Multifunctional roles of leader protein of foot-and-mouth disease viruses in suppressing host antiviral responses

Veterinary Research

Volumn 46, Issue 1, 2015, Pages

  Liu, Yingqi ^a,b   Zhu, Zixiang ^a   Zhang, Miaotao ^b   Zheng, Haixue ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b NORTHWEST A F UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LEADER PROTEINASE, FOOT-AND-MOUTH DISEASE VIRUS; PROTEINASE;

ANIMAL; ARTIODACTYLA; FOOT AND MOUTH DISEASE; FOOT AND MOUTH DISEASE VIRUS; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PHYSIOLOGY; VIROLOGY;

ANIMALS; ARTIODACTYLA; ENDOPEPTIDASES; FOOT-AND-MOUTH DISEASE; FOOT-AND-MOUTH DISEASE VIRUS; IMMUNITY, INNATE;

EID: 84945295942     PISSN: 09284249     EISSN: 12979716     Source Type: Journal    
DOI: 10.1186/s13567-015-0273-1     Document Type: Review

References (100)

1. Ding YZ, Chen HT, Zhang J, Zhou JH, Ma LN, Zhang L, Gu Y, Liu YS (2013) An overview of control strategy and diagnostic technology for foot-and-mouth disease in China. Virol J 10:78
2. Grubman MJ, Baxt B (2004) Foot-and-mouth disease. Clin Microbiol Rev 17:465-493
3. Conda-Sheridan M, Lee SS, Preslar AT, Stupp SI (2014) Esterase-activated release of naproxen from supramolecular nanofibres. Chem Commun (Camb) 50:13757-13760
4. Strebel K, Beck E (1986) A second protease of foot-and-mouth disease virus. J Virol 58:893-899
5. Du Y, Bi J, Liu J, Liu X, Wu X, Jiang P, Yoo D, Zhang Y, Wu J, Wan R, Zhao X, Guo L, Sun W, Cong X, Chen L, Wang J (2014) 3Cpro of foot-and-mouth disease virus antagonizes the interferon signaling pathway by blocking STAT1/STAT2 nuclear translocation. J Virol 88:4908-4920
6. Wang D, Fang L, Li K, Zhong H, Fan J, Ouyang C, Zhang H, Duan E, Luo R, Zhang Z, Liu X, Chen H, Xiao S (2012) Foot-and-mouth disease virus 3C protease cleaves NEMO to impair innate immune signaling. J Virol 86:9311-9322
7. Devaney MA, Vakharia VN, Lloyd RE, Ehrenfeld E, Grubman MJ (1988) Leader protein of foot-and-mouth disease virus is required for cleavage of the p220 component of the cap-binding protein complex. J Virol 62:4407-4409
8. de Los Santos T, Diaz-San Segundo F, Grubman MJ (2007) Degradation of nuclear factor kappa B during foot-and-mouth disease virus infection. J Virol 81:12803-12815
9. Belsham GJ, McInerney GM, Ross-Smith N (2000) Foot-and-mouth disease virus 3C protease induces cleavage of translation initiation factors eIF4A and eIF4G within infected cells. J Virol 74:272-280
10. de Los Santos T, de Avila Botton S, Weiblen R, Grubman MJ (2006) The leader proteinase of foot-and-mouth disease virus inhibits the induction of beta interferon mRNA and blocks the host innate immune response. J Virol 80:1906-1914
11. Rodriguez Pulido M, Serrano P, Saiz M, Martinez-Salas E (2007) Foot-and-mouth disease virus infection induces proteolytic cleavage of PTB, eIF3a, b, and PABP RNA-binding proteins. Virology 364:466-474
12. Esteban-Torres M, Landete JM, Reveron I, Santamaria L, de las Rivas B, Munoz R (2015) A Lactobacillus plantarum esterase active on a broad range of phenolic esters. Appl Environ Microbiol 81:3235-3242
13. Gu X, Kumar S, Kim E, Kim Y (2015) A whole genome screening and RNA interference identify a juvenile hormone esterase-like gene of the diamondback moth, Plutella xylostella. J Insect Physiol 80:81-87
14. Poyry TA, Jackson RJ (2011) Mechanisms governing the selection of translation initiation sites on foot-and-mouth disease virus RNA. J Virol 85:10178-10188
15. Piccone ME, Rieder E, Mason PW, Grubman MJ (1995) The foot-and-mouth disease virus leader proteinase gene is not required for viral replication. J Virol 69:5376-5382
16. Brown CC, Piccone ME, Mason PW, McKenna TS, Grubman MJ (1996) Pathogenesis of wild-type and leaderless foot-and-mouth disease virus in cattle. J Virol 70:5638-5641
17. Chinsangaram J, Mason PW, Grubman MJ (1998) Protection of swine by live and inactivated vaccines prepared from a leader proteinase-deficient serotype A12 foot-and-mouth disease virus. Vaccine 16:1516-1522
18. Chinsangaram J, Piccone ME, Grubman MJ (1999) Ability of foot-and-mouth disease virus to form plaques in cell culture is associated with suppression of alpha/beta interferon. J Virol 73:9891-9898
19. Belsham GJ (2013) Influence of the Leader protein coding region of foot-and-mouth disease virus on virus replication. J Gen Virol 94:1486-1495
20. Steinberger J, Skern T (2014) The leader proteinase of foot-and-mouth disease virus: structure-function relationships in a proteolytic virulence factor. Biol Chem 395:1179-1185
21. Gradi A, Foeger N, Strong R, Svitkin YV, Sonenberg N, Skern T, Belsham GJ (2004) Cleavage of eukaryotic translation initiation factor 4GII within foot-and-mouth disease virus-infected cells: identification of the L-protease cleavage site in vitro. J Virol 78:3271-3278
22. Wang D, Fang L, Li P, Sun L, Fan J, Zhang Q, Luo R, Liu X, Li K, Chen H, Chen Z, Xiao S (2011) The leader proteinase of foot-and-mouth disease virus negatively regulates the type I interferon pathway by acting as a viral deubiquitinase. J Virol 85:3758-3766
23. Wang D, Fang L, Liu L, Zhong H, Chen Q, Luo R, Liu X, Zhang Z, Chen H, Xiao S (2011) Foot-and-mouth disease virus (FMDV) leader proteinase negatively regulates the porcine interferon-lambda1 pathway. Mol Immunol 49:407-412
24. Gorbalenya AE, Koonin EV, Lai MM (1991) Putative papain-related thiol proteases of positive-strand RNA viruses. Identification of rubi- and aphthovirus proteases and delineation of a novel conserved domain associated with proteases of rubi-, alpha- and coronaviruses. FEBS Lett 288:201-205
25. Clarke BE, Sangar DV, Burroughs JN, Newton SE, Carroll AR, Rowlands DJ (1985) Two initiation sites for foot-and-mouth disease virus polyprotein in vivo. J Gen Virol 66:2615-2626
26. Piccone ME, Diaz-San Segundo F, Kramer E, Rodriguez LL, de los Santos T (2011) Introduction of tag epitopes in the inter-AUG region of foot and mouth disease virus: effect on the L protein. Virus Res 155:91-97
27. Medina M, Domingo E, Brangwyn JK, Belsham GJ (1993) The two species of the foot-and-mouth disease virus leader protein, expressed individually, exhibit the same activities. Virology 194:355-359
28. Glaser W, Cencic R, Skern T (2001) Foot-and-mouth disease virus leader proteinase: involvement of C-terminal residues in self-processing and cleavage of eIF4GI. J Biol Chem 276:35473-35481
29. Greve J, Bas M, Hoffmann TK, Schuler PJ, Weller P, Kojda G, Strassen U (2015) Effect of C1-Esterase-inhibitor in angiotensin-converting enzyme inhibitor-induced angioedema. Laryngoscope 125:E198-E202
30. Crowther M, Bauer KA, Kaplan AP (2014) The thrombogenicity of C1 esterase inhibitor (human): review of the evidence. Allergy Asthma Proc 35:444-453
31. Scozzafava A, Kalin P, Supuran CT, Gülçin I, Alwasel SH (2015) The impact of hydroquinone on acetylcholine esterase and certain human carbonic anhydrase isoenzymes (hCA I, II, IX, and XII). J Enzym Inhib Med Chem. doi: 10.3109/14756366.2014.999236
32. Poyry TA, Hentze MW, Jackson RJ (2001) Construction of regulatable picornavirus IRESes as a test of current models of the mechanism of internal translation initiation. RNA 7:647-660
33. Cao X, Bergmann IE, Fullkrug R, Beck E (1995) Functional analysis of the two alternative translation initiation sites of foot-and-mouth disease virus. J Virol 69:560-563
34. Guarne A, Hampoelz B, Glaser W, Carpena X, Tormo J, Fita I, Skern T (2000) Structural and biochemical features distinguish the foot-and-mouth disease virus leader proteinase from other papain-like enzymes. J Mol Biol 302:1227-1240
35. Cencic R, Mayer C, Juliano MA, Juliano L, Konrat R, Kontaxis G, Skern T (2007) Investigating the substrate specificity and oligomerisation of the leader protease of foot and mouth disease virus using NMR. J Mol Biol 373:1071-1087
36. Sangar DV, Clark RP, Carroll AR, Rowlands DJ, Clarke BE (1988) Modification of the leader protein (Lb) of foot-and-mouth disease virus. J Gen Virol 69:2327-2333
37. Steinberger J, Kontaxis G, Rancan C, Skern T (2013) Comparison of self-processing of foot-and-mouth disease virus leader proteinase and porcine reproductive and respiratory syndrome virus leader proteinase nsp1alpha. Virology 443:271-277
38. Steinberger J, Grishkovskaya I, Cencic R, Juliano L, Juliano MA, Skern T (2014) Foot-and-mouth disease virus leader proteinase: structural insights into the mechanism of intermolecular cleavage. Virology 468-470:397-408
39. de los Santos T, Diaz-San Segundo F, Zhu J, Koster M, Dias CC, Grubman MJ (2009) A conserved domain in the leader proteinase of foot-and-mouth disease virus is required for proper subcellular localization and function. J Virol 83:1800-1810
40. Kirchweger R, Ziegler E, Lamphear BJ, Waters D, Liebig HD, Sommergruber W, Sobrino F, Hohenadl C, Blaas D, Rhoads RE, Skern T (1994) Foot-and-mouth disease virus leader proteinase: purification of the Lb form and determination of its cleavage site on eIF-4 gamma. J Virol 68:5677-5684
41. Nieter A, Haase-Aschoff P, Kelle S, Linke D, Krings U, Popper L, Berger RG (2015) A chlorogenic acid esterase with a unique substrate specificity from Ustilago maydis. Appl Environ Microbiol 81:1679-1688
42. Guarne A, Tormo J, Kirchweger R, Pfistermueller D, Fita I, Skern T (1998) Structure of the foot-and-mouth disease virus leader protease: a papain-like fold adapted for self-processing and eIF4G recognition. EMBO J 17:7469-7479
43. Brocklehurst K, Philpott MP (2013) Cysteine proteases: mode of action and role in epidermal differentiation. Cell Tissue Res 351:237-244
44. Gingras AC, Raught B, Sonenberg N (1999) eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68:913-963
45. Sonenberg N, Hinnebusch AG (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136:731-745
46. Colvin OC, Kransdorf MJ, Roberts CC, Chivers FS, Lorans R, Beauchamp CP, Schwartz AJ (2015) Leukocyte esterase analysis in the diagnosis of joint infection: can we make a diagnosis using a simple urine dipstick? Skelet Radiol 44:673-677
47. Lamphear BJ, Kirchweger R, Skern T, Rhoads RE (1995) Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases. Implications for cap-dependent and cap-independent translational initiation. J Biol Chem 270:21975-21983
48. Kashima TG, Inagaki Y, Grammatopoulos G, Athanasou NA (2015) Use of chloroacetate esterase staining for the histological diagnosis of prosthetic joint infection. Virchows Arch 466:595-601
49. Torrelo G, Ribeiro de Souza FZ, Carrilho E, Hanefeld U (2015) Xylella fastidiosa esterase rather than hydroxynitrile lyase. Chembiochem 16:625-630
50. Pham H, Santucci S, Yang WH (2014) Successful use of daily intravenous infusion of C1 esterase inhibitor concentrate in the treatment of a hereditary angioedema patient with ascites, hypovolemic shock, sepsis, renal and respiratory failure. Allergy Asthma Clin Immunol 10:62
51. Yeom HJ, Jung CS, Kang J, Kim J, Lee JH, Kim DS, Kim HS, Park PS, Kang KS, Park IK (2015) Insecticidal and acetylcholine esterase inhibition activity of Asteraceae plant essential oils and their constituents against adults of the German cockroach (Blattella germanica). J Agric Food Chem 63:2241-2248
52. Sabharwal G, Craig T (2015) Recombinant human C1 esterase inhibitor for the treatment of hereditary angioedema due to C1 inhibitor deficiency (C1-INH-HAE). Expert Rev Clin Immunol 11:319-327
53. Belsham GJ (2009) Divergent picornavirus IRES elements. Virus Res 139:183-192
54. Pineiro D, Ramajo J, Bradrick SS, Martinez-Salas E (2012) Gemin5 proteolysis reveals a novel motif to identify L protease targets. Nucleic Acids Res 40:4942-4953
55. Pacheco A, Lopez de Quinto S, Ramajo J, Fernandez N, Martinez-Salas E (2009) A novel role for Gemin5 in mRNA translation. Nucleic Acids Res 37:582-590
56. Michaelson JS, Leder P (2003) RNAi reveals anti-apoptotic and transcriptionally repressive activities of DAXX. J Cell Sci 116:345-352
57. Jung MY, Lorenz L, Richter JD (2006) Translational control by neuroguidin, a eukaryotic initiation factor 4E and CPEB binding protein. Mol Cell Biol 26:4277-4287
58. Perera R, Daijogo S, Walter BL, Nguyen JH, Semler BL (2007) Cellular protein modification by poliovirus: the two faces of poly(rC)-binding protein. J Virol 81:8919-8932
59. Mukherjee A, Morosky SA, Delorme-Axford E, Dybdahl-Sissoko N, Oberste MS, Wang T, Coyne CB (2011) The coxsackievirus B 3C protease cleaves MAVS and TRIF to attenuate host type I interferon and apoptotic signaling. PLoS Pathog 7:e1001311
60. Almstead LL, Sarnow P (2007) Inhibition of U snRNP assembly by a virus-encoded proteinase. Genes Dev 21:1086-1097
61. Barral PM, Sarkar D, Fisher PB, Racaniello VR (2009) RIG-I is cleaved during picornavirus infection. Virology 391:171-176
62. Dougherty JD, White JP, Lloyd RE (2011) Poliovirus-mediated disruption of cytoplasmic processing bodies. J Virol 85:64-75
63. Honda K, Yanai H, Takaoka A, Taniguchi T (2005) Regulation of the type I IFN induction: a current view. Int Immunol 17:1367-1378
64. Grubman MJ, Moraes MP, Diaz-San Segundo F, Pena L, de los Santos T (2008) Evading the host immune response: how foot-and-mouth disease virus has become an effective pathogen. FEMS Immunol Med Microbiol 53:8-17
65. Stahl MC, Harris CK, Matto S, Bernstein JA (2014) Idiopathic nonhistaminergic angioedema successfully treated with ecallantide, icatibant, and C1 esterase inhibitor replacement. J Allergy Clin Immunol Pract 2:818-819
66. Goodbourn S, Didcock L, Randall RE (2000) Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J Gen Virol 81:2341-2364
67. Diaz-San Segundo F, Moraes MP, de Los Santos T, Dias CC, Grubman MJ (2010) Interferon-induced protection against foot-and-mouth disease virus infection correlates with enhanced tissue-specific innate immune cell infiltration and interferon-stimulated gene expression. J Virol 84:2063-2077
68. Andersen J, VanScoy S, Cheng TF, Gomez D, Reich NC (2008) IRF-3-dependent and augmented target genes during viral infection. Genes Immun 9:168-175
69. Taniguchi T, Takaoka A (2002) The interferon-alpha/beta system in antiviral responses: a multimodal machinery of gene regulation by the IRF family of transcription factors. Curr Opin Immunol 14:111-116
70. Ank N, West H, Bartholdy C, Eriksson K, Thomsen AR, Paludan SR (2006) Lambda interferon (IFN-lambda), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J Virol 80:4501-4509
71. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, Langer JA, Sheikh F, Dickensheets H, Donnelly RP (2003) IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 4:69-77
72. Zhu J, Weiss M, Grubman MJ, de los Santos T (2010) Differential gene expression in bovine cells infected with wild type and leaderless foot-and-mouth disease virus. Virology 404:32-40
73. Stenfeldt C, Heegaard PM, Stockmarr A, Tjornehoj K, Belsham GJ (2011) Analysis of the acute phase responses of serum amyloid a, haptoglobin and type 1 interferon in cattle experimentally infected with foot-and-mouth disease virus serotype O. Vet Res 42:66
74. Feng Q, Langereis MA, Lork M, Nguyen M, Hato SV, Lanke K, Emdad L, Bhoopathi P, Fisher PB, Lloyd RE, van Kuppeveld FJ (2014) Enterovirus 2Apro targets MDA5 and MAVS in infected cells. J Virol 88:3369-3378
75. Zoll J, Melchers WJ, Galama JM, van Kuppeveld FJ (2002) The mengovirus leader protein suppresses alpha/beta interferon production by inhibition of the iron/ferritin-mediated activation of NF-kappa B. J Virol 76:9664-9672
76. Bacot-Davis VR, Palmenberg AC (2013) Encephalomyocarditis virus Leader protein hinge domain is responsible for interactions with Ran GTPase. Virology 443:177-185
77. Wang D, Fang L, Luo R, Ye R, Fang Y, Xie L, Chen H, Xiao S (2010) Foot-and-mouth disease virus leader proteinase inhibits dsRNA-induced type I interferon transcription by decreasing interferon regulatory factor 3/7 in protein levels. Biochem Biophys Res Commun 399:72-78
78. Bibeau-Poirier A, Servant MJ (2008) Roles of ubiquitination in pattern-recognition receptors and type I interferon receptor signaling. Cytokine 43:359-367
79. Nijman SM, Luna-Vargas MP, Velds A, Brummelkamp TR, Dirac AM, Sixma TK, Bernards R (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell 123:773-786
80. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S, Wu P, Wiesmann C, Baker R, Boone DL, Ma A, Koonin EV, Dixit VM (2004) De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430:694-699
81. Kelliher MA, Grimm S, Ishida Y, Kuo F, Stanger BZ, Leder P (1998) The death domain kinase RIP mediates the TNF-induced NF-kappaB signal. Immunity 8:297-303
82. Yokota S, Okabayashi T, Yokosawa N, Fujii N (2008) Measles virus P protein suppresses Toll-like receptor signal through up-regulation of ubiquitin-modifying enzyme A20. FASEB J 22:74-83
83. Ratia K, Saikatendu KS, Santarsiero BD, Barretto N, Baker SC, Stevens RC, Mesecar AD (2006) Severe acute respiratory syndrome coronavirus papain-like protease: structure of a viral deubiquitinating enzyme. Proc Natl Acad Sci U S A 103:5717-5722
84. Kim S, Kim H, Choi Y, Kim Y (2015) A new strategy for fluorogenic esterase probes displaying low levels of non-specific hydrolysis. Chemistry 21:9645-9649
85. Devi L, Pawar RM, Makala H, Goel S (2015) Conserved expression of ubiquitin carboxyl-terminal esterase L1 (UCHL1) in mammalian testes. Indian J Exp Biol 53:305-312
86. Okumura A, Alce T, Lubyova B, Ezelle H, Strebel K, Pitha PM (2008) HIV-1 accessory proteins VPR and Vif modulate antiviral response by targeting IRF-3 for degradation. Virology 373:85-97
87. Gale M Jr, Sen GC (2009) Viral evasion of the interferon system. J Interferon Cytokine Res 29:475-476
88. Viswanathan K, Fruh K, DeFilippis V (2010) Viral hijacking of the host ubiquitin system to evade interferon responses. Curr Opin Microbiol 13:517-523
89. Yang X, Chen X, Bian G, Tu J, Xing Y, Wang Y, Chen Z (2014) Proteolytic processing, deubiquitinase and interferon antagonist activities of Middle East respiratory syndrome coronavirus papain-like protease. J Gen Virol 95:614-626
90. Gazzard L, Williams K, Chen H, Axford L, Blackwood E, Burton B, Chapman K, Crackett P, Drobnick J, Ellwood C, Epler J, Flagella M, Gancia E, Gill M, Goodacre S, Halladay J, Hewitt J, Hunt H, Kintz S, Lyssikatos J, Macleod C, Major S, Medard G, Narukulla R, Ramiscal J, Schmidt S, Seward E, Wiesmann C, Wu P, Yee S, Yen I, Malek S (2015) Mitigation of acetylcholine esterase activity in the 1,7-diazacarbazole series of inhibitors of checkpoint kinase 1. J Med Chem 58:5053-5074
91. Hu M, Li P, Song L, Jeffrey PD, Chenova TA, Wilkinson KD, Cohen RE, Shi Y (2005) Structure and mechanisms of the proteasome-associated deubiquitinating enzyme USP14. EMBO J 24:3747-3756
92. Aravind L, Koonin EV (2000) SAP-a putative DNA-binding motif involved in chromosomal organization. Trends Biochem Sci 25:112-114
93. Kipp M, Gohring F, Ostendorp T, van Drunen CM, van Driel R, Przybylski M, Fackelmayer FO (2000) SAF-Box, a conserved protein domain that specifically recognizes scaffold attachment region DNA. Mol Cell Biol 20:7480-7489
94. Shuai K (2006) Regulation of cytokine signaling pathways by PIAS proteins. Cell Res 16:196-202
95. Kubota T, Matsuoka M, Xu S, Otsuki N, Takeda M, Kato A, Ozato K (2011) PIASy inhibits virus-induced and interferon-stimulated transcription through distinct mechanisms. J Biol Chem 286:8165-8175
96. Everett RD, Chelbi-Alix MK (2007) PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89:819-830
97. Chang TH, Kubota T, Matsuoka M, Jones S, Bradfute SB, Bray M, Ozato K (2009) Ebola Zaire virus blocks type I interferon production by exploiting the host SUMO modification machinery. PLoS Pathog 5:e1000493
98. Jang HD, Yoon K, Shin YJ, Kim J, Lee SY (2004) PIAS3 suppresses NF-kappaB-mediated transcription by interacting with the p65/RelA subunit. J Biol Chem 279:24873-24880
99. Diaz-San Segundo F, Weiss M, Perez-Martin E, Dias CC, Grubman MJ, de los Santos T (2012) Inoculation of swine with foot-and-mouth disease SAP-mutant virus induces early protection against disease. J Virol 86:1316-1327
100. Zhu Z, Yang F, Zhang K, Cao W, Jin Y, Wang G, Mao R, Li D, Guo J, Liu X, Zheng H (2015) Comparative proteomic analysis of wild-type and SAP domain mutant foot-and-mouth disease virus-infected porcine cells identifies the ubiquitin-activating enzyme UBE1 required for virus replication. J Proteom Res 14:4194-4206