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Molecular Mechanism of Reactive Oxygen Species-dependent ASK1 Activation in Innate Immunity

  • Yamauchi, Shota (Laboratory of Cell Signaling, Graduate School of Pharmaceutical Sciences, Strategic Approach to Drug Discovery and Development in Pharmaceutical Sciences, Center of Excellence (COE) Program, and Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Corporation, The University of Tokyo) ;
  • Noguchi, Takuya (Laboratory of Cell Signaling, Graduate School of Pharmaceutical Sciences, Strategic Approach to Drug Discovery and Development in Pharmaceutical Sciences, Center of Excellence (COE) Program, and Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Corporation, The University of Tokyo) ;
  • Ichijo, Hidenori (Laboratory of Cell Signaling, Graduate School of Pharmaceutical Sciences, Strategic Approach to Drug Discovery and Development in Pharmaceutical Sciences, Center of Excellence (COE) Program, and Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Corporation, The University of Tokyo)
  • Published : 2008.03.30
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Abstract

Apoptosis signal-regulating kinase 1 (ASK1), a mitogen- activated protein kinase kinase kinase, plays pivotal roles in stress responses. In addition, ASK1 has emerged as a key regulator of immune responses elicited by pathogen-associated molecular patterns (PAMPs) and endogenous danger signals. Recent studies have demonstrated that reactive oxygen species (ROS)-dependent activation of ASK1 is required for LPS-stimulated cytokine production as well as extracellular ATP-induced apoptosis in immune cells. The mechanism of ROS-dependent regulation of ASK1 activity by thioredoxin and TRAFs has been well characterized. In this review, we focus on the molecular details of the activation of ASK1 and its involvement in innate immunity.

Keywords

References

  1. Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81:807-69, 2001 https://doi.org/10.1152/physrev.2001.81.2.807
  2. 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 275:90-4, 1997 https://doi.org/10.1126/science.275.5296.90
  3. 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 2:389-95, 1998 https://doi.org/10.1016/S1097-2765(00)80283-X
  4. 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 2:222-8, 2001 https://doi.org/10.1093/embo-reports/kve046
  5. Takeda K, Matsuzawa A, Nishitoh H, Tobiume K, Kishida S, Ninomiya-Tsuji J, Matsumoto K, Ichijo H. Involvement of ASK1 in Ca2+-induced p38 MAP kinase activation. EMBO Rep 5:161-6, 2004 https://doi.org/10.1038/sj.embor.7400072
  6. Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, Inoue K, Hori S, Kakizuka A, Ichijo H. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 16:1345-55, 2002 https://doi.org/10.1101/gad.992302
  7. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 124:783-801, 2006 https://doi.org/10.1016/j.cell.2006.02.015
  8. 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 6:587-92, 2005 https://doi.org/10.1038/ni1200
  9. Hayakawa T, Matsuzawa A, Noguchi T, Takeda K, Ichijo H. The ASK1-MAP kinase pathways in immune and stress responses. Microbes Infect 8:1098-107, 2006 https://doi.org/10.1016/j.micinf.2005.12.001
  10. Skoberne M, Beignon AS, Bhardwaj N. Danger signals: a time and space continuum. Trends Mol Med 10:251-7, 2004 https://doi.org/10.1016/j.molmed.2004.04.001
  11. Takeda K, Noguchi T, Naguro I, Ichijo H. Apoptosis Signal-Regulating Kinase 1 in Stress and Immune Response. Annu Rev Pharmacol Toxicol, 2007
  12. Fujino G, Noguchi T, Takeda K, Ichijo H. Thioredoxin and protein kinases in redox signaling. Semin Cancer Biol 16:427-35, 2006 https://doi.org/10.1016/j.semcancer.2006.09.003
  13. 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 280: 37033-40, 2005 https://doi.org/10.1074/jbc.M506771200
  14. Powis G, Montfort WR. Properties and biological activities of thioredoxins. Annu Rev Biophys Biomol Struct 30:421-55, 2001 https://doi.org/10.1146/annurev.biophys.30.1.421
  15. Masutani H, Ueda S, Yodoi J. The thioredoxin system in retroviral infection and apoptosis. Cell Death Differ 12 Suppl 1:991-8, 2005 https://doi.org/10.1038/sj.cdd.4401625
  16. 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 17:2596-606, 1998 https://doi.org/10.1093/emboj/17.9.2596
  17. 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 27:8152-63, 2007 https://doi.org/10.1128/MCB.00227-07
  18. Liu H, Nishitoh H, Ichijo H, Kyriakis JM. 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 20:2198-208, 2000 https://doi.org/10.1128/MCB.20.6.2198-2208.2000
  19. Chung JY, Park YC, Ye H, Wu H. All TRAFs are not created equal: common and distinct molecular mechanisms of TRAF-mediated signal transduction. J Cell Sci 115:679-88, 2002
  20. 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 191:95-104, 2002 https://doi.org/10.1002/jcp.10080
  21. Ohto U, Fukase K, Miyake K, Satow Y. Crystal structures of human MD-2 and its complex with antiendotoxic lipid IVa. Science 316:1632-4, 2007 https://doi.org/10.1126/science.1139111
  22. Symons A, Beinke S, Ley SC. MAP kinase kinase kinases and innate immunity. Trends Immunol 27:40-8, 2006 https://doi.org/10.1016/j.it.2005.11.007
  23. Huang Q, Yang J, Lin Y, Walker C, Cheng J, Liu ZG, Su B. Differential regulation of interleukin 1 receptor and Toll-like receptor signaling by MEKK3. Nat Immunol 5:98-103, 2004 https://doi.org/10.1038/ni1014
  24. Dumitru CD, Ceci JD, Tsatsanis C, Kontoyiannis D, Stamatakis K, Lin JH, Patriotis C, Jenkins NA, Copeland NG, Kollias G, Tsichlis PN. TNF-alpha induction by LPS is regulated posttranscriptionally via a Tpl2/ERK-dependent pathway. Cell 103:1071-83, 2000 https://doi.org/10.1016/S0092-8674(00)00210-5
  25. Grandvaux N, Soucy-Faulkner A, Fink K. Innate host defense: Nox and Duox on phox's tail. Biochimie 89:1113-22, 2007 https://doi.org/10.1016/j.biochi.2007.04.008
  26. Park HS, Jung HY, Park EY, Kim J, Lee WJ, Bae YS. Cutting edge: direct interaction of TLR4 with NAD(P)H oxidase 4 isozyme is essential for lipopolysaccharide-induced production of reactive oxygen species and activation of NF-kappa B. J Immunol 173:3589-93, 2004 https://doi.org/10.4049/jimmunol.173.6.3589
  27. Chiang E, Dang O, Anderson K, Matsuzawa A, Ichijo H, David M. Cutting edge: apoptosis-regulating signal kinase 1 is required for reactive oxygen species-mediated activation of IFN regulatory factor 3 by lipopolysaccharide. J Immunol 176:5720-4, 2006 https://doi.org/10.4049/jimmunol.176.10.5720
  28. Bodin P, Burnstock G. Purinergic signalling: ATP release. Neurochem Res 26:959-69, 2001 https://doi.org/10.1023/A:1012388618693
  29. Khakh BS, North RA. P2X receptors as cell-surface ATP sensors in health and disease. Nature 442:527-32, 2006 https://doi.org/10.1038/nature04886
  30. Ferrari D, Pizzirani C, Adinolfi E, Lemoli RM, Curti A, Idzko M, Panther E, Di Virgilio F. The P2X7 receptor: a key player in IL-1 processing and release. J Immunol 176:3877-83, 2006 https://doi.org/10.4049/jimmunol.176.7.3877
  31. Lister MF, Sharkey J, Sawatzky DA, Hodgkiss JP, Davidson DJ, Rossi AG, Finlayson K. The role of the purinergic P2X7 receptor in inflammation. J Inflamm (Lond) 4:5, 2007 https://doi.org/10.1186/1476-9255-4-5
  32. Lammas DA, Stober C, Harvey CJ, Kendrick N, Panchalingam S, Kumararatne DS. ATP-induced killing of mycobacteria by human macrophages is mediated by purinergic P2Z(P2X7) receptors. Immunity 7:433-44, 1997 https://doi.org/10.1016/S1074-7613(00)80364-7
  33. Wang C, Deng L, Hong M, Akkaraju GR, Inoue J, Chen ZJ. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412:346-51, 2001 https://doi.org/10.1038/35085597
  34. Adhikari A, Xu M, Chen ZJ. Ubiquitin-mediated activation of TAK1 and IKK. Oncogene 26:3214-26, 2007 https://doi.org/10.1038/sj.onc.1210413
  35. Sato S, Sanjo H, Takeda K, Ninomiya-Tsuji J, Yamamoto M, Kawai T, Matsumoto K, Takeuchi O, Akira S. Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat Immunol 6:1087-95, 2005 https://doi.org/10.1038/ni1255
  36. Yamamoto M, Okamoto T, Takeda K, Sato S, Sanjo H, Uematsu S, Saitoh T, Yamamoto N, Sakurai H, Ishii KJ, Yamaoka S, Kawai T, Matsuura Y, Takeuchi O, Akira S. Key function for the Ubc13 E2 ubiquitin-conjugating enzyme in immune receptor signaling. Nat Immunol 7:962-70, 2006 https://doi.org/10.1038/ni1367
  37. Fukushima T, Matsuzawa S, Kress CL, Bruey JM, Krajewska M, Lefebvre S, Zapata JM, Ronai Z, Reed JC. Ubiquitin-conjugating enzyme Ubc13 is a critical component of TNF receptor-associated factor (TRAF)-mediated inflammatory responses. Proc Natl Acad Sci USA 104:6371-6, 2007 https://doi.org/10.1073/pnas.0700548104
  38. Bunkoczi G, Salah E, Filippakopoulos P, Fedorov O, Muller S, Sobott F, Parker SA, Zhang H, Min W, Turk BE, Knapp S. Structural and functional characterization of the human protein kinase ASK1. Structure 15:1215-26, 2007 https://doi.org/10.1016/j.str.2007.08.011