La Piedad Michoacán Mexico Virus V protein antagonizes type I interferon response by binding STAT2 protein and preventing STATs nuclear translocation

Virus Research

Volumn 213, Issue , 2016, Pages 11-22

  Pisanelli, Giuseppe ^a,b   Laurent Rolle, Maudry ^a   Manicassamy, Balaji ^a,d   Belicha Villanueva, Alan ^a   Morrison, Juliet ^a,e   Lozano Dubernard, Bernardo ^c   Castro Peralta, Felipa ^c   Iovane, Giuseppe ^b   García Sastre, Adolfo ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c SA de CV   (Mexico)

^d UNIVERSITY OF CHICAGO   (United States)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

(LPMV) La Piedad Michoacan Mexico Virus; Interferon signaling antagonist; LPMV V; STAT2

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; GAMMA INTERFERON; STAT1 PROTEIN; STAT2 PROTEIN; VIRUS PROTEIN V; INTERFERON; PROTEIN BINDING; V PROTEIN, PORCINE RUBULAVIRUS; VIRAL PROTEIN;

ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN; CONTROLLED STUDY; CYTOPLASM; HELA CELL LINE; HUMAN; HUMAN CELL; INNATE IMMUNITY; LA PIEDAD MICHOACAN MEXICO VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RUBULAVIRUS; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; IMMUNOLOGY; METABOLISM; PIG; PROTEIN TRANSPORT;

ANIMALS; CELL LINE; HUMANS; INTERFERON TYPE I; PROTEIN BINDING; PROTEIN TRANSPORT; RUBULAVIRUS; STAT2 TRANSCRIPTION FACTOR; SWINE; VIRAL PROTEINS;

EID: 84958758698     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2015.10.027     Document Type: Article

References (76)

1. Andrejeva J., Childs K.S., Young D.F., Carlos T.S., Stock N., Goodbourn S., Randall R.E. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(49):17264-17269.
2. Andrejeva J., Young D.F., Goodbourn S., Randall R.E. Degradation of STAT1 and STAT2 by the V proteins of simian virus 5 and human parainfluenza virus type 2, respectively: consequences for virus replication in the presence of alpha/beta and gamma interferons. J. Virol. 2002, 76(5):2159-2167.
3. Berg M., Bergvall A.C., Svenda M., Sundqvist A., Moreno-Lopez J., Linne T. Analysis of the fusion protein gene of the porcine rubulavirus LPMV: comparative analysis of paramyxovirus F proteins. Virus Genes 1997, 14(1):55-61.
4. Berg M., Hjertner B., Moreno-Lopez J., Linne T. The P gene of the porcine paramyxovirus LPMV encodes three possible polypeptides P, V and C: the P protein mRNA is edited. J. Gen Virol 1992, 73(Pt. 5):1195-1200.
5. Berg M., Sundqvist A., Moreno-Lopez J., Linne T. Identification of the porcine paramyxovirus LPMV matrix protein gene: comparative sequence analysis with other paramyxoviruses. J Gen. Virol. 1991, 72(Pt 5):1045-1050.
6. Billiau A., Matthys P. Interferon-gamma: a historical perspective. Cytokine Growth Factor Rev. 2009, 20(2):97-113.
7. Childs K., Randall R., Goodbourn S. Paramyxovirus V proteins interact with the RNA Helicase LGP2 to inhibit RIG-I-dependent interferon induction. J. Virol. 2012, 86(7):3411-3421.
8. Colamonici O., Yan H., Domanski P., Handa R., Smalley D., Mullersman J., Witte M., Krishnan K., Krolewski J. Direct binding to and tyrosine phosphorylation of the alpha subunit of the type I interferon receptor by p135tyk2 tyrosine kinase. Mol. Cell. Biol. 1994, 14(12):8133-8142.
9. Colamonici O.R., Platanias L.C., Domanski P., Handa R., Gilmour K.C., Diaz M.O., Reich N., Pitha-Rowe P. Transmembrane signaling by the alpha subunit of the type I interferon receptor is essential for activation of the JAK kinases and the transcriptional factor ISGF3. J. Biol. Chem. 1995, 270(14):8188-8193.
10. Cuevas-Romero J.S., Hernandez-Baumgarten E., Kennedy S., Hernandez-Jauregui P., Berg M., Moreno-Lopez J. Long-term RNA persistence of Porcine rubulavirus (PorPV-LPMV) after an outbreak of a natural infection: the detection of viral mRNA in sentinel pigs suggests viral transmission. Virus Res. 2014.
11. Cuevas-Romero S., Blomstrom A.L., Alvarado A., Hernandez-Jauregui P., Rivera-Benitez F., Ramirez-Mendoza H., Berg M. Development of a real-time RT-PCR method for detection of porcine rubulavirus (PoRV-LPMV). J. Virol. Methods 2013, 189(1):1-6.
12. Davis M.E., Wang M.K., Rennick L.J., Full F., Gableske S., Mesman A.W., Gringhuis S.I., Geijtenbeek T.B., Duprex W.P., Gack M.U. Antagonism of the phosphatase PP1 by the measles virus V protein is required for innate immune escape of MDA5. Cell Host Microbe 2014, 16(1):19-30.
13. Didcock L., Young D.F., Goodbourn S., Randall R.E. Sendai virus and simian virus 5 block activation of interferon-responsive genes: importance for virus pathogenesis. J. Virol. 1999, 73(4):3125-3133.
14. Didcock L., Young D.F., Goodbourn S., Randall R.E. The V protein of simian virus 5 inhibits interferon signalling by targeting STAT1 for proteasome-mediated degradation. J. Virol. 1999, 73(12):9928-9933.
15. Escobar-Lopez A.C., Rivera-Benitez J.F., Castillo-Juarez H., Ramirez-Mendoza H., Trujillo-Ortega M.E., Sanchez-Betancourt J.I. Identification of antigenic variants of the Porcine Rubulavirus in sera of field swine and their seroprevalence. Transbound Emerg. Dis. 2012, 59(5):416-420.
16. Flores-Ocelotl Mdel R., Rosas-Murrieta N.H., Vallejo-Ruiz V., Reyes-Leyva J., Herrera-Camacho I., Santos-Lopez G. Transcription of interferon stimulated genes in response to Porcine rubulavirus infection in vitro. Braz. J. Microbiol. 2011, 42(3):1167-1175.
17. Fu X.Y., Kessler D.S., Veals S.A., Levy D.E., Darnell J.E. ISGF3, the transcriptional activator induced by interferon alpha, consists of multiple interacting polypeptide chains. Proc. Natl. Acad. Sci. U. S. A. 1990, 87(21):8555-8559.
18. Garcia-Sastre A., Biron C.A. Type 1 interferons and the virus-host relationship: a lesson in detente. Science 2006, 312(5775):879-882.
19. Garcia-Sastre A., Egorov A., Matassov D., Brandt S., Levy D.E., Durbin J.E., Palese P., Muster T. Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 1998, 252(2):324-330.
20. Goodbourn S., Randall R.E. The regulation of type I interferon production by paramyxoviruses. J. Interferon Cytokine Res. 2009, 29(9):539-548.
21. Greenlund A.C., Morales M.O., Viviano B.L., Yan H., Krolewski J., Schreiber R.D. Stat recruitment by tyrosine-phosphorylated cytokine receptors: an ordered reversible affinity-driven process. Immunity 1995, 2(6):677-687.
22. Gupta S., Yan H., Wong L.H., Ralph S., Krolewski J., Schindler C. The SH2 domains of Stat1 and Stat2 mediate multiple interactions in the transduction of IFN-alpha signals. EMBO J. 1996, 15(5):1075-1084.
23. Hagmaier K., Stock N., Precious B., Childs K., Wang L.F., Goodbourn S., Randall R.E. Mapuera virus, a rubulavirus that inhibits interferon signalling in a wide variety of mammalian cells without degrading STATs. J. Gen. Virol. 2007, 88(Pt 3):956-966.
24. Hausmann S., Garcin D., Delenda C., Kolakofsky D. The versatility of paramyxovirus RNA polymerase stuttering. J. Virol. 1999, 73(7):5568-5576.
25. Hausmann S., Garcin D., Morel A.S., Kolakofsky D. Two nucleotides immediately upstream of the essential A6G3 slippery sequence modulate the pattern of G insertions during Sendai virus mRNA editing. J. Virol. 1999, 73(1):343-351.
26. Hernandez J., Reyes-Leyva J., Zenteno R., Ramirez H., Hernandez-Jauregui P., Zenteno E. Immunity to porcine rubulavirus infection in adult swine. Vet. Immunol. Immunopathol. 1998, 64(4):367-381.
27. Hernandez-Jauregui P., Ramirez Mendoza H., Mercado Garcia C., Moreno-Lopez J., Kennedy S. Experimental porcine rubulavirus (La Piedad-Michoacan virus) infection in pregnant gilts. J. Comp. Pathol. 2004, 130(1):1-6.
28. Iseni F., Baudin F., Garcin D., Marq J.B., Ruigrok R.W., Kolakofsky D. Chemical modification of nucleotide bases and mRNA editing depend on hexamer or nucleoprotein phase in Sendai virus nucleocapsids. RNA 2002, 8(8):1056-1067.
29. Kolakofsky D., Roux L., Garcin D., Ruigrok R.W. Paramyxovirus mRNA editing, the rule of six and error catastrophe: a hypothesis. J. Gen. Virol. 2005, 86(Pt 7):1869-1877.
30. Kubota T., Yokosawa N., Yokota S., Fujii N., Tashiro M., Kato A. Mumps virus V protein antagonizes interferon without the complete degradation of STAT1. J. Virol. 2005, 79(7):4451-4459.
31. Laurent-Rolle M., Morrison J., Rajsbaum R., Macleod J.M., Pisanelli G., Pham A., Ayllon J., Miorin L., Martinez-Romero C., tenOever B.R., Garcia-Sastre A. The interferon signaling antagonist function of yellow fever virus NS5 protein is activated by type I interferon. Cell Host Microbe 2014, 16(3):314-327.
32. Leung S., Qureshi S.A., Kerr I.M., Darnell J.E., Stark G.R. Role of STAT2 in the alpha interferon signaling pathway. Mol. Cell. Biol. 1995, 15(3):1312-1317.
33. Li X., Leung S., Kerr I.M., Stark G.R. Functional subdomains of STAT2 required for preassociation with the alpha interferon receptor and for signaling. Mol. Cell. Biol. 1997, 17(4):2048-2056.
34. Linne T., Berg M., Bergvall A.C., Hjertner B., Moreno-Lopez J. The molecular biology of the porcine paramyxovirus LPMV. Vet. Microbiol. 1992, 33(1-4):263-273.
35. Manicassamy B., Manicassamy S., Belicha-Villanueva A., Pisanelli G., Pulendran B., Garcia-Sastre A. Analysis of in vivo dynamics of influenza virus infection in mice using a GFP reporter virus. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(25):11531-11536.
36. Mendoza-Magana M.L., Godoy-Martinez D.V., Guerrero-Cazares H., Rodriguez-Peredo A., Duenas-Jimenez J.M., Duenas-Jimenez S.H., Ramirez-Herrera M.A. Blue eye disease porcine rubulavirus (PoRv) infects pig neurons and glial cells using sialo-glycoprotein as receptor. Vet. J. 2007, 173(2):428-436.
37. Meyer O. Interferons and autoimmune disorders. Joint Bone Spine 2009, 76(5):464-473.
38. Moreno-Lopez J., Correa-Giron P., Martinez A., Ericsson A. Characterization of a paramyxovirus isolated from the brain of a piglet in Mexico. Arch. Virol. 1986, 91(3-4):221-231.
39. Morrison J., Laurent-Rolle M., Maestre A.M., Rajsbaum R., Pisanelli G., Simon V., Mulder L.C., Fernandez-Sesma A., Garcia-Sastre A. Dengue virus co-opts UBR4 to degrade STAT2 and antagonize type I interferon signaling. PLoS Pathog. 2013, 9(3):e1003265.
40. Motz C., Schuhmann K.M., Kirchhofer A., Moldt M., Witte G., Conzelmann K.K., Hopfner K.P. Paramyxovirus V proteins disrupt the fold of the RNA sensor MDA5 to inhibit antiviral signaling. Science 2013, 339(6120):690-693.
41. Nadeau O.W., Domanski P., Usacheva A., Uddin S., Platanias L.C., Pitha P., Raz R., Levy D., Majchrzak B., Fish E., Colamonici O.R. The proximal tyrosines of the cytoplasmic domain of the beta chain of the type I interferon receptor are essential for signal transducer and activator of transcription (Stat) 2 activation. Evidence that two Stat2 sites are required to reach a threshold of interferon alpha-induced Stat2 tyrosine phosphorylation that allows normal formation of interferon-stimulated gene factor 3. J. Biol. Chem. 1999, 274(7):4045-4052.
42. Nishio M., Garcin D., Simonet V., Kolakofsky D. The carboxyl segment of the mumps virus V protein associates with Stat proteins in vitro via a tryptophan-rich motif. Virology 2002, 300(1):92-99.
43. Nishio M., Tsurudome M., Ito M., Garcin D., Kolakofsky D., Ito Y. Identification of paramyxovirus V protein residues essential for STAT protein degradation and promotion of virus replication. J. Virol. 2005, 79(13):8591-8601.
44. Nishio M., Tsurudome M., Ito M., Ito Y. Human parainfluenza virus type 4 is incapable of evading the interferon-induced antiviral effect. J. Virol. 2005, 79(23):14756-14768.
45. Niwa H., Yamamura K., Miyazaki J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 1991, 108(2):193-199.
46. Parisien J.P., Lau J.F., Rodriguez J.J., Sullivan B.M., Moscona A., Parks G.D., Lamb R.A., Horvath C.M. The V protein of human parainfluenza virus 2 antagonizes type I interferon responses by destabilizing signal transducer and activator of transcription 2. Virology 2001, 283(2):230-239.
47. Parisien J.P., Lau J.F., Rodriguez J.J., Ulane C.M., Horvath C.M. Selective STAT protein degradation induced by paramyxoviruses requires both STAT1 and STAT2 but is independent of alpha/beta interferon signal transduction. J. Virol. 2002, 76(9):4190-4198.
48. Park M.S., Shaw M.L., Munoz-Jordan J., Cros J.F., Nakaya T., Bouvier N., Palese P., Garcia-Sastre A., Basler C.F. Newcastle disease virus (NDV)-based assay demonstrates interferon-antagonist activity for the NDV V protein and the Nipah virus V, W, and C proteins. J. Virol. 2003, 77(2):1501-1511.
49. Precious B., Childs K., Fitzpatrick-Swallow V., Goodbourn S., Randall R.E. Simian virus 5V protein acts as an adaptor, linking DDB1 to STAT2, to facilitate the ubiquitination of STAT1. J. Virol. 2005, 79(21):13434-13441.
50. Precious B., Young D.F., Andrejeva L., Goodbourn S., Randall R.E. In vitro and in vivo specificity of ubiquitination and degradation of STAT1 and STAT2 by the V proteins of the paramyxoviruses simian virus 5 and human parainfluenza virus type 2. J. Gen. Virol. 2005, 86(Pt 1):151-158.
51. Qureshi S.A., Salditt-Georgieff M., Darnell J.E. Tyrosine-phosphorylated Stat1 and Stat2 plus a 48-kDa protein all contact DNA in forming interferon-stimulated-gene factor 3. Proc. Natl. Acad. Sci. U. S. A. 1995, 92(9):3829-3833.
52. Qureshi S.A., Leung S., Kerr I.M., Stark G.R., Darnell J.E. Function of Stat2 protein in transcriptional activation by alpha interferon. Mol. Cell. Biol. 1996, 16(1):288-293.
53. Rajsbaum R., Versteeg G.A., Schmid S., Maestre A.M., Belicha-Villanueva A., Martinez-Romero C., Patel J.R., Morrison J., Pisanelli G., Miorin L., Laurent-Rolle M., Moulton H.M., Stein D.A., Fernandez-Sesma A., tenOever B.R., Garcia-Sastre A. Unanchored K48-linked polyubiquitin synthesized by the E3-ubiquitin ligase TRIM6 stimulates the interferon-IKKepsilon kinase-mediated antiviral response. Immunity 2014, 40(6):880-895.
54. Ramachandran A., Horvath C.M. Paramyxovirus disruption of interferon signal transduction: STATus report. J. Interferon Cytokine Res. 2009, 29(9):531-537.
55. Ramirez-Mendoza H., Hernandez-Jauregui P., Reyes-Leyva J., Zenteno E., Moreno-Lopez J., Kennedy S. Lesions in the reproductive tract of boars experimentally infected with porcine rubulavirus. J. Comp. Pathol. 1997, 117(3):237-252.
56. Randall R.E., Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 2008, 89(Pt 1):1-47.
57. Reyes-Leyva J., Espinosa B., Santos G., Zenteno R., Hernandez J., Vallejo V., Zenteno E. Purification and characterization of the hemagglutinin-neuraminidase of Porcine rubulavirus LPMV. Glycoconj. J. 1999, 16(9):517-522.
58. Rivera-Benitez J.F., Cuevas-Romero S., Perez-Torres A., Reyes-Leyva J., Hernandez J., Ramirez-Mendoza H. Respiratory disease in growing pigs after Porcine rubulavirus experimental infection. Virus Res. 2013, 176(1-2):137-143.
59. Rodriguez J.J., Parisien J.P., Horvath C.M. Nipah virus V protein evades alpha and gamma interferons by preventing STAT1 and STAT2 activation and nuclear accumulation. J. Virol. 2002, 76(22):11476-11483.
60. Rodriguez J.J., Wang L.F., Horvath C.M. Hendra virus V protein inhibits interferon signaling by preventing STAT1 and STAT2 nuclear accumulation. J. Virol. 2003, 77(21):11842-11845.
61. Rodriguez K.R., Horvath C.M. Paramyxovirus V protein interaction with the antiviral sensor LGP2 disrupts MDA5 signaling enhancement but is not relevant to LGP2-mediated RLR signaling inhibition. J. Virol. 2014, 88(14):8180-8188.
62. Rodriguez-Ropon A., Hernandez-Jauregui P., Sanchez-Torres L., Favila-Castillo L., Estrada-Parra S., Moreno-Lopez J., Kennedy S. Apoptosis in lymph nodes and changes in lymphocyte subpopulations in peripheral blood of pigs infected with porcine rubulavirus. J. Comp. Pathol. 2003, 128(1):1-8.
63. Rothlisberger A., Wiener D., Schweizer M., Peterhans E., Zurbriggen A., Plattet P. Two domains of the V protein of virulent canine distemper virus selectively inhibit STAT1 and STAT2 nuclear import. J. Virol. 2010, 84(13):6328-6343.
64. Sanchez-Betancourt J.I., Trujillo M.E., Mendoza S.E., Reyes-Leyva J., Alonso R.A. Genetic and antigenic changes in porcine rubulavirus. Can. J. Vet. Res. 2012, 76(1):33-37.
65. Shuai K., Stark G.R., Kerr I.M., Darnell J.E. A single phosphotyrosine residue of STAT91 required for gene activation by interferon-gamma. Science 1993, 261(5129):1744-1746.
66. Solis M., Ramirez-Mendoza H., Mercado C., Espinosa S., Vallejo V., Reyes-Leyva J., Hernandez J. Semen alterations in porcine rubulavirus-infected boars are related to viral excretion and have implications for artificial insemination. Res. Vet. Sci. 2007, 83(3):403-409.
67. Stephan H.A., Gay G.M., Ramirez T.C. Encephalomyelitis, reproductive failure and corneal opacity (blue eye) in pigs, associated with a paramyxovirus infection. Vet. Rec. 1988, 122(1):6-10.
68. Sundqvist A., Berg M., Hernandez-Jauregui P., Linne T., Moreno-Lopez J. The structural proteins of a porcine paramyxovirus (LPMV). J. Gen. Virol. 1990, 71(Pt 3):609-613.
69. Sundqvist A., Berg M., Moreno-Lopez J., Linne T. The haemagglutinin-neuraminidase glycoprotein of the porcine paramyxovirus LPMV: comparison with other paramyxoviruses revealed the closest relationship to simian virus 5 and mumps virus. Arch. Virol. 1992, 122(3-4):331-340.
70. Svenda M., Berg M., Moreno-Lopez J., Linne T. Analysis of the large (L) protein gene of the porcine rubulavirus LPMV: identification of possible functional domains. Virus Res. 1997, 48(1):57-70.
71. Takeuchi K., Kadota S.I., Takeda M., Miyajima N., Nagata K. Measles virus V protein blocks interferon (IFN)-alpha/beta but not IFN-gamma signaling by inhibiting STAT1 and STAT2 phosphorylation. FEBS Lett. 2003, 545(2-3):177-182.
72. Thomas S.M., Lamb R.A., Paterson R.G. Two mRNAs that differ by two nontemplated nucleotides encode the amino coterminal proteins P and V of the paramyxovirus SV5. Cell 1988, 54(6):891-902.
73. Ulane C.M., Horvath C.M. Paramyxoviruses SV5 and HPIV2 assemble STAT protein ubiquitin ligase complexes from cellular components. Virology 2002, 304(2):160-166.
74. Wiman A.C., Hjertner B., Linne T., Herron B., Allan G., McNeilly F., Adair B., Moreno-Lopez J., Berg M. Porcine rubulavirus LPMV RNA persists in the central nervous system of pigs after recovery from acute infection. J. Neurovirol. 1998, 4(5):545-552.
75. Yan H., Krishnan K., Greenlund A.C., Gupta S., Lim J.T., Schreiber R.D., Schindler C.W., Krolewski J.J. Phosphorylated interferon-alpha receptor 1 subunit (IFNaR1) acts as a docking site for the latent form of the 113 kDa STAT2 protein. EMBO J. 1996, 15(5):1064-1074.
76. Zenteno-Cuevas R., Huerta-Yepez S., Reyes-Leyva J., Hernandez-Jauregui P., Gonzalez-Bonilla C., Ramirez-Mendoza H., Agundis C., Zenteno E. Identification of potential B cell epitope determinants by computer techniques, in hemagglutinin-neuraminidase from the porcine rubulavirus La Piedad Michoacan. Viral Immunol. 2007, 20(2):250-260.