MAVS protein and its interactions with hepatitis A, B and C viruses
Zbigniew Wyżewski 1 , Karolina P. Gregorczyk 1 , Justyna Struzik 1 , Marek Niemiałtowski 1 , Lidia Szulc-Dąbrowska 1Abstract
Mitochondrial antiviral signaling protein (MAVS) transmits activation signal of type I interferon (IFN) gene transcription in the molecular intracellular pathway, which depends on the protein encoded by retinoic acid inducible gene I (RIG-I) or melanoma differentiation-associated protein-5 (MDA-5). MAVS, as a signal molecule, performs an essential function in the development of an antiviral immune response. The molecule of MAVS consists of two domains: the N-terminal domain and the C-terminal domain. The N-terminal end of MAVS contains the caspase activation and recruitment domain (CARD). CARD is responsible for MAVS interaction with RIG-I and MDA-5, which act as cytosolic sensors detecting foreign viral genetic material in the host cell. After binding to viral RNA, RIG-I or MDA-5 activates MAVS and transmits the signal of IFN type I gene expression. The C-terminal transmembrane domain (TM) of MAVS anchors the protein to the outer mitochondrial membrane. In this paper interactions between MAVS and hepatitis virus type A (HAV), type B (HBV) and type C (HCV) are presented. Mechanisms of indirect activation of MAVS by viral DNA and RNA, as well as the strategies of HAV, HBV andHCV for blocking of the intracellular signaling pathway at the level of MAVS, are described.
References
- 1. Ablasser A., Bauernfeind F., Hartmann G., Latz E., Fitzgerald K.A.,Hornung V.: RIG-I-dependent sensing of poly(dA:dT) through theinduction of an RNA polymerase III-transcribed RNA intermediate.Nat. Immunol., 2009; 10: 1065-1072
Google Scholar - 2. Adrain C., Martin S.J.: The mitochondrial apoptosome: a killerunleashed by the cytochrome seas. Trends Biochem. Sci., 2001; 26:390-397
Google Scholar - 3. Aragonès L., Bosch A., Pintó R.M.: Hepatitis A virus mutant spectraunder the selective pressure of monoclonal antibodies: codon usageconstraints limit capsid variability. J. Virol., 2008; 82: 1688-1700
Google Scholar - 4. Arai M., Suzuki H., Tobita Y., Takagi A., Okamoto K., Ohta A.,Sudoh M., Kohara M.: Establishment of infectious HCV virion-producingcells with newly designed full-genome replicon RNA. Arch.Virol., 2011; 156: 295-304
Google Scholar - 5. Arnaud N., Dabo S., Maillard P., Budkowska A., Kalliampakou K.I.,Mavromara P., Garcin D., Hugon J., Gatignol A., Akazawa D., Wakita T.,Meurs E.F.: Hepatitis C virus controls interferon production throughPKR activation. PLoS One, 2010; 5: e10575
Google Scholar - 6. Baum A., García-Sastre A.: Differential recognition of viral RNAby RIG-I. Virulence, 2011; 2: 166-169
Google Scholar - 7. Bergstroem B., Johnsen I.B., Nguyen T.T., Hagen L., SlupphaugG., Thommesen L., Anthonsen M.W.: Identification of a novel in vivovirus-targeted phosphorylation site in interferon regulatory factor- 3 (IRF3). J. Biol. Chem., 2010; 285: 24904-24914
Google Scholar - 8. Bouchard M.J., Schneider R.J.: The enigmatic X gene of hepatitisB virus. J. Virol., 2004; 78: 12725-12734
Google Scholar - 9. Bouchier-Hayes L., Martin S.J..: CARD games in apoptosis and immunity.EMBO Rep., 2002; 3: 616-621
Google Scholar - 10. Broquet A.H., Hirata Y., McAllister C.S., Kagnoff M.F.: RIG-I/MDA5/MAVS are required to signal a protective IFN response inrotavirus-infected intestinal epithelium. J. Immunol., 2011; 186:1618-1626
Google Scholar - 11. Brundage S.C., Fitzpatrick A.N.: Hepatitis A. Am. Fam. Physician,2006; 73: 2162-2168
Google Scholar - 12. Bruss V.: Envelopment of the hepatitis B virus nucleocapsid.Virus Res., 2004; 106: 199-209
Google Scholar - 13. Cheng G., Zhong J., Chung J., Chisari F.V.: Double-stranded DNAand double-stranded RNA induce a common antiviral signaling pathwayin human cells. Proc. Natl. Acad. Sci. USA, 2007; 104: 9035-9040
Google Scholar - 14. Chiu Y.H., Macmillan J.B., Chen Z.J.: RNA polymerase III detectscytosolic DNA and induces type I interferons through the RIG-I pathway.Cell, 2009; 138: 576-591
Google Scholar - 15. Costa-Mattioli M., Di Napoli A., Ferre V., Billaudel S., Perez-Bercoff R., Cristina J.: Genetic variability of hepatitis A virus. J. Gen.Virol., 2003; 84: 3191-3201
Google Scholar - 16. De Francesco R., Steinkuhler C.: Structure and function of thehepatitis C virus NS3-NS4A serine proteinase. Curr. Top. Microbiol.Immunol., 2000; 242: 149-169
Google Scholar - 17. Ding Y., Sheng Q., Ma L., Dou X.: Chronic HBV infection amongpregnant women and their infants in Shenyang, China. Virol. J.,2013; 10: 17
Google Scholar - 18. Dixit E., Boulant S., Zhang Y., Lee A.S., Odendall C., Shum B.,Hacohen N., Chen Z.J., Whelan S.P., Fransen M., Nibert M.L., Superti-Furga G., Kagan J.C.: Peroxisomes are signaling platforms for antiviralinnate immunity. Cell, 2010; 141: 668-681
Google Scholar - 19. Drahos J., Racaniello V.R.: Cleavage of IPS-1 in cells infected withhuman rhinovirus. J. Virol., 2009; 83: 11581-11587
Google Scholar - 20. Faul E.J., Wanjalla C.N., Suthar M.S., Gale M., Wirblich C., SchnellM.J.: Rabies virus infection induces type I interferon production inan IPS-1 dependent manner while dendritic cell activation relies onIFNAR signaling. PLoS Pathog., 2010; 6: e1001016
Google Scholar - 21. Feng M., Ding Z., Xu L., Kong L., Wang W., Jiao S., Shi Z., GreeneM.I., Cong Y., Zhou Z.: Structural and biochemical studies of RIGIantiviral signaling. Protein Cell, 2013; 4: 142-154
Google Scholar - 22. Feng Q., Hato S.V., Langereis M.A., Zoll J., Virgen-Slane R., PeisleyA., Hur S., Semler B.L., van Rij R.P., van Kuppeveld F.J.: MDA5 detectsthe double-stranded RNA replicative form in picornavirus-infectedcells. Cell Rep., 2012; 2: 1187-1196
Google Scholar - 23. Figlerowicz M., Formanowicz P., Kędziora P., Alejska M., JackowiakP., Błażewicz J., Służewski W., Figlerowicz M.: Znaczenie klinicznezmian w populacji HCV w pierwszych tygodniach leczeniaprzewlekłego zapalenia wątroby typu C interferonem i rybawiryną.Przegl. Epidemiol., 2005; 59: 581-590
Google Scholar - 24. Franco E., Meleleo C., Serino L., Sorbara D., Zaratti L.: HepatitisA: epidemiology and prevention in developing countries. World J.Hepatol., 2012; 4: 68-73
Google Scholar - 25. Friedrich-Rust M., Zeuzem S., Sarrazin C.: Current therapy forhepatitis C. Int. J. Colorectal Dis., 2007; 22: 341-349
Google Scholar - 26. Gao W., Hu J.: Formation of hepatitis B virus covalently closedcircular DNA: removal of genome-linked protein. J. Virol., 2007; 81:6164-6174
Google Scholar - 27. Gitlin L., Barchet W., Gilfillan S., Cella M., Beutler B., FlavellR.A., Diamond M.S., Colonna M.: Essential role of mda-5 in typeI IFN responses to polyriboinosinic: polyribocytidulic acid and encephalomyocarditispicornavirus. Proc. Natl. Acad. Sci. USA., 2006;103: 8459-8464
Google Scholar - 28. Hong G.S., Jung Y.K.: Caspase recruitment domain (CARD) asa bi-functional switch of caspase regulation and NF-κB signals. J.Biochem. Mol. Biol., 2002; 35: 19-23
Google Scholar - 29. Hornung V., Ellegast J., Kim S., Brzózka K., Jung A., Kato H., PoeckH., Akira S., Conzelmann K.K., Schlee M., Endres S., Hartmann G.:5’-Triphosphate RNA is the ligand for RIG-I. Science, 2006; 314: 994-997
Google Scholar - 30. Hou F., Sun L., Zheng H., Skaug B., Jiang Q.X., Chen Z.J.: MAVSforms functional prion-like aggregates to activate and propagateantiviral innate immune response. Cell, 2011; 146: 448-461
Google Scholar - 31. Imran M., Waheed Y., Manzoor S., Bilal M., Ashraf W., Ali M.,Ashraf M.: Interaction of hepatitis C virus proteins with patternrecognition receptors. Virol. J., 2012; 9: 126
Google Scholar - 32. Jabłońska A., Paradowska E.: Rola receptorów RIG-I-podobnychw odpowiedzi przeciwwirusowej. Postępy Hig. Med. Dośw., 2014;68: 541-556
Google Scholar - 33. Johnson C.L., Owen D.M., Gale M.Jr.: Functional and therapeuticanalysis of hepatitis C virus NS3.4A protease control of antiviral immunedefense. J. Biol. Chem., 2007; 282: 10792-10803
Google Scholar - 34. Karoney M.J., Siika A.M.: Hepatitis C virus (HCV) infection inAfrica: a review. Pan Afr. Med. J., 2013; 14: 44
Google Scholar - 35. Kato H., Takahasi K., Fujita T.: RIG-I-like receptors: cytoplasmicsensors for non-self RNA. Immunol. Rev., 2011; 243: 91-98
Google Scholar - 36. Kato H., Takeuchi O., Mikamo-Satoh E., Hirai R., Kawai T., MatsushitaK., Hiiragi A., Dermody T.S., Fujita T., Akira S.: Length-dependentrecognition of double-stranded ribonucleic acids by retinoicacid-inducible gene-I and melanoma differentiation-associated gene 5 J. Exp. Med., 2008; 205: 1601-1610
Google Scholar - 37. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., MatsuiK., Uematsu S., Jung A., Kawai T., Ishii K.J., Yamaguchi O., OtsuK., Tsujimura T., Koh C.S., Reis e Sousa C. i wsp.: Differential rolesof MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature,2006; 441: 101-105
Google Scholar - 38. Kawai T., Takahashi K., Sato S., Coban C., Kumar H., Kato H.,Ishii K.J., Takeuchi O., Akira S.: IPS-1, an adaptor triggering RIGI-and Mda5-mediated type I interferon induction. Nat. Immunol.,2005; 6: 981-988
Google Scholar - 39. Kfutwah A.K., Tejiokem M.C., Njouom R.: A low proportion ofHBeAg among HBsAg-positive pregnant women with known HIVstatus could suggest low perinatal transmission of HBV in Cameroon.Virol. J., 2012; 9: 62
Google Scholar - 40. Koch A., Yoon Y., Bonekamp N.A., McNiven M.A., Schrader M.:A role for Fis1 in both mitochondrial and peroxisomal fission inmammalian cells. Mol. Biol. Cell, 2005; 16: 5077-5086
Google Scholar - 41. Koshiba T., Bashiruddin N., Kawabata S.: Mitochondria and antiviralinnate immunity. Int. J. Biochem. Mol. Biol., 2011; 2: 257-262
Google Scholar - 42. Kumar H., Kawai T., Kato H., Sato S., Takahashi K., Caban C.,Yamamoto M., Uematsu S., Ishii K.J., Takeuchi O., Akira S.: Essentialrole of IPS-1 in innate immune responses against RNA viruses. J.Exp. Med., 2006; 203: 1795-1803
Google Scholar - 43. Kumar M., Jung S.Y., Hodgson A.J., Madden C.R., Qin J., SlagleB.L.: Hepatitis B virus regulatory HBx protein binds to adaptor proteinIPS-1 and inhibits the activation of beta interferon. J. Virol.,2011; 85: 987-995
Google Scholar - 44. Li X.D., Sun L., Seth R.B., Pineda G., Chen Z.J.: Hepatitis C virusprotease NS3/4A cleaves mitochondrial antiviral signaling proteinoff the mitochondria to evade innate immunity. Proc. Natl. Acad.Sci. USA, 2005; 102: 17717-17722
Google Scholar - 45. Li Y., Xie J., Wu S., Xia J., Zhang P., Liu C., Zhang P., Huang X.:Protein kinase regulated by dsRNA downregulates the interferonproduction in dengue virus- and dsRNA-stimulated human lungepithelial cells. PLoS One, 2013; 8: e55108
Google Scholar - 46. Loo Y.M., Owen D.M., Li K., Erickson A.K., Johnson C.L., FishP.M., Carney D.S., Wang T., Ishida H., Yoneyama M., Fujita T., SaitoT., Lee W.M., Hagedorn C.H., Lau D.T., Weinman S.A., Lemon S.M.,Gale M.Jr.: Viral and therapeutic control of IFN-β promoter stimulator 1 during hepatitis C virus infection. Proc. Natl. Acad. Sci. USA,2006; 103: 6001-6006
Google Scholar - 47. Lugoboni F., Pajusco B., Albiero A., Quaglio G.: Hepatitis A virusamong drug users and the role of vaccination: a review. Front.Psychiatry, 2011; 2: 79
Google Scholar - 48. Malmgaard L.: Induction and regulation of IFNs during viralinfections. J. Interferon Cytokine Res., 2004; 24: 439-454
Google Scholar - 49. McWhirter S.M., Tenoever B.R., Maniatis T.: Connecting mitochondriaand innate immunity. Cell, 2005; 122: 645-647
Google Scholar - 50. Michailidis E., Kirby K.A., Hachiya A., Yoo W., Hong S.P., Kim S.O.,Folk W.R., Sarafianos S.G.: Antiviral therapies: focus on Hepatitis Breverse transcriptase. Int. J. Biochem. Cell Biol., 2012; 44: 1060-1071
Google Scholar - 51. Moradpour D., Penin F.: Hepatitis C virus proteins: from structureto function. Curr. Top. Microbiol. Immunol., 2013; 369: 113-142
Google Scholar - 52. Mottola G., Cardinali G., Ceccacci A., Trozzi C., Bartholomew L.,Torrisi M.R., Pedrazzini E., Bonatti S., Migliaccio G.: Hepatitis C virusnonstructural proteins are localized in a modified endoplasmicreticulum of cells expressing viral subgenomic replicons. Virology,2002; 293: 31-43
Google Scholar - 53. Mukherjee A., Morosky S.A., Delorme-Axford E., Dybdahl-SissokoN., Oberste M.S., Wang T., Coyne C.B.: The coxsackievirus B 3Cpro proteasecleaves MAVS and TRIF to attenuate host type I interferon andapoptotic signaling. PLoS Pathog., 2011; 7: e1001311
Google Scholar - 54. Onoguchi K., Onomoto K., Takamatsu S., Jogi M., Takemura A.,Morimoto S., Julkunen I., Namiki H., Yoneyama M., Fujita T.: Virusinfectionor 5’ppp-RNA activates antiviral signal through redistributionof IPS-1 mediated by MFN1. PLoS Pathog., 2010; 6: e1001012
Google Scholar - 55. Pairan A., Bruss V.: Functional surfaces of the hepatitis B viruscapsid. J. Virol., 2009; 83: 11616-11623
Google Scholar - 56. Papadakis M.A., Elefsiniotis I.S., Vlahos G., Daskalakis G., BarbatisC., Antsaklis A.: Intrauterine-transplacental transmission of hepatitisB virus (HBV) from hepatitis B e antigen negative (precore mutant,G1896A) chronic HBV infected mothers to their infants. Preliminaryresults of a prospective study. J. Clin. Virol., 2007; 38: 181-183
Google Scholar - 57. Paulmann D., Magulski T., Schwarz R., Heitmann L., Flehmig B.,Vallbracht A., Dotzauer A.: Hepatitis A virus protein 2B suppressesbeta interferon (IFN) gene transcription by interfering with IFNregulatory factor 3 activation. J. Gen. Virol., 2008; 89: 1593-1604
Google Scholar - 58. Pichlmair A., Schulz O., Tan C.P., Naslund T.I., Liljestrom P., WeberF., Reis e Sousa C.: RIG-I-mediated antiviral responses to singlestrandedRNA bearing 5’-phosphates. Science, 2006; 314: 997-1001
Google Scholar - 59. Plauzolles A., Lucas M., Gaudieri S.: Hepatitis C virus adaptationto T-cell immune pressure. ScientificWorldJournal, 2013; 2013:673240
Google Scholar - 60. Potter J.A., Randall R.E., Taylor G.L.: Crystal structure of humanIPS-1/MAVS/VISA/Cardif caspase activation recruitment domain.BMC Struct. Biol., 2008; 8: 11
Google Scholar - 61. Prusiner S.B.: Cell biology. A unifying role for prions in neurodegenerativediseases. Science, 2012; 336: 1511-1513
Google Scholar - 62. Ranjbar R., Davari A., Izadi M., Jonaidi N., Alavian S.M.: HIV/HBVco-infections: epidemiology, natural history, and treatment: a reviewarticle. Iran. Red Crescent Med. J., 2011; 13: 855-862
Google Scholar - 63. Rybicka M., Stalke P., Charmuszko U., Bielawski K.P.: Wpływpolimorfizmu wirusa zapalenia wątroby typu B na przebieg chorobyu osób przewlekle zakażonych. Postępy Hig. Med. Dośw., 2011;65: 244-254
Google Scholar - 64. Seth R.B., Sun L., Ea C.K., Chen Z.J.: Identification and characterizationof MAVS, a mitochondrial antiviral signaling protein thatactivates NF-κB and IRF3. Cell, 2005; 122: 669-682
Google Scholar - 65. Sharma S., Fitzgerald K.A.: Viral defense: it takes two MAVS totango. Cell, 2010; 141: 570-572
Google Scholar - 66. Saito T., Owen D.M., Jiang F., Marcotrigiano J., Gale M.Jr.: Innateimmunity induced by composition-dependent RIG-I recognition ofhepatitis C virus RNA. Nature, 2008; 454: 523-527
Google Scholar - 67. Solis M., Nakhaei P., Jalalirad M., Lacoste J., Douville R., ArguelloM., Zhao T., Laughrea M., Wainberg M.A., Hiscott J.: RIG-I-mediatedantiviral signaling is inhibited in HIV-1 infection by a protease-mediatedsequestration of RIG-I. J. Virol., 2011; 85: 1224-1236
Google Scholar - 68. Stabinski L., Reynolds S.J., Ocama P., Laeyendecker O., SerwaddaD., Gray R.H., Wawer M., Thomas D.L., Quinn T.C., Kirk G.D.: HepatitisB virus and sexual behavior in Rakai, Uganda. J. Med. Virol.,2011; 83: 796-800
Google Scholar - 69. Sumpter R.Jr., Loo Y.M., Foy E., Li K., Yoneyama M., Fujita T.,Lemon S.M., Gale M.Jr.: Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J. Virol., 2005; 79: 2689-2699
Google Scholar - 70. Suthar M.S., Ma D.Y., Thomas S., Lund J.M., Zhang N., Daffis S.,Rudensky A.Y., Bevan M.J., Clark E.A., Kaja M.K., Diamond M.S., GaleM.Jr.: IPS-1 is essential for the control of West Nile virus infectionand immunity. PLoS Pathog., 2010; 6: e1000757
Google Scholar - 71. Tam A.B., Mercado E.L., Hoffmann A., Niwa M.: ER stress activatesNF-κB by integrating functions of basal IKK activity, IRE1 andPERK. PLoS One, 2012; 7: e45078
Google Scholar - 72. Thomas S.L., Newell M.L., Peckham C.S., Ades A.E., Hall A.J.:A review of hepatitis C virus (HCV) vertical transmission: risks oftransmission to infants born to mothers with and without HCV viraemiaor human immunodeficiency virus infection. Int. J. Epidemiol.,1998; 27: 108-117
Google Scholar - 73. Tuite M.F., Serio T.R.: The prion hypothesis: from biologicalanomaly to basic regulatory mechanism. Nat. Rev. Mol. Cell Biol.,2010; 11: 823-833
Google Scholar - 74. van Regenmortel M.H., Mayo M.A., Fauquet C.M., Maniloff J.:Virus nomenclature: consensus versus chaos. Arch. Virol., 2000;145: 2227-2232
Google Scholar - 75. Wang L., Li S., Dorf M.E.: NEMO binds ubiquitinated TANK-bindingkinase 1 (TBK1) to regulate innate immune responses to RNAviruses. PLoS One, 2012; 7: e43756
Google Scholar - 76. Weasley A., Fiore A., Bell B.P.: Hepatitis A in the era of vaccination.Epidemiol. Rev., 2006; 28: 101-111
Google Scholar - 77. Webster D.P., Klenerman P., Dusheiko G.M.: Hepatitis C. Lancet,2015; 385: 1124-1135
Google Scholar - 78. Wei C., Ni C., Song T., Liu Y., Yang X., Zheng Z., Jia Y., Yuan Y.,Guan K., Xu Y., Cheng X., Zhang Y., Yang X., Wang Y., Wen C., WuQ., Shi W., Zhong H.: The hepatitis B virus X protein disrupts innateimmunity by downregulating mitochondrial antiviral signaling protein.J. Immunol., 2010; 185: 1158-1168
Google Scholar - 79. Wheeler C., Vogt T.M., Armstrong G.L., Vaughan G., Weltman A.,Nainan O.V., Dato V., Xia G., Waller K., Amon J., Lee T.M., Highbaugh-Battle A., Hembree C., Evenson S., Ruta M.A., Williams I.T., Fiore A.E.,Bell B.P.: An outbreak of hepatitis A associated with green onions.N. Engl. J. Med., 2005; 353: 890-897
Google Scholar - 80. Wilkins T., Malcolm J.K., Raina D., Schade R.R.: Hepatitis C: Diagnosisand treatment. Am. Fam. Physician, 2010; 81: 1351-1357
Google Scholar - 81. Yang Y., Liang Y., Qu L., Chen Z., Yi M., Li K., Lemon S.M.: Disruptionof innate immunity due to mitochondrial targeting of a picornaviralprotease precursor. Proc. Natl. Acad. Sci. USA, 2007; 104:7253-7258
Google Scholar - 82. Yoneyama M., Fujita T.: RNA recognition and signal transductionby RIG-I-like receptors. Immunol. Rev., 2009; 227: 54-65
Google Scholar - 83. Yoneyama M., Kikuchi M., Natsukawa T., Schinobu N., ImaizumiT., Miyagishi M., Taira K., Akira S., Fijita T.: The RNA helicase RIGIhas an essential function in double-stranded RNA-induced innateantiviral responses. Nat. Immunol., 2004; 5: 730-737
Google Scholar - 84. Zhang Q.M., Song W.Q., Li Y.J., Qian J., Zhai A.X., Wu J., Li A.M.,He J.M., Zhao J.Y., Yu X., Wei L.L., Zhang F.M.: Over-expression ofmitochondrial antiviral signaling protein inhibits coxsackievirusB3 infection by enhancing type-I interferons production. Virol. J.,2012; 9: 312
Google Scholar