Hypoxia protects HepG2 cells against etoposide-induced apoptosis VIA a HIF-1-independent pathway

Experimental Cell Research

Volumn 312, Issue 15, 2006, Pages 2908-2920

  Piret, Jean Pascal ^a   Cosse, Jean Philippe ^a   Ninane, Noelle ^a   Raes, Martine ^a   Michiels, Carine ^a  

^a UNIVERSITY OF NAMUR   (Belgium)

Author keywords

AP 1; Apoptosis; Cancer cells; Etoposide; HIF 1; Hypoxia; Resistance

Indexed keywords

CASPASE; DNA FRAGMENT; ETOPOSIDE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; TRANSCRIPTION FACTOR AP 1;

ANALYTIC METHOD; APOPTOSIS; ARTICLE; CELL ASSAY; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HYPOXIA; PARAMETER; PRIORITY JOURNAL;

EID: 33747376305     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2006.05.018     Document Type: Article

References (50)

1. Bussink J., Kaanders J.H., and van der Kogel A.J. Tumor hypoxia at the micro-regional level: clinical relevance and predictive value of exogenous and endogenous hypoxic cell markers. Radiother. Oncol. 67 (2003) 3-15
2. Hockel M., Schlenger K., Aral B., Mitze M., Schaffer U., and Vaupel P. Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res. 56 (1996) 4509-4515
3. Vaupel P., and Harrison L. Tumor hypoxia: causative factors, compensatory mechanisms, and cellular response. Oncologist 9 Suppl. 5 (2004) 4-9
4. Teicher B.A., Holden S.A., al-Achi A., and Herman T.S. Classification of antineoplastic treatments by their differential toxicity toward putative oxygenated and hypoxic tumor subpopulations in vivo in the FSaIIC murine fibrosarcoma. Cancer Res. 50 (1990) 3339-3344
5. Ivan M., Kondo K., Yang H., Kim W., Valiando J., Ohh M., Salic A., Asara J.M., Lane W.S., and Kaelin Jr. W.G. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292 (2001) 464-468
6. Jeong J.W., Bae M.K., Ahn M.Y., Kim S.H., Sohn T.K., Bae M.H., Yoo M.A., Song E.J., Lee K.J., and Kim K.W. Regulation and destabilization of HIF-1alpha by ARD1-mediated acetylation. Cell 111 (2002) 709-720
7. Jaakkola P., Mole D.R., Tian Y.M., Wilson M.I., Gielbert J., Gaskell S.J., Kriegsheim A., Hebestreit H.F., Mukherji M., Schofield C.J., Maxwell P.H., Pugh C.W., and Ratcliffe P.J. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292 (2001) 468-472
8. Zagzag D., Zhong H., Scalzitti J.M., Laughner E., Simons J.W., and Semenza G.L. Expression of hypoxia-inducible factor 1alpha in brain tumors: association with angiogenesis, invasion, and progression. Cancer 88 (2000) 2606-2618
9. Zhong H., De Marzo A.M., Laughner E., Lim M., Hilton D.A., Zagzag D., Buechler P., Isaacs W.B., Semenza G.L., and Simons J.W. Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res. 59 (1999) 5830-5855
10. Zhong H., Agani F., Baccala A.A., Laughner E., Rioseco-Camacho N., Isaacs W.B., Simons J.W., and Semenza G.L. Increased expression of hypoxia inducible factor-1alpha in rat and human prostate cancer. Cancer Res. 58 (1998) 5280-5284
11. Semenza G.L. Targeting HIF-1 for cancer therapy. Nat. Rev., Cancer 3 (2003) 721-732
12. Harris A.L. Hypoxia-A key regulatory factor in tumour growth. Nat. Rev., Cancer 2 (2002) 38-47
13. Akakura N., Kobayashi M., Horiuchi I., Suzuki A., Wang J., Chen J., Niizeki H., Kawamura K., Hosokawa M., and Asaka M. Constitutive expression of hypoxia-inducible factor-1a renders pancreatic cancer cells resistant to apoptosis induced by hypoxia and nutrient deprivation. Cancer Res. 61 (2001) 6548-6554
14. 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., and Kobayashi M. Dominant-negative hypoxia-inducible factor-1 alpha reduces tumorigenicity of pancreatic cancer cells through the suppression of glucose metabolism. Am. J. Pathol. 162 (2003) 1283-1291
15. Yu E.Z., Li Y.Y., Liu X.H., Kagan E., and McCarron R.M. Antiapoptotic action of hypoxia-inducible factor-1alpha in human endothelial cells. Lab. Invest. 84 (2004) 553-561
16. Piret J.P., Minet E., Cosse J.P., Ninane N., Debacq C., Raes M., and Michiels C. Hypoxia-inducible factor-1-dependent overexpression of myeloid cell factor-1 protects hypoxic cells against tert-butyl hydroperoxide-induced apoptosis. J. Biol. Chem. 280 (2005) 9336-9344
17. Erler J.T., Cawthorne C.J., Williams K.J., Koritzinsky M., Wouters B.G., Wilson C., Miller C., Demonacos C., Stratford I.J., and Dive C. 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. 24 (2004) 2875-2889
18. Dong Z., Venkatachalam M.A., Wang J., Patel Y., Saikumar P., Semenza G.L., Force T., and Nishiyama J. Up-regulation of apoptosis inhibitory protein IAP-2 by hypoxia. Hif-1-independent mechanisms. J. Biol. Chem. 276 (2001) 18702-18709
19. Dong Z., and Wang J. Hypoxia selection of death-resistant cells. A role for Bcl-X(L). J. Biol. Chem. 279 (2004) 9215-9221
20. Cummins E.P., and Taylor C.T. Hypoxia-responsive transcription factors. Pflugers Arch. 450 (2005) 363-371
21. Park S., Hahm E.R., Lee D.K., and Yang C.H. Inhibition of AP-1 transcription activator induces myc-dependent apoptosis in HL60 cells. J. Cell. Biochem. 91 (2004) 973-986
22. Potapova O., Basu S., Mercola D., and Holbrook N.J. Protective role for c-Jun in the cellular response to DNA damage. J. Biol. Chem. 276 (2001) 28546-28553
23. Michel G., Minet E., Mottet D., Remacle J., and Michiels C. Site-directed mutagenesis studies of the hypoxia-inducible factor-1alpha DNA-binding domain. Biochim. Biophys. Acta 1578 (2002) 73-83
24. Piret J.P., Lecocq C., Toffoli S., Ninane N., Raes M., and Michiels C. Hypoxia and CoCl2 protect HepG2 cells against serum deprivation- and t-BHP-induced apoptosis: a possible anti-apoptotic role for HIF-1. Exp. Cell Res. 295 (2004) 340-349
25. Costa A., Coradini D., Carrassi A., Erdas R., Sardella A., and Daidone M.G. Re: Levels of hypoxia-inducible factor-1alpha during breast carcinogenesis. J. Natl. Cancer Inst. 93 (2001) 1175-1177
26. Harrison L., and Blackwell K. Hypoxia and anemia: factors in decreased sensitivity to radiation therapy and chemotherapy?. Oncologist 9 Suppl. 5 (2004) 31-40
27. Mottet D., Ruys S.P., Demazy C., Raes M., and Michiels C. Role for casein kinase 2 in the regulation of HIF-1 activity. Int. J. Cancer 117 (2005) 764-774
28. Michiels C., Minet E., Michel G., Mottet D., Piret J.P., and Raes M. HIF-1 and AP-1 cooperate to increase gene expression in hypoxia: role of MAP kinases. IUBMB Life 52 (2001) 49-53
29. Yao K.S., Xanthoudakis S., Curran T., and O'Dwyer P.J. Activation of AP-1 and of a nuclear redox factor, Ref-1, in the response of HT29 colon cancer cells to hypoxia. Mol. Cell. Biol. 14 (1994) 5997-6003
30. Greijer A.E., and vanderWall E. The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis. J. Clin. Pathol. 57 (2004) 1009-1014
31. Zhang S.X., Gozal D., Sachleben Jr. L.R., Rane M., Klein J.B., and Gozal E. Hypoxia induces an autocrine-paracrine survival pathway via platelet-derived growth factor (PDGF)-B/PDGF-beta receptor/phosphatidylinositol 3-kinase/Akt signaling in RN46A neuronal cells. FASEB J. 17 (2003) 1709-1711
32. Baek J.H., Jang J.E., Kang C.M., Chung H.Y., Kim N.D., and Kim K.W. Hypoxia-induced VEGF enhances tumor survivability via suppression of serum deprivation-induced apoptosis. Oncogene 19 (2000) 4621-4631
33. Karpinich N.O., Tafani M., Rothman R.J., Russo M.A., and Farber J.L. The course of etoposide-induced apoptosis from damage to DNA and p53 activation to mitochondrial release of cytochrome c. J. Biol. Chem. 277 (2002) 16547-16552
34. Matteucci E., Modora S., Simone M., and Desiderio M.A. Hepatocyte growth factor induces apoptosis through the extrinsic pathway in hepatoma cells: favouring role of hypoxia-inducible factor-1 deficiency. Oncogene 22 (2003) 4062-4073
35. Leek R.D., Stratford I., and Harris A.L. The role of hypoxia-inducible factor-1 in three-dimensional tumor growth, apoptosis, and regulation by the insulin-signaling pathway. Cancer Res. 65 (2005) 4147-4152
36. Unruh A., Ressel A., Mohamed H.G., Johnson R.S., Nadrowitz R., Richter E., Katschinski D.M., and Wenger R.H. The hypoxia-inducible factor-1 alpha is a negative factor for tumor therapy. Oncogene 22 (2003) 3213-3220
37. Yang L., Cao Z., Li F., Post D.E., VanMeir E.G., Zhong H., and Wood W.C. Tumor-specific gene expression using the survivin promoter is further increased by hypoxia. Gene Ther. 11 (2004) 1215-1223
38. Suzuki A., Kusakai G.I., Shimojo Y., Chen J., Ogura T., Kobayashi M., and Esumi H. Involvement of TGF-beta1 signaling in hypoxia-induced tolerance to glucose starvation. J. Biol. Chem. 280 (2005) 31557-31563
39. Paris S., Denis H., Delaive E., Dieu M., Dumont V., Ninane N., Raes M., and Michiels C. Up-regulation of 94-kDa glucose-regulated protein by hypoxia-inducible factor-1 in human endothelial cells in response to hypoxia. FEBS Lett. 579 (2005) 105-114
40. Dang D.T., Chen F., Gardner L.B., Cummins J.M., Rago C., Bunz F., Kantsevoy S.V., and Dang L.H. Hypoxia-inducible factor-1alpha promotes nonhypoxia-mediated proliferation in colon cancer cells and xenografts. Cancer Res. 66 (2006) 1684-1936
41. Minet E., Michel G., Mottet D., Piret J.P., Barbieux A., Raes M., and Michiels C. c-JUN gene induction and AP-1 activity is regulated by a JNK-dependent pathway in hypoxic HepG2 cells. Exp. Cell Res. 265 (2001) 114-124
42. Laderoute K.R., Calaoagan J.M., Gustafson-Brown C., Knapp A.M., Li G.C., Mendonca H.L., Ryan H.E., Wang Z., and Johnson R.S. The response of c-jun/AP-1 to chronic hypoxia is hypoxia-inducible factor 1 alpha dependent. Mol. Cell. Biol. 22 (2002) 2515-2523
43. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 103 (2000) 239-252
44. Fan M., Goodwin M.E., Birrer M.J., and Chambers T.C. The c-Jun NH(2)-terminal protein kinase/AP-1 pathway is required for efficient apoptosis induced by vinblastine. Cancer Res. 61 (2001) 4450-4458
45. Bennett B.L., Sasaki D.T., Murray B.W., O'Leary E.C., Sakata S.T., Xu W., Leisten J.C., Motiwala A., Pierce S., Satoh Y., Bhagwat S.S., Manning A.M., and Anderson D.W. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 13681-13686
46. Kunz M., Ibrahim S., Koczan D., Thiesen H.J., Kohler H.J., Acker T., Plate K.H., Ludwig S., Rapp U.R., Brocker E.B., vanMuijen G.N., Flory E., and Gross G. Activation of c-Jun NH2-terminal kinase/stress-activated protein kinase (JNK/SAPK) is critical for hypoxia-induced apoptosis of human malignant melanoma. Cell Growth Differ. 12 (2001) 137-145
47. Zhou G., Golden T., Aragon I.V., and Honkanen R.E. Ser/Thr protein phosphatase 5 inactivates hypoxia-induced activation of an apoptosis signal-regulating kinase 1/MKK-4/JNK signaling cascade. J. Biol. Chem. 279 (2004) 46595-46605
48. Dougherty C.J., Kubasiak L.A., Prentice H., Andreka P., Bishopric N.H., and Webster K.A. Activation of c-Jun N-terminal kinase promotes survival of cardiac myocytes after oxidative stress. Biochem. J. 362 (2002) 561-571
49. Okuno S., Saito A., Hayashi T., and Chan P.H. The c-Jun N-terminal protein kinase signaling pathway mediates Bax activation and subsequent neuronal apoptosis through interaction with Bim after transient focal cerebral ischemia. J. Neurosci. 24 (2004) 7879-7887
50. Comerford K.M., Cummins E.P., and Taylor C.T. c-Jun NH2-terminal kinase activation contributes to hypoxia-inducible factor 1alpha-dependent P-glycoprotein expression in hypoxia. Cancer Res. 64 (2004) 9057-9061