Mitochondria-nucleus shuttling FK506-binding protein 51 interacts with TRAF proteins and facilitates the RIG-I-like receptor-mediated expression of type I IFN

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Akiyama, Taishin ^a   Shiraishi, Takuma ^a   Qin, Junwen ^a,b   Konno, Hiroyasu ^a   Akiyama, Nobuko ^a   Shinzawa, Miho ^a   Miyauchi, Maki ^a   Takizawa, Nobukazu ^a   Yanai, Hiromi ^a   Ohashi, Hiroyuki ^a   Miyamoto Sato, Etsuko ^a   Yanagawa, Hiroshi ^c   Yong, Weidong ^d   Shou, Weinian ^d   Inoue, Jun Ichiro ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b JINAN UNIVERSITY   (China)

^c KEIO UNIVERSITY   (Japan)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; FK 506 BINDING PROTEIN; INTERFERON; PROTEIN BCL 6; RETINOIC ACID INDUCIBLE PROTEIN I; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; PROTEIN BINDING; TACROLIMUS BINDING PROTEIN 5; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INNATE IMMUNITY; MITOCHONDRION; MOUSE; NEWCASTLE DISEASE PARAMYXOVIRUS; NONHUMAN; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION; VIRUS INFECTION; ANIMAL; CELL LINE; CELL NUCLEUS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; NEWCASTLE DISEASE VIRUS; PROTEIN ANALYSIS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CELL NUCLEUS; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; INTERFERON TYPE I; MICE; MITOCHONDRIA; NEWCASTLE DISEASE VIRUS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN INTERACTION MAPS; PROTEIN TRANSPORT; RNA, DOUBLE-STRANDED; SIGNAL TRANSDUCTION; TACROLIMUS BINDING PROTEINS; TNF RECEPTOR-ASSOCIATED FACTOR 3; TNF RECEPTOR-ASSOCIATED FACTOR 6; TUMOR NECROSIS FACTOR RECEPTOR-ASSOCIATED PEPTIDES AND PROTEINS;

EID: 84900404337     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095992     Document Type: Article

References (47)

1. Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140: 805-820.
2. Barbalat R, Ewald SE, Mouchess ML, Barton GM (2011) Nucleic acid recognition by the innate immune system. Annu Rev Immunol 29: 185-214.
3. Kato H, Takahasi K, Fujita T (2011) RIG-I-like receptors: cytoplasmic sensors for non-self RNA. Immunol Rev 243: 91-98.
4. Loo YM, Gale M (2011) Immune signaling by RIG-I-like receptors. Immunity 34: 680-692.
5. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, et al. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5: 730-737. (Pubitemid 39023305)
6. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, et al. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105.
7. Gitlin L, Barchet W, Gilfillan S, Cella M, Beutler B, et al. (2006) Essential role of mda-5 in type I IFN responses to polyriboinosinic: polyribocytidylic acid and encephalomyocarditis picornavirus. Proc Natl Acad Sci U S A 103: 8459-8464. (Pubitemid 43838477)
8. Satoh T, Kato H, Kumagai Y, Yoneyama M, Sato S, et al. (2010) LGP2 is a positive regulator of RIG-I- and MDA5-mediated antiviral responses. Proc Natl Acad Sci U S A 107: 1512-1517.
9. Seth RB, Sun L, Ea CK, Chen ZJ (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122: 669-682. (Pubitemid 41242633)
10. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, et al. (2005) Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437: 1167-1172. (Pubitemid 41509355)
11. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, et al. (2005) IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 6: 981-988. (Pubitemid 41486182)
12. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, et al. (2005) VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol Cell 19: 727-740. (Pubitemid 41316668)
13. Ramos HJ, Gale M (2011) RIG-I like receptors and their signaling crosstalk in the regulation of antiviral immunity. Curr Opin Virol 1: 167-176.
14. Belgnaoui SM, Paz S, Hiscott J (2011) Orchestrating the interferon antiviral response through the mitochondrial antiviral signaling (MAVS) adapter. Curr Opin Immunol 23: 564-572.
15. Dixit E, Boulant S, Zhang Y, Lee AS, Odendall C, et al. (2010) Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141: 668-681.
16. Oeckinghaus A, Hayden MS, Ghosh S (2011) Crosstalk in NF-κB signaling pathways. Nat Immunol 12: 695-708.
17. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, et al. (2003) IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4: 491-496. (Pubitemid 36592443)
18. Hemmi H, Takeuchi O, Sato S, Yamamoto M, Kaisho T, et al. (2004) The roles of two IkappaB kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J Exp Med 199: 1641-1650. (Pubitemid 38821997)
19. Honda K, Takaoka A, Taniguchi T (2006) Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 25: 349-360. (Pubitemid 44354220)
20. Oganesyan G, Saha SK, Guo B, He JQ, Shahangian A, et al. (2006) Critical role of TRAF3 in the Toll-like receptor-dependent and -independent antiviral response. Nature 439: 208-211. (Pubitemid 43083142)
21. Saha SK, Pietras EM, He JQ, Kang JR, Liu SY, et al. (2006) Regulation of antiviral responses by a direct and specific interaction between TRAF3 and Cardif. EMBO J 25: 3257-3263. (Pubitemid 44141784)
22. Konno H, Yamamoto T, Yamazaki K, Gohda J, Akiyama T, et al. (2009) TRAF6 establishes innate immune responses by activating NF-kappaB and IRF7 upon sensing cytosolic viral RNA and DNA. PLoS One 4: e5674.
23. Yoshida R, Takaesu G, Yoshida H, Okamoto F, Yoshioka T, et al. (2008) TRAF6 and MEKK1 play a pivotal role in the RIG-I-like helicase antiviral pathway. J Biol Chem 283: 36211-36220.
24. Mikkelsen SS, Jensen SB, Chiliveru S, Melchjorsen J, Julkunen I, et al. (2009) RIG-I-mediated activation of p38 MAPK is essential for viral induction of interferon and activation of dendritic cells: dependence on TRAF2 and TAK1. J Biol Chem 284: 10774-10782.
25. Tang ED, Wang CY (2010) TRAF5 is a downstream target of MAVS in antiviral innate immune signaling. PLoS One 5: e9172.
26. Paz S, Vilasco M, Werden SJ, Arguello M, Joseph-Pillai D, et al. (2011) A functional C-terminal TRAF3-binding site in MAVS participates in positive and negative regulation of the IFN antiviral response. Cell Res 21: 895-910.
27. Kang CB, Hong Y, Dhe-Paganon S, Yoon HS (2008) FKBP family proteins: immunophilins with versatile biological functions. Neurosignals 16: 318-325.
28. Romano S, Sorrentino A, Di Pace AL, Nappo G, Mercogliano C, et al. (2011) The emerging role of large immunophilin FK506 binding protein 51 in cancer. Curr Med Chem 18: 5424-5429.
29. Wang L (2011) FKBP51 regulation of AKT/protein kinase B phosphorylation. Curr Opin Pharmacol 11: 360-364.
30. Galigniana NM, Ballmer LT, Toneatto J, Erlejman AG, Lagadari M, et al. (2012) Regulation of the glucocorticoid response to stress-related disorders by the Hsp90-binding immunophilin FKBP51. J Neurochem 122: 4-18.
31. Gallo LI, Lagadari M, Piwien-Pilipuk G, Galigniana MD (2011) The 90-kDa heat-shock protein (Hsp90)-binding immunophilin FKBP51 is a mitochondrial protein that translocates to the nucleus to protect cells against oxidative stress. J Biol Chem 286: 30152-30160.
32. Bouwmeester T, Bauch A, Ruffner H, Angrand PO, Bergamini G, et al. (2004) A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat Cell Biol 6: 97-105. (Pubitemid 38425708)
33. Romano S, D'Angelillo A, Pacelli R, Staibano S, De Luna E, et al. (2010) Role of FK506-binding protein 51 in the control of apoptosis of irradiated melanoma cells. Cell Death Differ 17: 145-157.
34. Yong W, Yang Z, Periyasamy S, Chen H, Yucel S, et al. (2007) Essential role for Co-chaperone Fkbp52 but not Fkbp51 in androgen receptor-mediated signaling and physiology. J Biol Chem 282: 5026-5036. (Pubitemid 47100995)
35. Miyamoto-Sato E, Takashima H, Fuse S, Sue K, Ishizaka M, et al. (2003) Highly stable and efficient mRNA templates for mRNA-protein fusions and C-terminally labeled proteins. Nucleic Acids Res 31: e78.
36. Miyamoto-Sato E, Ishizaka M, Horisawa K, Tateyama S, Takashima H, et al. (2005) Cell-free cotranslation and selection using in vitro virus for high-throughput analysis of protein-protein interactions and complexes. Genome Res 15: 710-717. (Pubitemid 41043641)
37. Miyamoto-Sato E, Fujimori S, Ishizaka M, Hirai N, Masuoka K, et al. (2010) A comprehensive resource of interacting protein regions for refining human transcription factor networks. PLoS One 5: e9289.
38. Lienenklaus S, Cornitescu M, Zietara N, Łyszkiewicz M, Gekara N, et al. (2009) Novel reporter mouse reveals constitutive and inflammatory expression of IFN-beta in vivo. J Immunol 183: 3229-3236.
39. Yang K, Shi H, Qi R, Sun S, Tang Y, et al. (2006) Hsp90 regulates activation of interferon regulatory factor 3 and TBK-1 stabilization in Sendai virus-infected cells. Mol Biol Cell 17: 1461-1471. (Pubitemid 43376563)
40. Ye H, Arron JR, Lamothe B, Cirilli M, Kobayashi T, et al. (2002) Distinct molecular mechanism for initiating TRAF6 signalling. Nature 418: 443-447. (Pubitemid 34826847)
41. Ye H, Park YC, Kreishman M, Kieff E, Wu H (1999) The structural basis for the recognition of diverse receptor sequences by TRAF2. Mol Cell 4: 321-330. (Pubitemid 29499785)
42. Inoue J, Gohda J, Akiyama T (2007) Characteristics and biological functions of TRAF6. Adv Exp Med Biol 597: 72-79.
43. Yamazaki K, Gohda J, Kanayama A, Miyamoto Y, Sakurai H, et al. (2009) Two mechanistically and temporally distinct NF-kappaB activation pathways in IL-1 signaling. Sci Signal 2: ra66.
44. Häcker H, Tseng PH, Karin M (2011) Expanding TRAF function: TRAF3 as a tri-faced immune regulator. Nat Rev Immunol 11: 457-468.
45. West AP, Shadel GS, Ghosh S (2011) Mitochondria in innate immune responses. Nat Rev Immunol 11: 389-402.
46. Burack WR, Shaw AS (2000) Signal transduction: hanging on a scaffold. Curr Opin Cell Biol 12: 211-216. (Pubitemid 30142568)
47. Ferrell JE (2000) What do scaffold proteins really do? Sci STKE 2000: pe1.