Apoptosis signal-regulating kinase 1 as a therapeutic target

Expert Opinion on Therapeutic Targets

Volumn 18, Issue 6, 2014, Pages 651-664

  Kawarazaki, Yosuke ^a   Ichijo, Hidenori ^a   Naguro, Isao ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Apoptosis; Apoptosis signal regulating kinase 1; Cancer; Endoplasmic reticulum stress; Infection; Neurodegenerative diseases; Oxidative stress

Indexed keywords

APOPTOSIS SIGNAL REGULATING KINASE 1; CYTOKINE; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; CELL STRESS; DEGENERATIVE DISEASE; ENDOPLASMIC RETICULUM STRESS; ENZYME ANALYSIS; REVIEW; ANIMAL; ANTAGONISTS AND INHIBITORS; COLONIC NEOPLASMS; DIABETES MELLITUS; HUMAN; NEURODEGENERATIVE DISEASES; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; STOMACH NEOPLASMS; UBIQUITINATION;

ANIMALS; APOPTOSIS; COLONIC NEOPLASMS; DIABETES MELLITUS; HUMANS; MAP KINASE KINASE KINASE 5; MAP KINASE SIGNALING SYSTEM; NEURODEGENERATIVE DISEASES; PHOSPHORYLATION; SKIN NEOPLASMS; STOMACH NEOPLASMS; UBIQUITINATION;

EID: 84900796050     PISSN: 14728222     EISSN: 17447631     Source Type: Journal    
DOI: 10.1517/14728222.2014.896903     Document Type: Review

References (95)

1. Tibbles LA, Woodgett JR. The stress-activated protein kinase pathways. Cell Mol Life Sci 1999;55:1230-54
2. Wagner EF, Nebreda AR. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 2009;9:537-49
3. Kim EK, Choi EJ. Pathological roles of MAPK signaling pathways in human diseases. Biochim Biophys Acta 2010;1802:396-405
4. Muslin AJ. MAPK signalling in cardiovascular health and disease: molecular mechanisms and therapeutic targets. Clin Sci 2008;115:203-18
5. Ichijo H, Nishida E, Irie K, et al. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 1997;275:90-4
6. Saitoh M, Nishitoh H, Fujii M, et al. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. Embo J 1998;17:2596-606
7. Gotoh Y, Cooper JA. Reactive oxygen species-and dimerization-induced activation of apoptosis signal-regulating kinase 1 in tumor necrosis factor-alpha signal transduction. J Biol Chem 1998;273:17477-82
8. Nishitoh H, Matsuzawa A, Tobiume K, et al. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 2002;16:1345-55
9. Takeda K, Matsuzawa A, Nishitoh H, et al. Involvement of ASK1 in Ca2+-induced p38 MAP kinase activation. EMBO Rep 2004;5:161-6
10. Matsuzawa A, Saegusa K, Noguchi T, et al. ROS-dependent activation of the TRAF6-ASK1-p38 pathway is selectively required for TLR4-mediated innate immunity. Nat Immunol 2005;6:587-92
11. Kanamoto T, Mota M, Takeda K, et al. Role of apoptosis signal-regulating kinase in regulation of the c-Jun N-terminal kinase pathway and apoptosis in sympathetic neurons. Mol Cell Biol 2000;20:196-204
12. Tobiume K, Matsuzawa A, Takahashi T, et al. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2001;2:222-8
13. Noguchi T, Ishii K, Fukutomi H, et al. Requirement of reactive oxygen species-dependent activation of ASK1-p38 MAPK pathway for extracellular ATP-induced apoptosis in macrophage. J Biol Chem 2008;283:7657-65
14. Takeda K, Hatai T, Hamazaki TS, et al. Apoptosis signal-regulating kinase 1 (ASK1) induces neuronal differentiation and survival of PC12 cells. J Biol Chem 2000;275:9805-13
15. Sayama K, Hanakawa Y, Shirakata Y, et al. Apoptosis signal-regulating kinase 1 (ASK1) is an intracellular inducer of keratinocyte differentiation. J Biol Chem 2001;276:999-1004
16. Iriyama T, Takeda K, Nakamura H, et al. ASK1 and ASK2 differentially regulate the counteracting roles of apoptosis and inflammation in tumorigenesis. EMBO J 2009;28:843-53
17. Hayakawa Y, Hirata Y, Nakagawa H, et al. Apoptosis signal-regulating kinase 1 and cyclin D1 compose a positive feedback loop contributing to tumor growth in gastric cancer. Proc Natl Acad Sci USA 2011;108:780-5
18. Hayakawa Y, Hirata Y, Nakagawa H, et al. Apoptosis signal-regulating kinase 1 regulates colitis and colitis-associated tumorigenesis by the innate immune responses. Gastroenterology 2010;138:1055-67.e1-4
19. Nishitoh H, Kadowaki H, Nagai A, et al. ALS-linked mutant SOD1 induces ER stress-and ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev 2008;22:1451-64
20. Kadowaki H, Nishitoh H, Urano F, et al. Amyloid beta induces neuronal cell death through ROS-mediated ASK1 activation. Cell Death Differ 2005;12:19-24
21. Lee KW, Zhao X, Im JY, et al. Apoptosis signal-regulating kinase 1 mediates MPTP toxicity and regulates glial activation. PLoS One 2012;7:e29935
22. Tobiume K, Inage T, Takeda K, et al. Molecular cloning and characterization of the mouse apoptosis signal-regulating kinase 1. Biochem Biophys Res Commun 1997;239:905-10
23. Kuranaga E, Kanuka H, Igaki T, et al. Reaper-mediated inhibition of DIAP1-induced DTRAF1 degradation results in activation of JNK in Drosophila. Nat Cell Biol 2002;4:705-10
24. Sagasti A, Hisamoto N, Hyodo J, et al. The CaMKII UNC-43 activates the MAPKKK NSY-1 to execute a lateral signaling decision required for asymmetric olfactory neuron fates. Cell 2001;105:221-32
25. Cho JH, Lee MK, Yoon KW, et al. Arginine methylation-dependent regulation of ASK1 signaling by PRMT1. Cell Death Differ 2012;19:859-70
26. Moudgil KD, Choubey D. Cytokines in autoimmunity: role in induction, regulation, and treatment. J Interferon Cytokine Res 2011;31:695-703
27. 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
28. Taylor SS, Ilouz R, Zhang P, Kornev AP. Assembly of allosteric macromolecular switches: lessons from PKA. Nat Rev Mol Cell Biol 2012;13:646-58
29. Fujino G, Noguchi T, Matsuzawa A, et al. 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;27:8152-63
30. Nishitoh H, Saitoh M, Mochida Y, et al. ASK1 is essential for JNK/SAPK activation by TRAF2. Mol Cell 1998;2:389-95
31. Noguchi T, Takeda K, Matsuzawa A, et al. 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;280:37033-40
32. Morita K, Saitoh M, Tobiume K, et al. Negative feedback regulation of ASK1 by protein phosphatase 5 (PP5) in response to oxidative stress. EMBO J 2001;20:6028-36
33. Sekine Y, Hatanaka R, Watanabe T, et al. The Kelch repeat protein KLHDC10 regulates oxidative stress-induced ASK1 activation by suppressing PP5. Mol Cell 2012;48:692-704
34. Maruyama T, Araki T, Kawarazaki Y, et al. Roquin-2 promotes ubiquitin-mediated degradation of ASK1 to regulate stress responses. Sci Signal 2014;7:ra8
35. Nagai H, Noguchi T, Homma K, et al. Ubiquitin-like sequence in ASK1 plays critical roles in the recognition and stabilization by USP9X and oxidative stress-induced cell death. Mol Cell 2009;36:805-18
36. Puckett MC, Goldman EH, Cockrell LM, et al. Integration of apoptosis signal-regulating kinase 1-mediated stress signaling with the Akt/protein kinase B-IkappaB kinase cascade. Mol Cell Biol 2013;33:2252-9
37. Liu QH, Wilkins BJ, Lee YJ, et al. Direct interaction and reciprocal regulation between ASK1 and calcineurin-NFAT control cardiomyocyte death and growth. Mol Cell Biol 2006;26:3785-97
38. Zhang L, Chen J, Fu H. Suppression of apoptosis signal-regulating kinase 1-induced cell death by 14-3-3 proteins. Proc Natl Acad Sci USA 1999;96:8511-15
39. Kim AH, Khursigara G, Sun X, et al. Akt phosphorylates and negatively regulates apoptosis signal-regulating kinase 1. Mol Cell Biol 2001;21:893-901
40. Takeda K, Shimozono R, Noguchi T, et al. Apoptosis signal-regulating kinase (ASK) 2 functions as a mitogen-activated protein kinase kinase kinase in a heteromeric complex with ASK1. J Biol Chem 2007;282:7522-31
41. Wang XS, Diener K, Tan TH, Yao Z. MAPKKK6, a novel mitogen-activated protein kinase kinase kinase, that associates with MAPKKK5. Biochem Biophys Res Commun 1998;253:33-7
42. Humphreys JM, Piala AT, Akella R, et al. Precisely ordered phosphorylation reactions in the p38 MAP kinase cascade. J Biol Chem 2013;288:23322-30
43. Morrison DK, Davis RJ. Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu Rev Cell Dev Biol 2003;19:91-118
44. Kocieniewski P, Faeder JR, Lipniacki T. The interplay of double phosphorylation and scaffolding in MAPK pathways. J Theor Biol 2012;295:116-24
45. Hatai T, Matsuzawa A, Inoshita S, et al. Execution of apoptosis signal-regulating kinase 1 (ASK1)-induced apoptosis by the mitochondria- dependent caspase activation. J Biol Chem 2000;275:26576-81
46. Tait SWG, Green DR. Caspase-independent cell death: leaving the set without the final cut. Oncogene 2008;27:6452-61
47. Tang D, Kang R, Coyne CB, et al. PAMPs and DAMPs: signal 0s that spur autophagy and immunity. Immunol Rev 2012;249:158-75
48. Kim DH, Feinbaum R, Alloing G, et al. A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 2002;297:623-6
49. Shivers RP, Kooistra T, Chu SW, et al. Tissue-specific activities of an immune signaling module regulate physiological responses to pathogenic and nutritional bacteria in C. elegans. Cell Host Microbe 2009;6:321-30
50. Sekine Y, Takagahara S, Hatanaka R, et al. p38 MAPKs regulate the expression of genes in the dopamine synthesis pathway through phosphorylation of NR4A nuclear receptors. J Cell Sci 2011;124:3006-16
51. Hayakawa Y, Hirata Y, Sakitani K, et al. Apoptosis signal-regulating kinase-1 inhibitor as a potent therapeutic drug for the treatment of gastric cancer. Cancer Sci 2012;103:2181-5
52. Podolsky DK. Inflammatory bowel disease. N Engl J Med 2002;347:417-29
53. Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol 2004;287:G7-17
54. Yoshihara T, Ishigaki S, Yamamoto M, et al. Differential expression of inflammation-and apoptosis-related genes in spinal cords of a mutant SOD1 transgenic mouse model of familial amyotrophic lateral sclerosis. J Neurochem 2002;80:158-67
55. Kunst CB, Mezey E, Brownstein MJ, Patterson D. Mutations in SOD1 associated with amyotrophic lateral sclerosis cause novel protein interactions. Nat Genet 1997;15:91-4
56. Pasinelli P, Borchelt DR, Houseweart MK, et al. Caspase-1 is activated in neural cells and tissue with amyotrophic lateral sclerosis-associated mutations in copper-zinc superoxide dismutase. Proc Natl Acad Sci USA 1998;95:15763-8
57. Bowling AC, Schulz JB, Brown RH Jr, Beal MF. Superoxide dismutase activity, oxidative damage, and mitochondrial energy metabolism in familial and sporadic amyotrophic lateral sclerosis. J Neurochem 1993;61:2322-5
58. Tobisawa S, Hozumi Y, Arawaka S, et al. Mutant SOD1 linked to familial amyotrophic lateral sclerosis, but not wild-type SOD1, induces ER stress in COS7 cells and transgenic mice. Biochem Biophys Res Commun 2003;303:496-503
59. Sekine Y, Takeda K, Ichijo H. The ASK1-MAP kinase signaling in ER stress and neurodegenerative diseases. Curr Mol Med 2006;6:87-97
60. Fujisawa T, Homma K, Yamaguchi N, et al. A novel monoclonal antibody reveals a conformational alteration shared by amyotrophic lateral sclerosis-linked SOD1 mutants. Ann Neurol 2012;72:739-49
61. Urano F, Wang X, Bertolotti A, et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000;287:664-6
62. Kakizuka A. Protein precipitation: a common etiology in neurodegenerative disorders? Trends Genet 1998;14:396-402
63. Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001;292:1552-5
64. Yankner BA. Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron 1996;16:921-32
65. Suzuki N, Cheung TT, Cai XD, et al. An increased percentage of long amyloid beta protein secreted by familial amyloid beta protein precursor (beta APP717) mutants. Science 1994;264:1336-40
66. Tillement L, Lecanu L, Papadopoulos V. Alzheimer's disease: effects of beta-amyloid on mitochondria. Mitochondrion 2011;11:13-21
67. Valente EM, Abou-Sleiman PM, Caputo V, et al. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 2004;304:1158-60
68. Shen J. Protein kinases linked to the pathogenesis of Parkinson's disease. Neuron 2004;44:575-7
69. Bonifati V, Rizzu P, van Baren MJ, et al. Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 2003;299:256-9
70. Kitada T, Asakawa S, Hattori N, et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998;392:605-8
71. Duty S, Jenner P. Animal models of Parkinson's disease: a source of novel treatments and clues to the cause of the disease. Br J Pharmacol 2011;164:1357-91
72. Maruoka S, Hashimoto S, Gon Y, et al. ASK1 regulates influenza virus infection-induced apoptotic cell death. Biochem Biophys Res Commun 2003;307:870-6
73. Lu X, Masic A, Li Y, et al. The PI3K/Akt pathway inhibits influenza A virus-induced Bax-mediated apoptosis by negatively regulating the JNK pathway via ASK1. J Gen Virol 2010;91:1439-49
74. Jaworowski A, Crowe SM. Does HIV cause depletion of CD4+ T cells in vivo by the induction of apoptosis? Immunol Cell Biol 1999;77:90-8
75. Geleziunas R, Xu WD, Takeda K, et al. HIV-1 Nef inhibits ASK1-dependent death signalling providing a potential mechanism for protecting the infected host cell. Nature 2001;410:834-8
76. Bhattacharyya A, Pathak S, Basak C, et al. Execution of macrophage apoptosis by Mycobacterium avium through apoptosis signal-regulating kinase 1/p38 mitogen-activated protein kinase signaling and caspase 8 activation. J Biol Chem 2003;278:26517-25
77. Hawkins CC, Gold JW, Whimbey E, et al. Mycobacterium avium complex infections in patients with the acquired immunodeficiency syndrome. Ann Intern Med 1986;105:184-8
78. Fratazzi C, Arbeit RD, Carini C, Remold HG. Programmed cell death of Mycobacterium avium serovar 4-infected human macrophages prevents the mycobacteria from spreading and induces mycobacterial growth inhibition by freshly added, uninfected macrophages. J Immunol 1997;158:4320-7
79. Glickman MS, Jacobs WR. Microbial pathogenesis of Mycobacterium tuberculosis: dawn of a discipline. Cell 2001;104:477-85
80. Kundu M, Pathak SK, Kumawat K, et al. A TNF-and c-Cbl-dependent FLIP (S)-degradation pathway and its function in Mycobacterium tuberculosis-induced macrophage apoptosis. Nat Immunol 2009;10:918-26
81. Sospedra M, Martin R. Immunology of multiple sclerosis. Annu Rev Immunol 2005;23:683-747
82. Guo X, Harada C, Namekata K, et al. Regulation of the severity of neuroinflammation and demyelination by TLR-ASK1-p38 pathway. EMBO Mol Med 2010;2:504-15
83. Saltiel AR, Kahn CR. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 2001;414:799-806
84. Zick Y. Ser/Thr phosphorylation of IRS proteins: a molecular basis for insulin resistance. Sci STKE 2005;2005:pe4
85. Kanety H, Feinstein R, Papa MZ, et al. Tumor necrosis factor alpha-induced phosphorylation of insulin receptor substrate-1 (IRS-1). Possible mechanism for suppression of insulin-stimulated tyrosine phosphorylation of IRS-1. J Biol Chem 1995;270:23780-4
86. Aguirre V, Uchida T, Yenush L, et al. The c-Jun NH2-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser (307). J Biol Chem 2000;275:9047-54
87. Imoto K, Kukidome D, Nishikawa T, et al. Impact of mitochondrial reactive oxygen species and apoptosis signal-regulating kinase 1 on insulin signaling. Diabetes 2006;55:1197-204
88. Yamaguchi K, Takeda K, Kadowaki H, et al. Involvement of ASK1-p38 pathway in the pathogenesis of diabetes triggered by pancreatic ss cell exhaustion. Biochim Biophys Acta 2013;1830:3656-63
89. Levy D, Garrison RJ, Savage DD, et al. Prognostic implications of echocardiographically determined left ventricular mass in the Framingham Heart Study. N Engl J Med 1990;322:1561-6
90. Izumiya Y, Kim S, Izumi Y, et al. Apoptosis signal-regulating kinase 1 plays a pivotal role in angiotensin II-induced cardiac hypertrophy and remodeling. Circ Res 2003;93:874-83
91. Hirotani S, Otsu K, Nishida K, et al. Involvement of nuclear factor-kappaB and apoptosis signal-regulating kinase 1 in G-protein-coupled receptor agonist-induced cardiomyocyte hypertrophy. Circulation 2002;105:509-15
92. Kashiwase K, Higuchi Y, Hirotani S, et al. CaMKII activates ASK1 and NF-kappaB to induce cardiomyocyte hypertrophy. Biochem Biophys Res Commun 2005;327:136-42
93. Bogoyevitch MA, Ngoei KR, Zhao TT, et al. c-Jun N-terminal kinase (JNK) signaling: recent advances and challenges. Biochim Biophys Acta 2010;1804:463-75
94. Tudor C, Marchese FP, Hitti E, et al. The p38 MAPK pathway inhibits tristetraprolin-directed decay of interleukin-10 and pro-inflammatory mediator mRNAs in murine macrophages. FEBS Lett 2009;583:1933-8
95. Aouadi M, Binetruy B, Caron L, et al. Role of MAPKs in development and differentiation: lessons from knockout mice. Biochimie 2006;88:1091-8