Mechanisms of MAVS regulation at the mitochondrial membrane

Journal of Molecular Biology

Volumn 425, Issue 24, 2013, Pages 5009-5019

  Jacobs, Jana L ^a   Coyne, Carolyn B ^b  

^a UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

innate immunity; MAVS; MDA5; RIG I

Indexed keywords

ABELSON KINASE; BINDING PROTEIN; CELL MEMBRANE PROTEIN; CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE 5 B PROTEIN; FOCAL ADHESION KINASE; GC 1 QR PROTEIN; INTERFERON INDUCED PROTEIN WITH TETRATRICOPEPTIDE REPEAT 3; LGP 2 PROTEIN; MITOCHONDRIAL ANTIVIRAL SIGNALING PROTEIN; MITOCHONDRIAL PROTEIN; MITOFUSIN 1; MITOFUSIN 2; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR X 1; POLO LIKE KINASE 1; POLY RC BINDING PROTEIN 2; SMURF 1 PROTEIN; TETRASPANIN PROTEIN 6; TETRATRICOPEPTIDE REPEAT PROTEIN; TRIPARTITE MOTIF PROTEIN 5; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG;

HUMAN; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

EID: 84887990870     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.10.007     Document Type: Review

References (95)

1. S.M. Cloonan, and A.M. Choi Mitochondria: sensors and mediators of innate immune receptor signaling Curr Opin Microbiol 16 2013 327 338
2. S.M. Cloonan, and A.M. Choi Mitochondria: commanders of innate immunity and disease? Curr Opin Immunol 24 2012 32 40
3. R.J. Youle, and A.M. van der Bliek Mitochondrial fission, fusion, and stress Science 337 2012 1062 1065
4. G. Csordas, C. Renken, P. Varnai, L. Walter, D. Weaver, and K.F. Buttle Structural and functional features and significance of the physical linkage between ER and mitochondria J Cell Biol 174 2006 915 921
5. A.A. Rowland, and G.K. Voeltz Endoplasmic reticulum-mitochondria contacts: function of the junction Nat Rev Mol Cell Biol 13 2012 607 625
6. L. Galluzzi, O. Kepp, and G. Kroemer Mitochondria: master regulators of danger signalling Nat Rev Mol Cell Biol 13 2012 780 788
7. E. Meylan, J. Curran, K. Hofmann, D. Moradpour, M. Binder, and R. Bartenschlager Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus Nature 437 2005 1167 1172
8. T. Kawai, K. Takahashi, S. Sato, C. Coban, H. Kumar, and H. Kato IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction Nat Immunol 6 2005 981 988
9. R.B. Seth, L. Sun, C.K. Ea, and Z.J. Chen Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3 Cell 122 2005 669 682
10. L.G. Xu, Y.Y. Wang, K.J. Han, L.Y. Li, Z. Zhai, and H.B. Shu VISA is an adapter protein required for virus-triggered IFN-beta signaling Mol Cell 19 2005 727 740
11. V.A. Rathinam, and K.A. Fitzgerald Innate immune sensing of DNA viruses Virology 411 2011 153 162
12. S.R. Paludan, and A.G. Bowie Immune sensing of DNA Immunity 38 2013 870 880
13. T. Kawai, and S. Akira Antiviral signaling through pattern recognition receptors J Biochem 141 2007 137 145
14. K.G. Harris, and C.B. Coyne Enter at your own risk: how enteroviruses navigate the dangerous world of pattern recognition receptor signaling Cytokine 63 2013 230 236
15. M. Yoneyama, M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, and M. Miyagishi The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses Nat Immunol 5 2004 730 737
16. T. Saito, R. Hirai, Y.M. Loo, D. Owen, C.L. Johnson, and S.C. Sinha Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2 Proc Natl Acad Sci USA 104 2007 582 587
17. M. Yoneyama, M. Kikuchi, K. Matsumoto, T. Imaizumi, M. Miyagishi, and K. Taira Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity J Immunol 175 2005 2851 2858
18. V. Hornung, J. Ellegast, S. Kim, K. Brzozka, A. Jung, and H. Kato 5′-Triphosphate RNA is the ligand for RIG-I Science 314 2006 994 997
19. A. Pichlmair, O. Schulz, C.P. Tan, T.I. Naslund, P. Liljestrom, and F. Weber RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates Science 314 2006 997 1001
20. A. Schmidt, T. Schwerd, W. Hamm, J.C. Hellmuth, S. Cui, and M. Wenzel 5′-Triphosphate RNA requires base-paired structures to activate antiviral signaling via RIG-I Proc Natl Acad Sci USA 106 2009 12067 12072
21. T. Saito, D.M. Owen, F. Jiang, J. Marcotrigiano, and M. Gale Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA Nature 454 2008 523 527
22. D. Uzri, and L. Gehrke Nucleotide sequences and modifications that determine RIG-I/RNA binding and signaling activities J Virol 83 2009 4174 4184
23. H. Kato, O. Takeuchi, E. Mikamo-Satoh, R. Hirai, T. Kawai, and K. Matsushita Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5 J Exp Med 205 2008 1601 1610
24. H. Kato, O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, and K. Matsui Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses Nature 441 2006 101 105
25. E. Dixit, S. Boulant, Y. Zhang, A.S. Lee, C. Odendall, and B. Shum Peroxisomes are signaling platforms for antiviral innate immunity Cell 141 2010 668 681
26. S.K. Saha, E.M. Pietras, J.Q. He, J.R. Kang, S.Y. Liu, and G. Oganesyan Regulation of antiviral responses by a direct and specific interaction between TRAF3 and Cardif EMBO J 25 2006 3257 3263
27. G. Oganesyan, S.K. Saha, B. Guo, J.Q. He, A. Shahangian, and B. Zarnegar Critical role of TRAF3 in the Toll-like receptor-dependent and -independent antiviral response Nature 439 2006 208 211
28. K.A. Fitzgerald, S.M. McWhirter, K.L. Faia, D.C. Rowe, E. Latz, and D.T. Golenbock IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway Nat Immunol 4 2003 491 496
29. M.C. Michallet, E. Meylan, M.A. Ermolaeva, J. Vazquez, M. Rebsamen, and J. Curran TRADD protein is an essential component of the RIG-like helicase antiviral pathway Immunity 28 2008 651 661
30. B. Guo, and G. Cheng Modulation of the interferon antiviral response by the TBK1/IKKi adaptor protein TANK J Biol Chem 282 2007 11817 11826
31. C. Richetta, and M. Faure Autophagy in antiviral innate immunity Cell Microbiol 15 2013 368 376
32. S. Rothenfusser, N. Goutagny, G. DiPerna, M. Gong, B.G. Monks, and A. Schoenemeyer The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I J Immunol 175 2005 5260 5268
33. A. Komuro, and C.M. Horvath RNA- and virus-independent inhibition of antiviral signaling by RNA helicase LGP2 J Virol 80 2006 12332 12342
34. E.D. Tang, and C.Y. Wang MAVS self-association mediates antiviral innate immune signaling J Virol 83 2009 3420 3428
35. T. Venkataraman, M. Valdes, R. Elsby, S. Kakuta, G. Caceres, and S. Saijo Loss of DExD/H box RNA helicase LGP2 manifests disparate antiviral responses J Immunol 178 2007 6444 6455
36. T. Satoh, H. Kato, Y. Kumagai, M. Yoneyama, S. Sato, and K. Matsushita LGP2 is a positive regulator of RIG-I- and MDA5-mediated antiviral responses Proc Natl Acad Sci USA 107 2010 1512 1517
37. I.C. Allen, C.B. Moore, M. Schneider, Y. Lei, B.K. Davis, and M.A. Scull NLRX1 protein attenuates inflammatory responses to infection by interfering with the RIG-I-MAVS and TRAF6-NF-kappaB signaling pathways Immunity 34 2011 854 865
38. M. Rebsamen, J. Vazquez, A. Tardivel, G. Guarda, J. Curran, and J. Tschopp NLRX1/NOD5 deficiency does not affect MAVS signalling Cell Death Differ 18 2011 1387
39. F. Soares, I. Tattoli, M.E. Wortzman, D. Arnoult, D.J. Philpott, and S.E. Girardin NLRX1 does not inhibit MAVS-dependent antiviral signalling Innate Immun 19 2012 438 448
40. A. Ling, F. Soares, D.O. Croitoru, I. Tattoli, L.A. Carneiro, and M. Boniotto Post-transcriptional inhibition of luciferase reporter assays by the Nod-like receptor proteins NLRX1 and NLRC3 J Biol Chem 287 2012 28705 28716
41. D.C. Chan Mitochondrial fusion and fission in mammals Annu Rev Cell Dev Biol 22 2006 79 99
42. O.M. de Brito, and L. Scorrano Mitofusin 2 tethers endoplasmic reticulum to mitochondria Nature 456 2008 605 610
43. K. Yasukawa, H. Oshiumi, M. Takeda, N. Ishihara, Y. Yanagi, and T. Seya Mitofusin 2 inhibits mitochondrial antiviral signaling Sci Signaling 2 2009 ra47
44. T. Koshiba, K. Yasukawa, Y. Yanagi, and S. Kawabata Mitochondrial membrane potential is required for MAVS-mediated antiviral signaling Sci Signaling 4 2011 ra7
45. X.Y. Liu, B. Wei, H.X. Shi, Y.F. Shan, and C. Wang Tom70 mediates activation of interferon regulatory factor 3 on mitochondria Cell Res 20 2010 994 1011
46. M.J. Baker, A.E. Frazier, J.M. Gulbis, and M.T. Ryan Mitochondrial protein-import machinery: correlating structure with function Trends Cell Biol 17 2007 456 464
47. K. Yang, H. Shi, R. Qi, S. Sun, Y. Tang, and B. Zhang Hsp90 regulates activation of interferon regulatory factor 3 and TBK-1 stabilization in Sendai virus-infected cells Mol Biol Cell 17 2006 1461 1471
48. J.C. Young, N.J. Hoogenraad, and F.U. Hartl Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70 Cell 112 2003 41 50
49. V. Fensterl, and G.C. Sen The ISG56/IFIT1 gene family J Interferon Cytokine Res 31 2011 71 78
50. X.Y. Liu, W. Chen, B. Wei, Y.F. Shan, and C. Wang IFN-induced TPR protein IFIT3 potentiates antiviral signaling by bridging MAVS and TBK1 J Immunol 187 2011 2559 2568
51. M.D. Beatch, J.C. Everitt, L.J. Law, and T.C. Hobman Interactions between rubella virus capsid and host protein p32 are important for virus replication J Virol 79 2005 10807 10820
52. M. Marschall, A. Marzi, P. aus dem Siepen, R. Jochmann, M. Kalmer, and S. Auerochs Cellular p32 recruits cytomegalovirus kinase pUL97 to redistribute the nuclear lamina J Biol Chem 280 2005 33357 33367
53. J. Dedio, W. Jahnen-Dechent, M. Bachmann, and W. Muller-Esterl The multiligand-binding protein gC1qR, putative C1q receptor, is a mitochondrial protein J Immunol 160 1998 3534 3542
54. P. Wang, L. Yang, G. Cheng, G. Yang, Z. Xu, and F. You UBXN1 interferes with Rig-I-like receptor-mediated antiviral immune response by targeting MAVS Cell Rep 3 2013 1057 1070
55. S. Liu, J. Chen, X. Cai, J. Wu, X. Chen, and Y.T. Wu MAVS recruits multiple ubiquitin E3 ligases to activate antiviral signaling cascades Elife 2 2013 e00785
56. K. Joseph, B. Ghebrehiwet, E.I. Peerschke, K.B. Reid, and A.P. Kaplan Identification of the zinc-dependent endothelial cell binding protein for high molecular weight kininogen and factor XII: identity with the receptor that binds to the globular "heads" of C1q (gC1q-R) Proc Natl Acad Sci USA 93 1996 8552 8557
57. L. Xu, N. Xiao, F. Liu, H. Ren, and J. Gu Inhibition of RIG-I and MDA5-dependent antiviral response by gC1qR at mitochondria Proc Natl Acad Sci USA 106 2009 1530 1535
58. C. Castanier, D. Garcin, A. Vazquez, and D. Arnoult Mitochondrial dynamics regulate the RIG-I-like receptor antiviral pathway EMBO Rep 11 2010 133 138
59. K. Onoguchi, K. Onomoto, S. Takamatsu, M. Jogi, A. Takemura, and S. Morimoto Virus-infection or 5′ppp-RNA activates antiviral signal through redistribution of IPS-1 mediated by MFN1 PLoS Pathog 6 2010 e1001012
60. F. Hou, L. Sun, H. Zheng, B. Skaug, Q.X. Jiang, and Z.J. Chen MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response Cell 146 2011 448 461
61. S.M. Horner, H.M. Liu, H.S. Park, J. Briley, and M. Gale Mitochondrial-associated endoplasmic reticulum membranes (MAM) form innate immune synapses and are targeted by hepatitis C virus Proc Natl Acad Sci USA 108 2011 14590 14595
62. R.A. Bozym, E. Delorme-Axford, K. Harris, S. Morosky, M. Ikizler, and T.S. Dermody Focal adhesion kinase is a component of antiviral RIG-I-like receptor signaling Cell Host Microbe 11 2012 153 166
63. A. Soucy-Faulkner, E. Mukawera, K. Fink, A. Martel, L. Jouan, and Y. Nzengue Requirement of NOX2 and reactive oxygen species for efficient RIG-I-mediated antiviral response through regulation of MAVS expression PLoS Pathog 6 2010 e1000930
64. M.C. Tal, M. Sasai, H.K. Lee, B. Yordy, G.S. Shadel, and A. Iwasaki Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling Proc Natl Acad Sci USA 106 2009 2770 2775
65. R. Gonzalez-Dosal, K.A. Horan, S.H. Rahbek, H. Ichijo, Z.J. Chen, and J.J. Mieyal HSV infection induces production of ROS, which potentiate signaling from pattern recognition receptors: role for S-glutathionylation of TRAF3 and 6 PLoS Pathog 7 2011 e1002250
66. M.C. Tal, and A. Iwasaki Autophagic control of RLR signaling Autophagy 5 2009 749 750
67. Y. Zhao, X. Sun, X. Nie, L. Sun, T.S. Tang, and D. Chen COX5B regulates MAVS-mediated antiviral signaling through interaction with ATG5 and repressing ROS production PLoS Pathog 8 2012 e1003086
68. D. Galati, S. Srinivasan, H. Raza, S.K. Prabu, M. Hardy, and K. Chandran Role of nuclear-encoded subunit Vb in the assembly and stability of cytochrome c oxidase complex: implications in mitochondrial dysfunction and ROS production Biochem J 420 2009 439 449
69. J.L. Campian, X. Gao, M. Qian, and J.W. Eaton Cytochrome C oxidase activity and oxygen tolerance J Biol Chem 282 2007 12430 12438
70. J. Huang, G.Y. Lam, and J.H. Brumell Autophagy signaling through reactive oxygen species Antioxid Redox Signaling 14 2011 2215 2231
71. D.J. Klionsky, and S.D. Emr Autophagy as a regulated pathway of cellular degradation Science 290 2000 1717 1721
72. P. Boya, F. Reggiori, and P. Codogno Emerging regulation and functions of autophagy Nat Cell Biol 15 2013 1017
73. Y. Jia, T. Song, C. Wei, C. Ni, Z. Zheng, and Q. Xu Negative regulation of MAVS-mediated innate immune response by PSMA7 J Immunol 183 2009 4241 4248
74. D. Voges, P. Zwickl, and W. Baumeister The 26S proteasome: a molecular machine designed for controlled proteolysis Annu Rev Biochem 68 1999 1015 1068
75. O. Coux, K. Tanaka, and A.L. Goldberg Structure and functions of the 20S and 26S proteasomes Annu Rev Biochem 65 1996 801 847
76. F. You, H. Sun, X. Zhou, W. Sun, S. Liang, and Z. Zhai PCBP2 mediates degradation of the adaptor MAVS via the HECT ubiquitin ligase AIP4 Nat Immunol 10 2009 1300 1308
77. A.V. Makeyev, and S.A. Liebhaber The poly(C)-binding proteins: a multiplicity of functions and a search for mechanisms RNA 8 2002 265 278
78. H. Leffers, K. Dejgaard, and J.E. Celis Characterisation of two major cellular poly(rC)-binding human proteins, each containing three K-homologous (KH) domains Eur J Biochem 230 1995 447 453
79. M. Kiledjian, X. Wang, and S.A. Liebhaber Identification of two KH domain proteins in the alpha-globin mRNP stability complex EMBO J 14 1995 4357 4364
80. X. Zhou, F. You, H. Chen, and Z. Jiang Poly(C)-binding protein 1 (PCBP1) mediates housekeeping degradation of mitochondrial antiviral signaling (MAVS) Cell Res 22 2012 717 727
81. C. Castanier, N. Zemirli, A. Portier, D. Garcin, N. Bidere, and A. Vazquez MAVS ubiquitination by the E3 ligase TRIM25 and degradation by the proteasome is involved in type I interferon production after activation of the antiviral RIG-I-like receptors BMC Biol 10 2012 44
82. M.U. Gack, Y.C. Shin, C.H. Joo, T. Urano, C. Liang, and L. Sun TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity Nature 446 2007 916 920
83. Y. Wang, X. Tong, and X. Ye Ndfip1 negatively regulates RIG-I-dependent immune signaling by enhancing E3 ligase Smurf1-mediated MAVS degradation J Immunol 189 2012 5304 5313
84. T. Mund, and H.R. Pelham Control of the activity of WW-HECT domain E3 ubiquitin ligases by NDFIP proteins EMBO Rep 10 2009 501 507
85. T. Mund, and H.R. Pelham Regulation of PTEN/Akt and MAP kinase signaling pathways by the ubiquitin ligase activators Ndfip1 and Ndfip2 Proc Natl Acad Sci USA 107 2010 11429 11434
86. Y. Wang, X. Tong, E.S. Omoregie, W. Liu, S. Meng, and X. Ye Tetraspanin 6 (TSPAN6) negatively regulates retinoic acid-inducible gene I-like receptor-mediated immune signaling in a ubiquitination-dependent manner J Biol Chem 287 2012 34626 34634
87. M.E. Hemler Tetraspanin functions and associated microdomains Nat Rev Mol Cell Biol 6 2005 801 811
88. D. Vitour, S. Dabo, M. Ahmadi Pour, M. Vilasco, P.O. Vidalain, and Y. Jacob Polo-like kinase 1 (PLK1) regulates interferon (IFN) induction by MAVS J Biol Chem 284 2009 21797 21809
89. K.Y. Cheng, E.D. Lowe, J. Sinclair, E.A. Nigg, and L.N. Johnson The crystal structure of the human polo-like kinase-1 polo box domain and its phospho-peptide complex EMBO J 22 2003 5757 5768
90. A.E. Elia, P. Rellos, L.F. Haire, J.W. Chao, F.J. Ivins, and K. Hoepker The molecular basis for phosphodependent substrate targeting and regulation of Plks by the Polo-box domain Cell 115 2003 83 95
91. B. Garcia-Alvarez, G. de Carcer, S. Ibanez, E. Bragado-Nilsson, and G. Montoya Molecular and structural basis of polo-like kinase 1 substrate recognition: implications in centrosomal localization Proc Natl Acad Sci USA 104 2007 3107 3112
92. S. Paz, M. Vilasco, S.J. Werden, M. Arguello, D. Joseph-Pillai, and T. Zhao A functional C-terminal TRAF3-binding site in MAVS participates in positive and negative regulation of the IFN antiviral response Cell Res 21 2011 895 910
93. T. Song, C. Wei, Z. Zheng, Y. Xu, X. Cheng, and Y. Yuan c-Abl tyrosine kinase interacts with MAVS and regulates innate immune response FEBS Lett 584 2010 33 38
94. A.M. Pendergast The Abl family kinases: mechanisms of regulation and signaling Adv Cancer Res 85 2002 51 100
95. C. Wen, Z. Yan, X. Yang, K. Guan, C. Xu, and T. Song Identification of tyrosine-9 of MAVS as critical target for inducible phosphorylation that determines activation PLoS One 7 2012 e41687