Vaccinia-related kinase 2 modulates the stress response to hypoxia mediated by TAK1

Molecular and Cellular Biology

Volumn 27, Issue 20, 2007, Pages 7273-7283

  Blanco, Sandra ^a   Santos, Claudio ^a   Lazo, Pedro A ^a,b  

^a Salamanca Spain   (Spain)

^b CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PHOSPHOTRANSFERASE; PROTEIN JIP1; SCAFFOLD PROTEIN; SHORT HAIRPIN RNA; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UNCLASSIFIED DRUG; VACCINIA RELATED KINASE 2;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN COS1; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HELA CELL; HUMAN; HUMAN CELL; HYPOXIA; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STRESS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL HYPOXIA; CERCOPITHECUS AETHIOPS; COS CELLS; ENZYME ACTIVATION; HELA CELLS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE KINASES; MICE; MULTIPROTEIN COMPLEXES; OXIDATIVE STRESS; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION;

EID: 35148817342     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00025-07     Document Type: Article

References (60)

1. Alfranca, A., M. D. Gutierrez, A. Vara, J. Aragones, F. Vidal, and M. O. Landazuri. 2002. c-Jun and hypoxia-inducible factor 1 functionally cooperate in hypoxia-induced gene transcription. Mol. Cell. Biol. 22:12-22.
2. Bandyopadhyay, R. S., M. Phelan, and D. V. Faller. 1995. Hypoxia induces AP-1-regulated genes and AP-1 transcription factor binding in human endothelial and other cell types. Biochim. Biophys. Acta 1264:72-78.
3. Barcia, R., S. Lopez-Borges, F. M. Vega, and P. A. Lazo. 2002. Kinetic properties of p53 phosphorylation by the human vaccinia-related kinase 1. Arch. Biochem. Biophys. 399:1-5.
4. Berra, E., G. Pages, and J. Pouyssegur. 2000. MAP kinases and hypoxia in the control of VEGF expression. Cancer Metastasis Rev. 19:139-145.
5. Bishopric, N. H., P. Andreka, T. Slepak, and K. A. Webster. 2001. Molecular mechanisms of apoptosis in the cardiac myocyte. Curr. Opin. Pharmacol. 1:141-150.
6. Blanco, S., L. Klimcakova, F. M. Vega, and P. A. Lazo. 2006. The subcellular localization of vaccinia-related kinase-2 (VRK2) isoforms determines their different effect on p53 stability in tumour cell lines. FEBS J. 273:2487-2504.
7. Chihab, R., C. Ferry, V. Koziel, P. Monin, and J. L. Daval. 1998. Sequential activation of activator protein-1-related transcription factors and JNK protein kinases may contribute to apoptotic death induced by transient hypoxia in developing brain neurons. Brain Res. Mol. Brain Res. 63:105-120.
8. Comerford, K. M., E. P. Cummins, and C. T. Taylor. 2004. c-Jun NH2-terminal kinase activation contributes to hypoxia-inducible factor 1 alpha-dependent P-glycoprotein expression in hypoxia. Cancer Res. 64:9057-9061.
9. Davis, R. J. 2000. Signal transduction by the JNK group of MAP kinases. Cell 103:239-252.
10. Dhanasekaran, D. N., K. Kashef, C. M. Lee, H. Xu, and E. P. Reddy. 2007. Scaffold proteins of MAP-kinase modules. Oncogene 26:3185-3202.
11. Dong, Z., L. Zhou, K. Del Villar, M. Ghanevati, V. Tashjian, and C. A. Miller. 2005. JIP1 regulates neuronal apoptosis in response to stress. Brain Res. Mol. Brain Res. 134:282-293.
12. Dougherty, C. J., L. A. Kubasiak, D. P. Frazier, H. Li, W. C. Xiong, N. H. Bishopric, and K. A. Webster. 2004. Mitochondrial signals initiate the activation of c-Jun N-terminal kinase (JNK) by hypoxia-reoxygenation. FASEB J. 18:1060-1070.
13. Dougherty, C. J., L. A. Kubasiak, H. Prentice, P. Andreka, N. H. Bishopric, and K. A. Webster. 2002. Activation of c-Jun N-terminal kinase promotes survival of cardiac myocytes after oxidative stress. Biochem. J. 362:561-571.
14. Gorjanacz, M., E. P. Klerkx, V. Galy, R. Santarella, C. Lopez-Iglesias, P. Askjaer, and I. W. Mattaj. 2007. Caenorhabditis elegans BAF-1 and its kinase VRK-1 participate directly in post-mitotic nuclear envelope assembly. EMBO J. 26:132-143.
15. Harris, A. L. 2002. Hypoxia: a key regulatory factor in tumour growth. Nat. Rev. Cancer 2:38-47.
16. Hoffmann, A., O. Preobrazhenska, C. Wodarczyk, Y. Medler, A. Winkel, S. Shahab, D. Huylebroeck, G. Gross, and K. Verschueren. 2005. Transforming growth factor-beta-activated kinase-1 (TAK1), a MAP3K, interacts with Smad proteins and interferes with osteogenesis in murine mesenchymal progenitors. J. Biol. Chem. 280:27271-27283.
17. Holtmann, H., J. Enninga, S. Kalble, A. Thiefes, A. Dorrie, M. Broemer, R. Winzen, A. Wilhelm, J. Ninomiya-Tsuji, K. Matsumoto, K. Resch, and M. Kracht. 2001. The MAPK kinase kinase TAK1 plays a central role in coupling the interleukin-1 receptor to both transcriptional and RNA-targeted mechanisms of gene regulation. J. Biol. Chem. 276:3508-3516.
18. Javelaud, D., and A. Mauviel. 2005. Crosstalk mechanisms between the mitogen-activated protein kinase pathways and Smad signaling downstream of TGF-beta: implications for carcinogenesis. Oncogene 24:5742-5750.
19. Jiang, Z., J. Ninomiya-Tsuji, Y. Qian, K. Matsumoto, and X. Li. 2002. Interleukin-1 (IL-1) receptor-associated kinase-dependent IL-1-induced signaling complexes phosphorylate TAK1 and TAB2 at the plasma membrane and activate TAK1 in the cytosol. Mol. Cell. Biol. 22:7158-7167.
20. Kang, T. H., and K. T. Kim. 2006. Negative regulation of ERK activity by VRK3-mediated activation of VHR phosphatase. Nat. Cell Biol. 8:863-869.
21. Karin, M., and E. Gallagher. 2005. From JNK to pay dirt: jun kinases, their biochemistry, physiology and clinical importance. IUBMB Life 57:283-295.
22. Kishimoto, K., K. Matsumoto, and J. Ninomiya-Tsuji. 2000. TAK1 mitogen-activated protein kinase kinase kinase is activated by autophosphorylation within its activation loop. J. Biol. Chem. 275:7359-7364.
23. Kolch, W. 2005. Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell. Biol. 6:827-837.
24. Laderoute, K. R., H. L. Mendonca, J. M. Calaoagan, A. M. Knapp, A. J. Giaccia, and P. J. Stork. 1999. Mitogen-activated protein kinase phosphatase-1 (MKP-1) expression is induced by low oxygen conditions found in solid tumor microenvironments. A candidate MKP for the inactivation of hypoxia-inducible stress-activated protein kinase/c-Jun N-terminal protein kinase activity. J. Biol. Chem. 274:12890-12897.
25. Li, L. Y., M. Y. Liu, H. M. Shih, C. H. Tsai, and J. Y. Chen. 2006. Human cellular protein VRK2 interacts specifically with Epstein-Barr virus BHRF1, a homologue of Bcl-2, and enhances cell survival. J. Gen. Virol. 87:2869-2878.
26. Lin, A. 2003. Activation of the JNK signaling pathway: breaking the brake on apoptosis. Bioessays 25:17-24.
27. Liu, X., F. Xu, Y. Fu, F. Liu, S. Sun, and X. Wu. 2006. Calreticulin induces delayed cardioprotection through mitogen-activated protein kinases. Proteomics 6:3792-3800.
28. Lopez-Borges, S., and P. A. Lazo. 2000. The human vaccinia-related kinase 1 (VRK1) phosphorylates threonine-18 within the mdm-2 binding site of the p53 tumour suppressor protein. Oncogene 19:3656-3664.
29. Manning, G., D. B. Whyte, R. Martinez, T. Hunter, and S. Sudarsanam. 2002. The protein kinase complement of the human genome. Science 298: 1912-1934.
30. McKay, M. M., and D. K. Morrison. 2007. Integrating signals from RTKs to ERK/MAPK. Oncogene 26:3113-3121.
31. Mooney, L. M., and A. J. Whitmarsh. 2004. Docking interactions in the c-Jun N-terminal kinase pathway. J. Biol. Chem. 279:11843-11852.
32. Morrison, D. K., and R. J. Davis. 2003. Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu. Rev. Cell Dev. Biol. 19:91-118.
33. Muller, J. M., B. Krauss, C. Kaltschmidt, P. A. Baeuerle, and R. A. Rupee. 1997. Hypoxia induces c-fos transcription via a mitogen-activated protein kinase-dependent pathway. J. Biol. Chem. 272:23435-23439.
34. Nezu, J., A. Oku, M. H. Jones, and M. Shimane. 1997. Identification of two novel human putative serine/threonine kinases, VRK1 and VRK2, with structural similarity to vaccinia virus B1R kinase. Genomics 45:327-331.
35. Nichols, R. J., and P. Traktman. 2004. Characterization of three paralogous members of the mammalian vaccinia related kinase family. J. Biol. Chem. 279:7934-7946.
36. Nichols, R. J., M. S. Wiebe, and P. Traktman. 2006. The vaccinia-related kinases phosphorylate the N′ terminus of BAF, regulating its interaction with DNA and its retention in the nucleus. Mol. Biol. Cell 17:2451-2464.
37. Norris, M. L., and D. E. Millhorn. 1995. Hypoxia-induced protein binding to O2-responsive sequences on the tyrosine hydroxylase gene. J. Biol. Chem. 270:23774-23779.
38. Pouyssegur, J., F. Dayan, and N. M. Mazure. 2006. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441:437-443.
39. Prabhakar, N. R., B. C. Shenoy, M. S. Simonson, and N. S. Cherniack. 1995. Cell selective induction and transcriptional activation of immediate early genes by hypoxia. Brain Res. 697:266-270.
40. Scheinfeld, M. H., R. Roncarati, P. Vito, P. A. Lopez, M. Abdallah, and L. D'Adamio. 2002. Jun NH2-terminal kinase (JNK) interacting protein 1 (JIP1) binds the cytoplasmic domain of the Alzheimer's beta-amyloid precursor protein (APP). J. Biol. Chem. 277:3767-3775.
41. Semenza, G. L. 2001. HIF-1 and mechanisms of hypoxia sensing. Curr. Opin. Cell Biol. 13:167-171.
42. Seta, K. A., Z. Spicer, Y. Yuan, G. Lu, and D. E. Millhorn. 2002. Responding to hypoxia: lessons from a model cell line. Sci. STKE 2002:RE11.
43. Sevilla, A., C. R. Santos, R. Barcia, F. M. Vega, and P. A. Lazo. 2004. c-Jun phosphorylation by the human vaccinia-related kinase 1 (VRK1) and its cooperation with the N-terminal kinase of c-Jun (JNK). Oncogene 23:8950-8958.
44. Sevilla, A., C. R. Santos, F. M. Vega, and P. A. Lazo. 2004. Human vaccinia-related kinase 1 (VRK1) activates the ATF2 transcriptional activity by novel phosphorylation on Thr-73 and Ser-62 and cooperates with JNK. J. Biol. Chem. 279:27458-27465.
45. Shim, J. H., C. Xiao, A. E. Paschal, S. T. Bailey, P. Rao, M. S. Hayden, K. Y. Lee, C. Bussey, M. Steckel, N. Tanaka, G. Yamada, S. Akira, K. Matsumoto, and S. Ghosh. 2005. TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev. 19:2668-2681.
46. Singhirunnusorn, P., S. Suzuki, N. Kawasaki, I. Saiki, and H. Sakurai. 2005. Critical roles of threonine 187 phosphorylation in cellular stress-induced rapid and transient activation of transforming growth factor-beta-activated kinase 1 (TAK1) in a signaling complex containing TAK1-binding protein TAB1 and TAB2. J. Biol. Chem. 280:7359-7368.
47. Song, J. J., and Y. J. Lee. 2005. Dissociation of Akt1 from its negative regulator JIP1 is mediated through the ASK1-MEK-JNK signal transduction pathway during metabolic oxidative stress: a negative feedback loop. J. Cell Biol. 170:61-72.
48. Sun, H. Y., N. P. Wang, M. Halkos, F. Kerendi, H. Kin, R. A. Guyton, J. Vinten-Johansen, and Z. Q. Zhao. 2006. Postconditioning attenuates cardiomyocyte apoptosis via inhibition of JNK and p38 mitogen-activated protein kinase signaling pathways. Apoptosis 11:1583-1593.
49. Tournier, C., A. J. Whitmarsh, J. Cavanagh, T. Barret, and R. J. Davis. 1997. Mitogen-activated protein kinase 7 is an activator of the jun NH2-terminal kinase. Proc. Natl. Acad. Sci. USA 94:7337-7342.
50. Valbuena, A., F. M. Vega, S. Blanco, and P. A. Lazo. 2006. p53 downregulates its activating vaccinia-related kinase 1, forming a new autoregulatory loop. Mol. Cell. Biol. 26:4782-4793.
51. Vega, F. M., A. Sevilla, and P. A. Lazo. 2004. p53 stabilization and accumulation induced by human vaccinia-related kinase 1. Mol. Cell. Biol. 24:10366-10380.
52. Webster, K. A., D. J. Discher, and N. H. Bishopric. 1993. Induction and nuclear accumulation of fos and jun proto-oncogenes in hypoxic cardiac myocytes. J. Biol. Chem. 268:16852-16858.
53. Weston, C. R., and R. J. Davis. 2002. The JNK signal transduction pathway. Curr. Opin. Genet. Dev. 12:14-21.
54. Whitmarsh, A. J., J. Cavanagh, C. Tournier, J. Yasuda, and R. J. Davis. 1998. A mammalian scaffold complex that selectively mediates MAP kinase activation. Science 281:1671-1674.
55. Whitmarsh, A. J., C. Y. Kuan, N. J. Kennedy, N. Kelkar, T. F. Haydar, J. P. Mordes, M. Appel, A. A. Rossini, S. N. Jones, R. A. Flavell, P. Rakic, and R. J. Davis. 2001. Requirement of the JIP1 scaffold protein for stress-induced JNK activation. Genes Dev. 15:2421-2432.
56. Willoughby, E. A., G. R. Perkins, M. K. Collins, and A. J. Whitmarsh. 2003. The JNK-interacting protein-1 scaffold protein targets MAPK phosphatase-7 to dephosphorylate JNK. J. Biol. Chem. 278:10731-10736.
57. Woo, K. J., T. J. Lee, J. W. Park, and T. K. Kwon. 2006. Desferrioxamine, an iron chelator, enhances HIF-1alpha accumulation via cyclooxygenase-2 signaling pathway. Biochem. Biophys. Res. Commun. 343:8-14.
58. Yasuda, J., A. J. Whitmarsh, J. Cavanagh, M. Sharma, and R. J. Davis. 1999. The JIP group of mitogen-activated protein kinase scaffold proteins. Mol. Cell. Biol. 19:7245-7254.
59. Yoshino, Y., M. Aoyagi, M. Tamaki, L. Duan, T. Morimoto, and K. Ohno. 2006. Activation of p38 MAPK and/or JNK contributes to increased levels of VEGF secretion in human malignant glioma cells. Int. J. Oncol. 29:981-987.
60. Zhou, L., K. Del Villar, Z. Dong, and C. A. Miller. 2004. Neurogenesis response to hypoxia-induced cell death: map kinase signal transduction mechanisms. Brain Res. 1021:8-19.