler, Ulrike ^c   Mann, Thomas ^c   Mueller Klieser, Wolfgang ^c   Ciminale, Vincenzo ^a   Amadori, Alberto ^a,b   Indraccolo, Stefano ^b  

^a UNIVERSITY OF PADOVA   (Italy)

^b VENETO INSTITUTE OF ONCOLOGY IOV IRCCS   (Italy)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; GLUCOSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CELL CYCLE ARREST; CELL DEATH; CELL METABOLISM; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; GLYCOLYSIS; HUMAN; HUMAN CELL; HYPOXIA; IMAGING; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; VASCULARIZATION;

EID: 53149153157     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2008.071183     Document Type: Article

References (55)

1. Harris AL: Hypoxia-a key regulatory factor in tumour growth. Nat Rev Cancer 2002, 2:38-47
2. Fenton BM, Paoni SF, Ding I: Effect of VEGF receptor-2 antibody on vascular function and oxygenation in spontaneous and transplanted tumors. Radiother Oncol 2004, 72:221-230
3. Franco M, Man S, Chen L, Emmenegger U, Shaked Y, Cheung AM, Brown AS, Hicklin DJ, Foster FS, Kerbel RS: Targeted anti-vascular endothelial growth factor receptor-2 therapy leads to short-term and long-term impairment of vascular function and increase in tumor hypoxia. Cancer Res 2006, 66:3639-3648
4. Winkler F, Kozin SV, Tong RT, Chae SS, Booth MF, Garkavtsev I, Xu L, Hicklin DJ, Fukumura D, di Tomaso E, Munn LL, Jain RK: Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 2004, 6:553-563
5. Ferrara N, Kerbel RS: Angiogenesis as a therapeutic target. Nature 2005, 438:967-974
6. Semenza GL: Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003, 3:721-732
7. Bacon AL, Harris AL: Hypoxia-inducible factors and hypoxic cell death in tumour physiology. Ann Med 2004, 36:530-539
8. Pouyssegur J, Dayan F, Mazure NM: Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 2006, 441:437-443
9. Gatenby RA, Gillies RJ: Why do cancers have high aerobic glycolysis? Nat Rev Cancer 2004, 4:891-899
10. Warburg O: On respiratory impairment in cancer cells. Science 1956, 124:269-270
11. Bos R, van Der Hoeven JJ, van Der Wall E, van Der Groep P, van Diest PJ, Comans EF, Joshi U, Semenza GL, Hoekstra OS, Lammertsma AA, Molthoff CF: Biologic correlates of (18)fluorodeoxyglucose uptake in human breast cancer measured by positron emission tomography. J Clin Oncol 2002, 20:379-387
12. Papandreou I, Krishna C, Kaper F, Cai D, Giaccia AJ, Denko NC: Anoxia is necessary for tumor cell toxicity caused by a low-oxygen environment. Cancer Res 2005, 65:3171-3178
13. Amellem O, Stokke T, Sandvik JA, Smedshammer L, Pettersen EO: Hypoxia-induced apoptosis in human cells with normal p53 status and function, without any alteration in the nuclear protein level. Exp Cell Res 1997, 232:361-370
14. Araya R, Uehara T, Nomura Y: Hypoxia induces apoptosis in human neuroblastoma SK-N-MC cells by caspase activation accompanying cytochrome c release from mitochondria. FEBS Lett 1998, 439:168-172
15. Brunelle JK, Santore MT, Budinger GR, Tang Y, Barrett TA, Zong WX, Kandel E, Keith B, Simon MC, Thompson CB, Hay N, Chandel NS: 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, 279:4305-4312
16. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW, Giaccia AJ: Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 1996, 379:88-91
17. Hockel M, Schlenger K, Hockel S, Vaupel P: Hypoxic cervical cancers with low apoptotic index are highly aggressive. Cancer Res 1999, 59:4525-4528
18. Steinbach JP, Wolburg H, Klumpp A, Probst H, Weller M: Hypoxia-induced cell death in human malignant glioma cells: energy deprivation promotes decoupling of mitochondrial cytochrome c release from caspase processing and necrotic cell death. Cell Death Differ 2003, 10:823-832
19. Yao KS, Clayton M, O'Dwyer PJ: Apoptosis in human adenocarcinoma HT29 cells induced by exposure to hypoxia. J Natl Cancer Inst 1995, 87:117-122
20. Indraccolo S, Tisato V, Agata S, Moserle L, Ferrari S, Callegaro M, Persano L, Palma MD, Scaini MC, Esposito G, Fassina A, Nicoletto O, Plebani M, Chieco-Bianchi L, Amadori A, D'Andrea E, Montagna M: Establishment and characterization of xenografts and cancer cell cultures derived from BRCA1-/- epithelial ovarian cancers. Eur J Cancer 2006, 42:1475-1483
21. Razorenova OV, Ivanov AV, Budanov AV, Chumakov PM: Virus-based reporter systems for monitoring transcriptional activity of hypoxia-inducible factor 1. Gene 2005, 350:89-98
22. Indraccolo S, Habeler W, Tisato V, Stievano L, Piovan E, Tosello V, Esposito G, Wagner R, Uberla K, Chieco-Bianchi L, Amadori A: Gene transfer in ovarian cancer cells: a comparison between retroviral and lentiviral vectors. Cancer Res 2002, 62:6099-6107
23. Indraccolo S, Tisato V, Tosello V, Habeler W, Esposito G, Moserle L, Stievano L, Persano L, Chieco-Bianchi L, Amadori A: Interferon-alpha gene therapy by lentiviral vectors contrasts ovarian cancer growth through angiogenesis inhibition. Hum Gene Ther 2005, 16:957-970
24. Indraccolo S, Stievano L, Minuzzo S, Tosello V, Esposito G, Piovan E, Zamarchi R, Chieco-Bianchi L, Amadori A: Interruption of tumor dormancy by a transient angiogenic burst within the tumor microenvironment. Proc Natl Acad Sci USA 2006, 103:4216-4221
25. Walenta S, Schroeder T, Mueller-Klieser W: Metabolic mapping with bioluminescence: basic and clinical relevance. Biomol Eng 2002, 18:249-262
26. Walenta S, Schroeder T, Mueller-Klieser W: Lactate in solid malignant tumors: potential basis of a metabolic classification in clinical oncology. Curr Med Chem 2004, 11:2195-2204
27. Goda N, Ryan HE, Khadivi B, McNulty W, Rickert RC, Johnson RS: Hypoxia-inducible factor 1alpha is essential for cell cycle arrest during hypoxia. Mol Cell Biol 2003, 23:359-369
28. Koshiji M, Huang LE: Dynamic balancing of the dual nature of HIF-1alpha for cell survival. Cell Cycle 2004, 3:853-854
29. Wang G, Reisdorph R, Clark RE Jr, Miskimins R, Lindahl R, Miskimins WK: Cyclin dependent kinase inhibitor p27(Kip1) is up-regulated by hypoxia via an ARNT dependent pathway. J Cell Biochem 2003, 90:548-560
30. Koshiji M, Kageyama Y, Pete EA, Horikawa I, Barrett JC, Huang LE: HIF-1alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J 2004, 23:1949-1956
31. 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
32. Quennet V, Yaromina A, Zips D, Rosner A, Walenta S, Baumann M, Mueller-Klieser W: Tumor lactate content predicts for response to fractionated irradiation of human squamous cell carcinomas in nude mice. Radiother Oncol 2006, 81:130-135
33. Greijer AE, van der Wall E: The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis. J Clin Pathol 2004, 57:1009-1014
34. Piret JP, Mottet D, Raes M, Michiels C: Is HIF-1alpha a pro- or an anti-apoptotic protein? Biochem Pharmacol 2002, 64:889-892
35. Nakayama K, Kanzaki A, Hata K, Katabuchi H, Okamura H, Miyazaki K, Fukumoto M, Takebayashi Y: Hypoxia-inducible factor 1 alpha (HIF-1 alpha) gene expression in human ovarian carcinoma. Cancer Lett 2002, 176:215-223
36. Birner P, Schindl M, Obermair A, Breitenecker G, Oberhuber G: Expression of hypoxia-inducible factor 1alpha in epithelial ovarian tumors: its impact on prognosis and on response to chemotherapy. Clin Cancer Res 2001, 7:1661-1668
37. Zhong H, De Marzo AM, Laughner E, Lim M, Hilton DA, Zagzag D, Buechler P, Isaacs WB, Semenza GL, Simons JW: Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res 1999, 59:5830-5835
38. Matoba S, Kang JG, Patino WD, Wragg A, Boehm M, Gavrilova O, Hurley PJ, Bunz F, Hwang PM: p53 regulates mitochondrial respiration. Science 2006, 312:1650-1653
39. Callahan DJ, Engle MJ, Volpe JJ: Hypoxic injury to developing glial cells: protective effect of high glucose. Pediatr Res 1990, 27:186-190
40. Saikumar P, Dong Z, Patel Y, Hall K, Hopfer U, Weinberg JM, Venkatachalam MA: Role of hypoxia-induced Bax translocation and cytochrome c release in reoxygenation injury. Oncogene 1998, 17:3401-3415
41. Malhotra R, Brosius FC, 3rd: Glucose uptake and glycolysis reduce hypoxia-induced apoptosis in cultured neonatal rat cardiac myocytes. J Biol Chem 1999, 274:12567-12575
42. Kim JW, Tchernyshyov I, Semenza GL, Dang CV: HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006, 3:177-185
43. Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC: HIF-1 mediates adaptation to hypoxia by actively down-regulating mitochondrial oxygen consumption. Cell Metab 2006, 3:187-197
44. Blouw B, Song H, Tihan T, Bosze J, Ferrara N, Gerber HP, Johnson RS, Bergers G: The hypoxic response of tumors is dependent on their microenvironment. Cancer Cell 2003, 4:133-146
45. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain RK, Collen D, Keshert E: Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 1998, 394:485-490
46. Leek RD, Stratford I, Harris AL: The role of hypoxia-inducible factor-1 in three-dimensional tumor growth, apoptosis, and regulation by the insulin-signaling pathway. Cancer Res 2005, 65:4147-4152
47. 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
48. Chen J, Zhao S, Nakada K, Kuge Y, Tamaki N, Okada F, Wang J, Shindo M, Higashino F, Takeda K, Asaka M, Katoh H, Sugiyama T, Hosokawa M, Kobayashi M: Dominant-negative hypoxia-inducible factor-1 alpha reduces tumorigenicity of pancreatic cancer cells through the suppression of glucose metabolism. Am J Pathol 2003, 162:1283-1291
49. Li J, Shi M, Cao Y, Yuan W, Pang T, Li B, Sun Z, Chen L, Zhao RC: Knockdown of hypoxia-inducible factor-1alpha in breast carcinoma MCF-7 cells results in reduced tumor growth and increased sensitivity to methotrexate. Biochem Biophys Res Commun 2006, 342:1341-1351
50. Li L, Lin X, Staver M, Shoemaker A, Semizarov D, Fesik SW, Shen Y: Evaluating hypoxia-inducible factor-1alpha as a cancer therapeutic target via inducible RNA interference in vivo. Cancer Res 2005, 65:7249-7258
51. Mizukami Y, Jo WS, Duerr EM, Gala M, Li J, Zhang X, Zimmer MA, Iliopoulos O, Zukerberg LR, Kohgo Y, Lynch MP, Rueda BR, Chung DC: Induction of interleukin-8 preserves the angiogenic response in HIF-1alpha-deficient colon cancer cells. Nat Med 2005, 11:992-997
52. Ryan HE, Poloni M, McNulty W, Elson D, Gassmann M, Arbeit JM, Johnson RS: Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res 2000, 60:4010-4015
53. Stoeltzing O, McCarty MF, Wey JS, Fan F, Liu W, Belcheva A, Bucana CD, Semenza GL, Ellis LM: Role of hypoxia-inducible factor 1alpha in gastric cancer cell growth, angiogenesis, and vessel maturation. J Natl Cancer Inst 2004, 96:946-956
54. Burger RA: Experience with bevacizumab in the management of epithelial ovarian cancer. J Clin Oncol 2007, 25:2902-2908
55. Melillo G: Inhibiting hypoxia-inducible factor 1 for cancer therapy. Mol Cancer Res 2006, 4:601-605 1202-1209