Hydrogen peroxide triggers nuclear export of telomerase reverse transcriptase via Src kinase family-dependent phosphorylation of tyrosine 707

Molecular and Cellular Biology

Volumn 23, Issue 13, 2003, Pages 4598-4610

  Haendeler, Judith ^a   Hoffmann, Jörg ^a   Brandes, Ralf P ^a   Zeiher, Andreas M ^a   Dimmeler, Stefanie ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; HYDROGEN PEROXIDE; LEPTOMYCIN B; PROTEIN KINASE; RAN PROTEIN; RNA DIRECTED DNA POLYMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TYROSINE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL NUCLEUS; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOSOL; ENZYME LOCALIZATION; ENZYME REGULATION; GENE MUTATION; GENE OVEREXPRESSION; GENE TRANSLOCATION; HUMAN; HUMAN CELL; NUCLEAR PORE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION;

ACTIVE TRANSPORT, CELL NUCLEUS; APOPTOSIS; CELL LINE; CELL NUCLEUS; CELL SEPARATION; CLONING, MOLECULAR; CYTOSOL; DNA-BINDING PROTEINS; FLOW CYTOMETRY; HUMANS; HYDROGEN PEROXIDE; IMMUNOBLOTTING; MICROSCOPY, FLUORESCENCE; OXIDATIVE STRESS; PHOSPHORYLATION; PLANT PROTEINS; PLASMIDS; PRECIPITIN TESTS; PROTEIN TRANSPORT; RAN GTP-BINDING PROTEIN; SRC-FAMILY KINASES; TELOMERASE; TIME FACTORS; TYROSINE;

EID: 0038721199     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.13.4598-4610.2003     Document Type: Article

References (66)

1. Adachi, M., M. Fukuda, and E. Nishida. 1999. Two co-existing mechanisms for nuclear import of MAP kinase: passive diffusion of a monomer and active transport of a dimer. EMBO J. 18:5347-5358.
2. Blackburn, E. H. 2000. Telomere states and cell fates. Nature 408:53-56.
3. Blasco, M. A. 2002. Telomerase beyond telomeres. Nat. Rev. Cancer 2:627-633.
4. Bodnar, A. G., M. Ouellette, M. Frolkis, S. E. Holt, C. P. Chin, 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. Breitschopf, K., A. M. Zeiher, and S. Dimmeler. 2001. Proatherosclerotic factors induce telomerase inactivation in endothelial cells through an Aktdependent mechanism. FEBS lett. 493:21-25.
6. Chandra, J. A. Samali, and S. Orrenius. 2000. Triggering and modulation of apoplosis by oxidative stress. Free Radic. Biol. Med. 29:323-333.
7. Chin, L., S. E. Artandi, Q. Shen, A. Tam, S. L. Lee, G. J. Gottlieb, C. W. Greider, and R. A. DePinho. 1999. p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell 97:527-538.
8. Colgin, L. M., and R. R. Reddel. 1999. Telomere maintenance mechanisms and cellular immortalization. Curr. Opin. Genet. Dev. 9:97-103.
9. 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 senescence. Proc. Natl. Acad. Sci. USA 95:14723-14728.
10. de Lange, T. 1998. Telomeres. Nature 392:753-754.
11. Ferrigno, P., F. Posas, D. Koepp, H. Saito, and P. A. Silver. 1998. Regulated nucleo/cytoplasmic exchange of HOG1 MAPK requires the importin beta homologs NMD5 and XPO1. EMBO J. 17:5606-5614.
12. Finkel, T., and N. J. Holbrook. 2000. Oxidants, oxidative stress and the biology of aging. Nature 408:239-247.
13. Fiscber-Fantuzzi, L., and C. Vesco. 1988. Cell-dependent efficiency of reiterated nuclear signals in a mutant simian virus 40 oncoprotein targeted to the nucleus. Mol. Cell. Biol. 8:5495-5503.
14. France-Lanord, V., B. Brugg, P. P. Michel, Y. Agid, and M. Ruberg. 1997. Mitochondrial free radical signal in ceramide-dependent apoptosis: a putative mechanism for neuronal death in Parkinson's disease. J. Neurochem. 69:1612-1621.
15. Fu, W., J. G. Begley, M. W. Killen, and M. P. Mattson. 1999. Anti-apoptotic role of telomerase in pheochromocytoma cells. J. Biol. Chem. 274:7264-7271.
16. Furumoto, K., E. Inoue, N. Nagao, E. Hiyama, and N. Miwa. 1998. Age-dependent telomere shortening is slowed down by enrichment of intracellular vitamin C via suppression of oxidative stress. Life Sci. 63:935-948.
17. González-Suárez, E., J. M. Flores, and M. A. Blasco. 2002. Cooperation between p53 mutation and high telomerase transgenic expression in spontaneous cancer development. Mol. Cell. Biol. 22:7291-7301.
18. Gonzalez-Suarez, E., E. Samper, A. Ramirez, J. M. Flores, J. Martin-Caballero, J. L. Jorcano, and M. A. Blasco. 2001. Increased epidermal tumors and increased skin wound healing in transgenic mice overexpresslng the catalytic subunit of telomerase, mTERT, in basal keratinocytes. EMBO J. 20:2619-2630.
19. Gorbunova, V., A. Seluanov, and O. Pereira-Smith. 2002. Expression of hTERT does not prevent stress-induced senescence in normal human fibroblasts, but protects the cells from stress-induced apoptosis and necrosis. J. Biol. Chem. 277:38540-38549.
20. Greider, C. W., and E. H. Blackbum. 1985. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43:405-413.
21. Greider, C. W., and E. H. Blackburn. 1989. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337:331-337.
22. Griendling, K. K., and D. G. Harrison. 1999. Dual role of reactive oxygen species in vascular growth. Circ. Res. 85:562-563.
23. Griendling, K. K., D. Sorescu, B. Lassegue, and M. Ushio-Fukai. 2000. Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology. Arterioscler. Thromb. Vasc. Biol. 20:2175-2183.
24. Haendeler, J., M. Ishida, L. Hunyady, and B. C. Berk. 2000. The third cytoplasmic loop of the angiotensin II type 1 receptor exerts differential effects on extracellular signal-regulated kinase (ERK1/ERK2) and apoptosis via Ras- and Rap1-dependent pathways. Circ. Res. 86:729-736.
25. Hanke, J. H., J. P. Gardner, R. L. Dow, P. S. Changelian, W. H. Brisseite, E. J. Weringer, B. A. Pollok, and P. A. Connelly. 1996. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271:695-701.
26. Heller, R. A., and M. Kronke. 1994. Tumor necrosis factor receptor-mediated signaling pathways. J. Cell Biol. 126:5-9.
27. Hemann, M. T., K. L. Rudolph, M. A. Strong, R. A. DePinho, L. Chin, and C. W. Greider. 2001. Telomere dysfunction triggers developmentally regulated germ cell apoptosis. Mol. Biol. Cell 12:2023-2030.
28. Hemann, M. T., M. A. Strong, L. Y. Hao, and C. W. Greider. 2001. The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107:67-77.
29. Holt, S. E., D. L. Aisner, J. Baur, V. M. Tesmer, M. Dy, M. Ouellette, J. B. Trager, G. B. Morin, D. O. Toft, J. W. Shay, W. E. Wright, and M. A. White. 1999. Functional requirement of p23 and Hsp90 in telomerase complex. Genes Dev. 13:817-826.
30. Kang, S. S., T. Kwon, D. Y. Kwon, and S. I. Do. 1999. Akt protein kinase enhances human telomerase activity through phosphorylation of telomerase reverse transcriptase subunit. J. Biol. Chem. 274:13085-13090.
31. Kharbanda, S., V. Kumar, S. Dhar, P. Pandey, C. Chen, P. Majumder, Z. M. Yuan, Y. Whang, W. Strauss, T. K. Pandita, D. Weaver, and D. Kufe. 2000. Regulation of the hTERT telomerase catalytic subunit by the c-Abl tyrosine kinase. Curr. Biol. 10:568-575.
32. Kudo, N., N. Matsumori, H. Taoka, D. Fujiwara, E. P. Schreiner, B. Wolff, M. Yoshida, and S. Horinouchi. 1999. Leptomycin B inactivates CRM/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc. Natl. Acad. Sci. USA 96:9112-9117.
33. Lee, S.-H., and M. Hannink. 2001. The N-terminal nuclear export sequence of IkBalpha is required for RanGTP-dependent binding to CRM-1. J. Biol. Chem. 276:23599-23606.
34. Li, H., L Zhao, Z. Yang, J. W. Funder, and J. P. Liu. 1998. Telomerase is controlled by protein kinase Calpha in human breast cancer cells. J. Biol. Chem. 273:33436-33442.
35. Lindsay, M, E., J. M. Holaska, K. Welch, B. M. Paschal, and I. G. Macara. 2001. Ran-binding protein 3 is a cofactor for CRM1-mediated nuclear protein export. J. Cell. Biol. 153:1391-1402.
36. Liu, J. P. 1999. Studies of the molecular mechanisms in the regulation of telomerase activity. FASEB J. 13:2091-2104.
37. Liu, K., R. J. Hodes, and N.-P. Weng. 2001. Telomerase activation in human T lymphocytes does not require increase in telomerase reverse transcriptase (hTERT) protein but is associated with hTERT phosphorylation and nuclear translocation. J. Immunol. 166:4826-4830.
38. Macara, I. G. 2001. Transport into and out of the nucleus. Microbiol. Mol. Biol. Rev. 65:570-594.
39. Mattson, M. P., and W. Klapper. 2001. Emerging roles for telomerase in neuronal development and apoptosis. J. Neurosci. Res. 63:1-9.
40. McBride, K. M., G. Banninger, C. McDonald, and N. C. Reich. 2002. Regulated nuclear import of STAT1 transcription factor by direct binding of importin-alpha. EMBO J. 21:1754-1763.
41. Meyerson, M., C. M. Counter, E. N. Eaton, L. W. Ellisen, P. Steiner, S. D. Caddle, L. Ziaugra, R. L. Beijersbergen, M. J. Davidoff, Q. Liu, S. Bacchetti, D. A. Haber, and R. A. Weinberg. 1997. hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell 90:785-795.
42. Minamino, T., and S. Kourembanas, 2001. Mechanisms of telomerase induction during vascular smooth muscle cell proliferation. Circ. Res. 89:237-243.
43. Nakamura, T. M., and T. R. Cech. 1998. Reversing time: origin of telomerase. Cell 92:587-590.
44. Nakielny, S., and G. Dreyfuss. 1999. Transport of proteins and RNAs in and out the nucleus. Cell 99:677-690.
45. Nordberg, J., and E. S. Arner. 2001. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic. Biol. Med. 31:1287-1312.
46. Oh, H., G. E. Taffet, K. A. Youker, M. L. Entman, P. A. Overbeek, L. H. Michael, and M. D. Schneider. 2001. Telomerase reverse transcriptase promotes cardiac muscle cell proliferation, hypertrophy, and survival. Proc. Natl. Acad. Sci. USA 98:10308-10313.
47. Paine, P. L., L. C. Moore, and S. B. Horowitz. 1975. Nuclear envelope permeability. Nature 254:109-114.
48. Parman, T., M. J. Wiley, and P. G. Wells. 1999. Free radical-mediated oxidative DNA damage in the mechanism of thalidomide teratogenicity. Nat. Med. 5:582-585.
49. Persic, L., M. Righi, A. Roberts, H. R. Hoogenboom, A. Cattaneo, and A. Bradhury. 1997. Targeting vectors for intracellular immunisation. Gene 187:1-8.
50. Rongish, B. J., and W. H. Kinsey. 2000. Transient nuclear localization of Fyn kinase during development in zebrafish. Anat. Rec. 260:115-123.
51. Rudolph, K. L., S. Chang, M. Millard, N. Schreiber-Agus, and R. A. De-Pinho. 2000. Inhibition of experimental liver cirrhosis in mice by telomerase gene delivery. Science 287:1253-1258.
52. Ryan, K. J., and S. R. Wente. 2000. The nuclear pore complex: a protein machine bridging the nucleus and cytoplasm. Curr. Opin. Cell Biol. 12:361-371.
53. Sachdev, S., S. Bagchi, D. D. Zhang, A. C. Mings, and M. Hannink. 2000. Nuclear import of IkBα, is accomplished by a Ran-independent transport pathway. Mol. Cell. Biol. 20:1571-1582.
54. Seimiya, H., H. Sawada, Y. Muramatsu, M. Shimizu, K. Ohko, K. Yamane, and T. Tsuruo. 2000. Involvement of 14-3-3 proteins in nuclear localization of telomerase. EMBO J. 19:2652-2661.
55. Seimiya, H., M. Tanji, T. Oh-Hara, A. Tomida, I. Naasani, and T. Tsuruo. 1999. Hypoxia up-regulates telomerase activity via mitogen-activated protein kinase signaling in human solid tumor cells. Biochem. Biophys. Res. Commun. 260:365-370.
56. Sloan-Lancaster, J., W. Zhang, J. Presley, B. L. Williams, R. T. Abraham, J. Lippincott-Schwartz, and L. E. Samelson. 1997. Regulation of ZAP-70 intracellular localization: visualization with the green fluorescent protein. J. Exp. Med. 186:1713-1724.
57. Suzuki, Y. J., H. J. Forman, and A. Sevanian. 1997. Oxidants as stimulators of signal transduction. Free Radic. Biol. Med. 22:269-285.
58. Uetz, P., S. Fumagalli, D. James, and R. Zeller. 1996. Molecular interaction between limb deformity proteins (formins) and Src family kinases. J. Biol. Chem. 271:33525-33530.
59. Vasa, M., K. Breitschopf, A. M. Zeiher, and S. Dimmeler. 2000. Nitric oxide activates telomerase and delays endothelial cell senescence. Circ. Res. 87:540-542.
60. White, C. R., T. A. Brock, L. Y. Chang, J. Crapo, P. Briscoe, D. Ku, W. A. Bradley, S. H. Gianturco, J. Gore, B. A. Freeman et al. 1994. Superoxide and peroxynitrite in atherosclerosis. Proc. Natl. Acad. Sci. USA 91:1044-1048.
61. Wong, J. M., L. Kusdra, and K. Collins. 2002. Subnuclear shuttling of human telomerase induced by transformation and DNA damage. Nat. Cell Biol. 4:731-736.
62. Wong, K. K., S. Chang, S. R. Weiler, S. Ganesan, J. Chaudhuri, C. Zhu, S. E. Artandi, K. L. Rudolph, G. J. Gottlieh, L. Chin, F. W. Alt, and R. A. DePinho. 2000. Telomere dysfunction impairs DNA repair and enhances sensitivity to ionizing radiation. Nat. Genet. 26:85-88
63. Woo, C. H., Y. W. Eom, M. H. Yoo, H. J. You, H. J. Han, W. K. Song, Y. J. You, J. S. Chun, and J. H. Kim. 2000. Tumor necrosis factor-alpha generates reactive oxygen species via a cytosolic phospholipase A2-linked cascade. J. Biol. Chem. 275:32357-32362.
64. Yang, J., E. Chang, A. M. Cherry, C. D. Bangs, Y. Oei, A. Bodnar, A. Bronstein, C. P. Chiu, and G. S. Herron. 1999. Human endothelial cell life extension by telomerase expression. J. Biol. Chem. 274:26141-26148.
65. Zeng, R., Y. Aoki, M. Yoshida, K. Arai, and S. Watanabe. 2002. Stat5B shuttles between cytoplasm and nucleus in a cytokine-dependent and -independent manner. J. Immunol. 168:4567-4575.
66. Zhu, H., W. Fu, and M. P. Mattson. 2000. The catalytic subunit of telomerase protects neurons against amyloid beta-peptide-induced apoptosis. J. Neurochem. 75:117-124.