The Kelch Repeat Protein KLHDC10 Regulates Oxidative Stress-Induced ASK1 Activation by Suppressing PP5

Molecular Cell

Volumn 48, Issue 5, 2012, Pages 692-704

  Sekine, Yusuke ^a   Hatanaka, Ryo ^a   Watanabe, Takeshi ^a   Sono, Naoki ^a   Iemura, Shun ichiro ^b,d   Natsume, Tohru ^b   Kuranaga, Erina ^a,c   Miura, Masayuki ^a   Takeda, Kohsuke ^a,e   Ichijo, Hidenori ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^c RIKEN Center for Biosystems Dynamics Research   (Japan)

^d FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

^e NAGASAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS SIGNAL REGULATING KINASE 1; KELCH REPEAT PROTEIN SLIM; MELANIN; PROTEIN; PROTEIN PHOSPHATASE 5; TRANSCRIPTION FACTOR GAL4; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; MALE; NONHUMAN; OXIDATIVE STRESS; POINT MUTATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEOMICS; SIGNAL TRANSDUCTION;

ANIMALS; CARRIER PROTEINS; CELL DEATH; CELL LINE, TUMOR; CLONING, MOLECULAR; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; HYDROGEN PEROXIDE; MAP KINASE KINASE KINASE 5; MAP KINASE KINASE KINASES; MELANINS; MICE; MUTAGENESIS, SITE-DIRECTED; NUCLEAR PROTEINS; OXIDANTS; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOPROTEIN PHOSPHATASES; POINT MUTATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTEOMICS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; UBIQUITIN-PROTEIN LIGASES;

MAMMALIA;

EID: 84870878552     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.09.018     Document Type: Article

References (44)

1. Adachi-Yamada T., Nakamura M., Irie K., Tomoyasu Y., Sano Y., Mori E., Goto S., Ueno N., Nishida Y., Matsumoto K. p38 mitogen-activated protein kinase can be involved in transforming growth factor beta superfamily signal transduction in Drosophila wing morphogenesis. Mol. Cell. Biol. 1999, 19:2322-2329.
2. Adams J., Kelso R., Cooley L. The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell Biol. 2000, 10:17-24.
3. Bennett E.J., Rush J., Gygi S.P., Harper J.W. Dynamics of cullin-RING ubiquitin ligase network revealed by systematic quantitative proteomics. Cell 2010, 143:951-965.
4. Borthwick E.B., Zeke T., Prescott A.R., Cohen P.T. Nuclear localization of protein phosphatase 5 is dependent on the carboxy-terminal region. FEBS Lett. 2001, 491:279-284.
5. Bosu D.R., Kipreos E.T. Cullin-RING ubiquitin ligases: global regulation and activation cycles. Cell Div. 2008, 3:7.
6. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
7. Calleja M., Herranz H., Estella C., Casal J., Lawrence P., Simpson P., Morata G. Generation of medial and lateral dorsal body domains by the pannier gene of Drosophila. Development 2000, 127:3971-3980.
8. Chen M.X., Cohen P.T. Activation of protein phosphatase 5 by limited proteolysis or the binding of polyunsaturated fatty acids to the TPR domain. FEBS Lett. 1997, 400:136-140.
9. Finkel T., Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 2000, 408:239-247.
10. Frew I.J., Krek W. pVHL: a multipurpose adaptor protein. Sci. Signal. 2008, 1:pe30. 10.1126/scisignal.124pe30.
11. Fujino G., Noguchi T., Matsuzawa A., Yamauchi S., Saitoh M., Takeda K., Ichijo H. Thioredoxin and TRAF family proteins regulate reactive oxygen species-dependent activation of ASK1 through reciprocal modulation of the N-terminal homophilic interaction of ASK1. Mol. Cell. Biol. 2007, 27:8152-8163.
12. Golden T., Swingle M., Honkanen R.E. The role of serine/threonine protein phosphatase type 5 (PP5) in the regulation of stress-induced signaling networks and cancer. Cancer Metastasis Rev. 2008, 27:169-178.
13. Hinds T.D., Sánchez E.R. Protein phosphatase 5. Int. J. Biochem. Cell Biol. 2008, 40:2358-2362.
14. Ichijo H., Nishida E., Irie K., ten Dijke P., Saitoh M., Moriguchi T., Takagi M., Matsumoto K., Miyazono K., Gotoh Y. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 1997, 275:90-94.
15. Iriyama T., Takeda K., Nakamura H., Morimoto Y., Kuroiwa T., Mizukami J., Umeda T., Noguchi T., Naguro I., Nishitoh H., et al. ASK1 and ASK2 differentially regulate the counteracting roles of apoptosis and inflammation in tumorigenesis. EMBO J. 2009, 28:843-853.
16. Izumiya Y., Kim S., Izumi Y., Yoshida K., Yoshiyama M., Matsuzawa A., Ichijo H., Iwao H. Apoptosis signal-regulating kinase 1 plays a pivotal role in angiotensin II-induced cardiac hypertrophy and remodeling. Circ. Res. 2003, 93:874-883.
17. Jubelin G., Taieb F., Duda D.M., Hsu Y., Samba-Louaka A., Nobe R., Penary M., Watrin C., Nougayrède J.P., Schulman B.A., et al. Pathogenic bacteria target NEDD8-conjugated cullins to hijack host-cell signaling pathways. PLoS Pathog. 2010, 6:e1001128. 10.1371/journal.ppat.1001128.
18. Kaelin W.G. The von Hippel-Lindau tumour suppressor protein: O2 sensing and cancer. Nat. Rev. Cancer 2008, 8:865-873.
19. Kamura T., Brower C.S., Conaway R.C., Conaway J.W. A molecular basis for stabilization of the von Hippel-Lindau (VHL) tumor suppressor protein by components of the VHL ubiquitin ligase. J. Biol. Chem. 2002, 277:30388-30393.
20. Kang H., Sayner S.L., Gross K.L., Russell L.C., Chinkers M. Identification of amino acids in the tetratricopeptide repeat and C-terminal domains of protein phosphatase 5 involved in autoinhibition and lipid activation. Biochemistry 2001, 40:10485-10490.
21. Kuranaga E., Kanuka H., Igaki T., Sawamoto K., Ichijo H., Okano H., Miura M. Reaper-mediated inhibition of DIAP1-induced DTRAF1 degradation results in activation of JNK in Drosophila. Nat. Cell Biol. 2002, 4:705-710.
22. Kyriakis J.M., Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 2001, 81:807-869.
23. Liu H., Nishitoh H., Ichijo H., Kyriakis J.M. Activation of apoptosis signal-regulating kinase 1 (ASK1) by tumor necrosis factor receptor-associated factor 2 requires prior dissociation of the ASK1 inhibitor thioredoxin. Mol. Cell. Biol. 2000, 20:2198-2208.
24. Mahrour N., Redwine W.B., Florens L., Swanson S.K., Martin-Brown S., Bradford W.D., Staehling-Hampton K., Washburn M.P., Conaway R.C., Conaway J.W. Characterization of Cullin-box sequences that direct recruitment of Cul2-Rbx1 and Cul5-Rbx2 modules to Elongin BC-based ubiquitin ligases. J. Biol. Chem. 2008, 283:8005-8013.
25. Matsuzawa A., Saegusa K., Noguchi T., Sadamitsu C., Nishitoh H., Nagai S., Koyasu S., Matsumoto K., Takeda K., Ichijo H. ROS-dependent activation of the TRAF6-ASK1-p38 pathway is selectively required for TLR4-mediated innate immunity. Nat. Immunol. 2005, 6:587-592.
26. Morita K., Saitoh M., Tobiume K., Matsuura H., Enomoto S., Nishitoh H., Ichijo H. Negative feedback regulation of ASK1 by protein phosphatase 5 (PP5) in response to oxidative stress. EMBO J. 2001, 20:6028-6036.
27. Nagai H., Noguchi T., Takeda K., Ichijo H. Pathophysiological roles of ASK1-MAP kinase signaling pathways. J. Biochem. Mol. Biol. 2007, 40:1-6.
28. Nagai H., Noguchi T., Homma K., Katagiri K., Takeda K., Matsuzawa A., Ichijo H. Ubiquitin-like sequence in ASK1 plays critical roles in the recognition and stabilization by USP9X and oxidative stress-induced cell death. Mol. Cell 2009, 36:805-818.
29. Nishitoh H., Saitoh M., Mochida Y., Takeda K., Nakano H., Rothe M., Miyazono K., Ichijo H. ASK1 is essential for JNK/SAPK activation by TRAF2. Mol. Cell 1998, 2:389-395.
30. Noguchi T., Takeda K., Matsuzawa A., Saegusa K., Nakano H., Gohda J., Inoue J., Ichijo H. Recruitment of tumor necrosis factor receptor-associated factor family proteins to apoptosis signal-regulating kinase 1 signalosome is essential for oxidative stress-induced cell death. J. Biol. Chem. 2005, 280:37033-37040.
31. Noguchi T., Ishii K., Fukutomi H., Naguro I., Matsuzawa A., Takeda K., Ichijo H. Requirement of reactive oxygen species-dependent activation of ASK1-p38 MAPK pathway for extracellular ATP-induced apoptosis in macrophage. J. Biol. Chem. 2008, 283:7657-7665.
32. Petroski M.D., Deshaies R.J. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 2005, 6:9-20.
33. Prag S., Adams J.C. Molecular phylogeny of the kelch-repeat superfamily reveals an expansion of BTB/kelch proteins in animals. BMC Bioinformatics 2003, 4:42.
34. Saitoh M., Nishitoh H., Fujii M., Takeda K., Tobiume K., Sawada Y., Kawabata M., Miyazono K., Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 1998, 17:2596-2606.
35. Sekine Y., Takagahara S., Hatanaka R., Watanabe T., Oguchi H., Noguchi T., Naguro I., Kobayashi K., Tsunoda M., Funatsu T., et al. p38 MAPKs regulate the expression of genes in the dopamine synthesis pathway through phosphorylation of NR4A nuclear receptors. J. Cell Sci. 2011, 124:3006-3016.
36. Skinner J., Sinclair C., Romeo C., Armstrong D., Charbonneau H., Rossie S. Purification of a fatty acid-stimulated protein-serine/threonine phosphatase from bovine brain and its identification as a homolog of protein phosphatase 5. J. Biol. Chem. 1997, 272:22464-22471.
37. Takeda K., Noguchi T., Naguro I., Ichijo H. Apoptosis signal-regulating kinase 1 in stress and immune response. Annu. Rev. Pharmacol. Toxicol. 2008, 48:199-225.
38. Toba G., Ohsako T., Miyata N., Ohtsuka T., Seong K.H., Aigaki T. The gene search system. A method for efficient detection and rapid molecular identification of genes in Drosophila melanogaster. Genetics 1999, 151:725-737.
39. Tobiume K., Matsuzawa A., Takahashi T., Nishitoh H., Morita K., Takeda K., Minowa O., Miyazono K., Noda T., Ichijo H. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep. 2001, 2:222-228.
40. Tobiume K., Saitoh M., Ichijo H. Activation of apoptosis signal-regulating kinase 1 by the stress-induced activating phosphorylation of pre-formed oligomer. J. Cell. Physiol. 2002, 191:95-104.
41. Widmann C., Gibson S., Jarpe M.B., Johnson G.L. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol. Rev. 1999, 79:143-180.
42. Yamaguchi Y., Katoh H., Mori K., Negishi M. Galpha(12) and Galpha(13) interact with Ser/Thr protein phosphatase type 5 and stimulate its phosphatase activity. Curr. Biol. 2002, 12:1353-1358.
43. Yang J., Roe S.M., Cliff M.J., Williams M.A., Ladbury J.E., Cohen P.T., Barford D. Molecular basis for TPR domain-mediated regulation of protein phosphatase 5. EMBO J. 2005, 24:1-10.
44. Zeke T., Morrice N., Vázquez-Martin C., Cohen P.T. Human protein phosphatase 5 dissociates from heat-shock proteins and is proteolytically activated in response to arachidonic acid and the microtubule-depolymerizing drug nocodazole. Biochem. J. 2005, 385:45-56.