Mitochondrial reactive oxygen species trigger hypoxia-inducible factor-dependent extension of the replicative life span during hypoxia

Molecular and Cellular Biology

Volumn 27, Issue 16, 2007, Pages 5737-5745

  Bell, Eric L ^a   Klimova, Tatyana A ^a   Eisenbart, James ^a   Schumacker, Paul T ^a   Chandel, Navdeep S ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; TELOMERASE REVERSE TRANSCRIPTASE; VON HIPPEL LINDAU PROTEIN;

ARTICLE; CELL DIVISION; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HYPOXIA; LIFESPAN; LUNG FIBROBLAST; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STABILITY; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

CELL AGING; CELL HYPOXIA; CELLS, CULTURED; CYTOSOL; DNA DAMAGE; FIBROBLASTS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; MITOCHONDRIA; OXYGEN; REACTIVE OXYGEN SPECIES; TELOMERASE; THERMODYNAMICS; TRANSCRIPTION, GENETIC; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 34547914798     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.02265-06     Document Type: Article

References (53)

1. Abe, J., M. Takahashi, M. Ishida, J. D. Lee, and B. C. Berk. 1997. c-Src is required for oxidative stress-mediated activation of big mitogen-activated protein kinase 1. J. Biol. Chem. 272:20389-20394.
2. Beckman, K. B., and B. N. Ames. 1998. The free radical theory of aging matures. Physiol. Rev. 78:547-581.
3. o site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J. Cell Biol, doi: 10.1083/jcb.200609074v1.
4. Bodnar, A. G., M. Ouellette, M. Frolkis, S. E. Holt, C. P. Chiu, G. B. Morin, C. B. Harley, J. W. Shay, S. Lichtsteiner, and W. E. Wright 1998. Extension of life-span by introduction of telomerase into normal human cells. Science 279:349-352.
5. Brunelle, J. K., E. L. Bell, N. M. Quesada, K. Vercauteren, V. Tiranti, M. Zeviani, R. C. Scarpulla, and N. S. Chandel. 2005. Oxygen sensing requires mitochondrial ROS but not oxidative phosphorylation. Cell Metab. 1:409-414.
6. Campisi, J. 2005. Suppressing cancer: the importance of being senescent. Science 309:886-587.
7. Chandel, N. S., E. Maltepe, E. Goldwasser, C. E. Mathieu, M. C. Simon, and P. T. Schumacker. 1998. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. USA 95:11715-11720.
8. 2 sensing. J. Biol. Chem. 275: 25130-25138.
9. Chen, Z., L. C. Trotman, D. Shaffer, H. K. Lin, Z. A. Dotan, M. Niki, J. A. Koutcher, H. I. Scher, T. Ludwig, W. Gerald, C. Cordon-Cardo, and P. P. Pandolfi. 2005. Crucial role of p53-dependent cellular senescence in suppression of PTEN-deficient tumorigenesis. Nature 436:725-730.
10. Counter, C. M., W. C. Hahn, W. Wei, S. D. Caddle, R. L. Beijersbergen, P. M. Lansdorp, J. M. Sedivy, and R. A. Weinberg. 1998. Dissociation among in vitro telomerase activity, telomere maintenance, and cellular immortalization. Proc. Natl. Acad. Sci. USA 95:14723-14728.
11. Counter, C. M., M. Meyerson, E. N. Eaton, L. W. Ellisen, S. D. Caddle, D. A. Haber, and R. A. Weinberg. 1998. Telomerase activity is restored in human cells by ectopic expression of hTERT (hEST2), the catalytic subunit of telomerase. Oncogene 16:1217-1222.
12. Cowden Dahl, K. D., B. H. Fryer, F. A. Mack, V. Compernolle, E. Maltepe, D. M. Adelman, P. Carmeliet, and M. C. Simon. 2005. Hypoxia-inducible factors 1α and 2α regulate trophoblast differentiation. Mol. Cell. Biol. 25: 10479-10491.
13. Dimri, G., X. Lee, G. Basile, M. Acosta, G. Scott, C. Roskelley, E. Medrano, M. Linskens, I. Rubelj, O. Pereira-Smith, M. Peacocke, and J. Campisi. 1995. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 92:9363-9367.
14. Dirmeier, R., K. M. O'Brien, M. Engle, A. Dodd, E. Spears, and R. O. Poyton. 2002. Exposure of yeast cells to anoxia induces transient oxidative stress. Implications for the induction of hypoxic genes. J. Biol. Chem. 277: 34773-34784.
15. Dooley, C. T., T. M. Dore, G. T. Hanson, W. C. Jackson, S. J. Remington, and R. Y. Tsien. 2004. Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J. Biol. Chem. 279:22284-22293.
16. Duranteau, J., N. S. Chandel, A. Kulisz, Z. Shao, and P. T. Schumacker. 1998. Intracellular signaling by reactive oxygen species during hypoxia in cardiomyocytes. J. Biol. Chem. 273:11619-11624.
17. Emerling, B. M., and N. S. Chandel. 2005. Oxygen sensing: getting pumped by sterols. Sci. STKE 2005:pe30.
18. Fandrey, J., S. Frede, and W. Jelkmann. 1994. Role of hydrogen peroxide in hypoxia-induced erythropoietin production. Biochem. J. 303:507-510.
19. Finkel, T. 2003. Oxidant signals and oxidative stress. Curr. Opin. Cell Biol. 15:247-254.
20. Forsyth, N. R., A. P. Evans, J. W. Shay, and W. E. Wright. 2003. Developmental differences in the immortalization of lung fibroblasts by telomerase. Aging Cell 2:235-243.
21. Forsythe, J. A., B. H. Jiang, N. V. Iyer, F. Agani, S. W. Leung, R. D. Koos, and G. L. Semenza. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16:4604-4613.
22. Georgiou, G. 2002. How to flip the (redox) switch. Cell 111:607-610.
23. Gustafsson, M. V., X. Zheng, T. Pereira, K. Gradin, S. Jin, J. Lundkvist, J. L. Ruas, L. Poellinger, U. Lendahl, and M. Bondesson. 2005. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev. Cell 9:617-628.
24. Guzy, R. D., B. Hoyos, E. Robin, H. Chen, L. Liu, K. D. Mansfield, M. C. Simon, U. Hammerling, and P. T. Schumacker. 2005. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab. 1:401-408.
25. Hayflick, L. 1965. The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37:614-636.
26. Irani, K., Y. Xia, J. L. Zweier, S. J. Sollott, C. J. Der, E. R. Fearon, M. Sundaresan, T. Finkel, and P. J. Goldschmidt-Clermont. 1997. Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 275: 1649-1652.
27. Kamata, H., S. Honda, S. Maeda, L. Chang, H. Hirata, and M. Karin. 2005. Reactive oxygen species promote TNFα-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120: 649-661.
28. Killilea, D. W., R. Hester, R. Balczon, P. Babal, and M. N. Gillespie. 2000. Free radical production in hypoxic pulmonary artery smooth muscle cells. Am. J. Physiol. Lung Cell Mol. Physiol. 279:L408-412.
29. Kondo, K., J. Klco, E. Nakamura, M. Lechpammer, J. Kaelin, and G. William. 2002. Inhibition of HIF is necessary for tumor suppression by the von Hippel-Lindau protein. Cancer Cell 1:237-246.
30. Liu, H., R. Colavitti, I. I. Rovira, and T. Finkel. 2005. Redox-dependent transcriptional regulation. Circ. Res. 97:967-974.
31. Mansfield, K. D., R. D. Guzy, Y. Pan, R. M. Young, T. P. Cash, P. T. Schumacker, and M. C. Simon. 2005. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-α activation. Cell Metab. 1:393-399.
32. Maranchie, J. K., J. R. Yasselli, J. Riss, J. S. Bonifacino, W. M. Linehan, and R. D. Klausner. 2002. The contribution of VHL substrate binding and HIF1-α to the phenotype of VHL loss in renal cell carcinoma. Cancer Cell 1:247-255.
33. Masutomi, K., E. Y. Yu, S. Khurts, I. Ben-Porath, J. L. Currier, G. B. Metz, M. W. Brooks, S. Kaneko, S. Murakami, J. A. DeCaprio, R. A. Weinberg, S. A. Stewart, and W. C. Hahn. 2003. Telomerase maintains telomere structure in normal human cells. Cell 114:241-253.
34. McEachern, M. J., A. Krauskopf, and E. H. Blackburn. 2000. Telomeres and their control. Annu. Rev. Genet. 34:331-358.
35. Meng, T. C., T. Fukada, and N. K. Tonks. 2002. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol. Cell 9:387-399.
36. Michelakis, E. D., I. Rebeyka, X. Wu, A. Nsair, B. Thebaud, K. Hashimoto, J. R. B. Dyck, A. Haromy, G. Harry, A. Barr, and S. L. Archer. 2002. O2 Sensing in the human ductus arteriosus: regulation of voltage-gated K+ channels in smooth muscle cells by a mitochondrial redox sensor. Circ. Res. 91:478-486.
37. Minamino, T., S. A. Mitsialis, and S. Kourembanas. 2001. Hypoxia extends the life span of vascular smooth muscle cells through telomerase activation. Mol. Cell. Biol. 21:3336-3342.
38. Nishi, H., T. Nakada, S. Kyo, M. Inoue, J. W. Shay, and K. Isaka. 2004. Hypoxia-inducible factor 1 mediates upregulation of telomerase (hTERT). Mol. Cell. Biol. 24:6076-6083.
39. Packer, L., and K. Fuehr. 1977. Low oxygen concentration extends the lifespan of cultured human diploid cells. Nature 267:423-425.
40. Paull, T. T., E. P. Rogakou, V. Yamazaki, C. U. Kirchgessner, M. Gellert, and W. M. Bonner. 2000. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10:886-895.
41. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
42. Safran, M., and W. G. Kaelin, Jr. 2003. HIF hydroxylation and the mammalian oxygen-sensing pathway. J. Clin. Investig. 111:779-783.
43. Saito, H., A. T. Hammond, and R. E. Moses. 1995. The effect of low oxygen tension on the in vitro-replicative life span of human diploid fibroblast cells and their transformed derivatives. Exp. Cell Res. 217:272-279.
44. Semenza, G. L. 2000. HIF-1 and human disease: one highly involved factor. Genes Dev. 14:1983-1991.
45. Semenza, G. L. 2003. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3:721-732.
46. Serrano, M., A. W. Lin, M. E. McCurrach, D. Beach, and S. W. Lowe. 1997. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88:593-602.
47. Tobiume, K., A. Matsuzawa, T. Takahashi, H. Nishitoh, K. Morita, K. Takeda, O. Minowa, K. Miyazono, T. Noda, and H. Ichijo. 2001. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep. 2:222-228.
48. Vaux, E. C., E. Metzen, K. M. Yeates, and P. J. Ratcliffe. 2001. Regulation of hypoxia-inducible factor is preserved in the absence of a functioning mitochondrial respiratory chain. Blood 98:296-302.
49. Vaziri, H., and S. Benchimol. 1998. Reconstitution of telomerase activity in normal human cells leads to elongation of telomeres and extended replicative life span. Curr. Biol. 8:279-282.
50. Wege, H., M. S. Chui, H. T. Le, J. M. Tran, and M. A. Zern. 2003. SYBR Green real-time telomeric repeat amplification protocol for the rapid quantification of telomerase activity. Nucleic Acids Res. 31:e3.
51. Welford, S. M., B. Bedogni, K. Gradin, L. Poellinger, M. Broome Powell, and A. J. Giaccia. 2006. HIF1α delays premature senescence through the activation of MIF. Genes Dev. 20:3366-3371.
52. Wood, J. G., J. S. Johnson, L. F. Mattioli, and N. C. Gonzalez. 1999. Systemic hypoxia promotes leukocyte-endothelial adherence via reactive oxidant generation. J Appl. Physiol. 87:1734-1740.
53. Yatabe, N., S. Kyo, Y. Maida, H. Nishi, M. Nakamura, T. Kanaya, M. Tanaka, K. Isaka, S. Ogawa, and M. Inoue. 2004. HIF-1-mediated activation of telomerase in cervical cancer cells. Oncogene 23:3708-3715.