Evolution and structural organization of the C proteins of Paramyxovirinae

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Lo, Michael K ^a   Søgaard, Teit Max ^b   Karlin, David G ^b  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN C; RECOMBINANT PROTEIN; STAT1 PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; GEL PERMEATION CHROMATOGRAPHY; MOLECULAR EVOLUTION; NIPAH VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PARAINFLUENZA VIRUS 1; PARAMYXOVIRUS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SCANDENTIA; SEQUENCE HOMOLOGY; VIRUS GENOME; VIRUS REPLICATION;

AMINO ACID SEQUENCE; BINDING SITES; EVOLUTION, MOLECULAR; MOLECULAR SEQUENCE DATA; PARAMYXOVIRINAE; PHOSPHOPROTEINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY, NUCLEIC ACID; SPECIES SPECIFICITY; STAT1 TRANSCRIPTION FACTOR; VIRAL PROTEINS;

EID: 84896107260     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090003     Document Type: Article

References (157)

1. Mayo MA (2002) A summary of taxonomic changes recently approved by ICTV. Arch Virol 147: 1655-1663.
2. Lamb RA, Parks GD (2007) Paramyxoviridae: the viruses and their replication. In: Knipe DM, Howley PM, editors. Fields Virology. Fifth edition ed. Philadelphia: Lippincott Williams & Wilkins. 1449-1496.
3. Bellini WJ, Englund G, Rozenblatt S, Arnheiter H, Richardson CD (1985) Measles virus P gene codes for two proteins. J Virol 53: 908-919. (Pubitemid 15173300)
4. Giorgi C, Blumberg BM, Kolakofsky D (1983) Sendai virus contains overlapping genes expressed from a single mRNA. Cell 35: 829-836. (Pubitemid 14168382)
5. Lo MK, Harcourt BH, Mungall BA, Tamin A, Peeples ME, et al. (2009) Determination of the henipavirus phosphoprotein gene mRNA editing frequencies and detection of the C, V and W proteins of Nipah virus in virus-infected cells. J Gen Virol 90: 398-404.
6. Curran J, Kolakofsky D (1988) Ribosomal initiation from an ACG codon in the Sendai virus P/C mRNA. EMBO J 7: 245-251.
7. Boeck R, Curran J, Matsuoka Y, Compans R, Kolakofsky D (1992) The parainfluenza virus type 1 P/C gene uses a very efficient GUG codon to start its C' protein. J Virol 66: 1765-1768.
8. Latorre P, Kolakofsky D, Curran J (1998) Sendai virus Y proteins are initiated by a ribosomal shunt. Molecular and Cellular Biology 18: 5021-5031. (Pubitemid 28388085)
9. de Breyne S, Monney RS, Curran J (2004) Proteolytic processing and translation initiation: two independent mechanisms for the expression of the Sendai virus Y proteins. J Biol Chem 279: 16571-16580. (Pubitemid 38509357)
10. Karlin D, Longhi S, Receveur V, Canard B (2002) The N-terminal domain of the phosphoprotein of Morbilliviruses belongs to the natively unfolded class of proteins. Virology 296: 251-262. (Pubitemid 34713265)
11. Habchi J, Mamelli L, Darbon H, Longhi S (2010) Structural disorder within Henipavirus nucleoprotein and phosphoprotein: from predictions to experimental assessment. PLoS One 5: e11684.
12. Chinchar VG, Portner A (1981) Inhibition of RNA synthesis following proteolytic cleavage of Newcastle disease virus P protein. Virology 115: 192-202.
13. Chinchar VG, Portner A (1981) Functions of Sendai virus nucleocapsid polypeptides: enzymatic activities in nucleocapsids following cleavage of polypeptide P by Staphylococcus aureus protease V8. Virology 109: 59-71. (Pubitemid 11173412)
14. Karlin D, Belshaw R (2012) Detecting remote sequence homology in disordered proteins: discovery of conserved motifs in the N-termini of Mononegavirales phosphoproteins. PLoS One 7: e31719.
15. Lo MK, Peeples ME, Bellini WJ, Nichol ST, Rota PA, et al. (2012) Distinct and overlapping roles of nipah virus p gene products in modulating the human endothelial cell antiviral response. PLOS ONE 7: e47790.
16. Takeuchi K, Komatsu T, Kitagawa Y, Sada K, Gotoh B (2008) Sendai virus C protein plays a role in restricting PKR activation by limiting the generation of intracellular double-stranded RNA. J Virol 82: 10102-10110.
17. Nakatsu Y, Takeda M, Ohno S, Shirogane Y, Iwasaki M, et al. (2008) Measles virus circumvents the host interferon response by different actions of the C and V proteins. J Virol 82: 8296-8306.
18. Nakatsu Y, Takeda M, Ohno S, Koga R, Yanagi Y (2006) Translational inhibition and increased interferon induction in cells infected with C protein-deficient measles virus. J Virol 80: 11861-11867. (Pubitemid 44788897)
19. Goodbourn S, Randall RE (2009) The regulation of type I interferon production by paramyxoviruses. J Interferon Cytokine Res 29: 539-547.
20. Sleeman K, Bankamp B, Hummel KB, Lo MK, BelliniWJ, et al. (2008) The C, V and W proteins of Nipah virus inhibit minigenome replication. J Gen Virol 89: 1300-1308.
21. Bankamp B, Wilson J, Bellini WJ, Rota PA (2005) Identification of naturally occurring amino acid variations that affect the ability of the measles virus C protein to regulate genome replication and transcription. Virology 336: 120-129. (Pubitemid 40603677)
22. Curran J, Marq JB, Kolakofsky D (1992) The Sendai virus nonstructural C proteins specifically inhibit viral mRNA synthesis. Virology 189: 647-656.
23. Cadd T, Garcin D, Tapparel C, Itoh M, Homma M, et al. (1996) The Sendai paramyxovirus accessory C proteins inhibit viral genome amplification in a promoter-specific fashion. J Virol 70: 5067-5074. (Pubitemid 26240677)
24. Reutter GL, Cortese-Grogan C, Wilson J, Moyer SA (2001) Mutations in the measles virus C protein that up regulate viral RNA synthesis. Virology 285: 100-109. (Pubitemid 32589012)
25. Audsley MD, Moseley GW (2013) Paramyxovirus evasion of innate immunity: Diverse strategies for common targets. World J Virol 2: 57-70.
26. Koyama S, Ishii KJ, Coban C, Akira S (2008) Innate immune response to viral infection. Cytokine 43: 336-341.
27. Chambers R, Takimoto T (2009) Antagonism of innate immunity by paramyxovirus accessory proteins. Viruses 1: 574-593.
28. McAllister CS, Toth AM, Zhang P, Devaux P, Cattaneo R, et al. (2010) Mechanisms of protein kinase PKR-mediated amplification of beta interferon induction by C protein-deficient measles virus. J Virol 84: 380-386.
29. Sparrer KM, Pfaller CK, Conzelmann KK (2012) Measles virus C protein interferes with Beta interferon transcription in the nucleus. J Virol 86: 796-805.
30. Boxer EL, Nanda SK, Baron MD (2009) The rinderpest virus non-structural C protein blocks the induction of type 1 interferon. Virology 385: 134-142.
31. Shaffer JA, Bellini WJ, Rota PA (2003) The C protein of measles virus inhibits the type I interferon response. Virology 315: 389-397. (Pubitemid 37324629)
32. Fontana JM, Bankamp B, Rota PA (2008) Inhibition of interferon induction and signaling by paramyxoviruses. Immunol Rev 225: 46-67.
33. Fontana JM, Bankamp B, Bellini WJ, Rota PA (2008) Regulation of interferon signaling by the C and V proteins from attenuated and wild-type strains of measles virus. Virology 374: 71-81.
34. Mathieu C, Guillaume V, Volchkova VA, Pohl C, Jacquot F, et al. (2012) Nonstructural Nipah virus C protein regulates both the early host proinflammatory response and viral virulence. J Virol 86: 10766-10775.
35. Yoneda M, Guillaume V, Sato H, Fujita K, Georges-Courbot MC, et al. (2010) The nonstructural proteins of Nipah virus play a key role in pathogenicity in experimentally infected animals. PLOS ONE 5: e12709.
36. Park MS, Shaw ML, Munoz-Jordan J, Cros JF, Nakaya T, et al. (2003) 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 77: 1501-1511. (Pubitemid 36055570)
37. Lo MK, Rota PA (2008) The emergence of Nipah virus, a highly pathogenic paramyxovirus. J Clin Virol 43: 396-400.
38. Boonyaratanakornkit J, Bartlett E, Schomacker H, Surman S, Akira S, et al. (2011) The C proteins of human parainfluenza virus type 1 limit double-stranded RNA accumulation that would otherwise trigger activation of MDA5 and protein kinase R. J Virol 85: 1495-1506.
39. Irie T, Nagata N, Igarashi T, Okamoto I, Sakaguchi T (2010) Conserved charged amino acids within Sendai virus C protein play multiple roles in the evasion of innate immune responses. PLoS One 5: e10719.
40. Wells G, Addington-Hall M, Malur AG (2012) Mutations within the human parainfluenza virus type 3 (HPIV 3) C protein affect viral replication and host interferon induction. Virus Res 167: 385-390.
41. Schomacker H, Hebner RM, Boonyaratanakornkit J, Surman S, Amaro-Carambot E, et al. (2012) The C proteins of human parainfluenza virus type 1 block IFN signaling by binding and retaining Stat1 in perinuclear aggregates at the late endosome. PLOS ONE 7: e28382.
42. Boonyaratanakornkit JB, Bartlett EJ, Amaro-Carambot E, Collins PL, Murphy BR, et al. (2009) The C proteins of human parainfluenza virus type 1 (HPIV1) control the transcription of a broad array of cellular genes that would otherwise respond to HPIV1 infection. J Virol 83: 1892-1910.
43. Van Cleve W, Amaro-Carambot E, Surman SR, Bekisz J, Collins PL, et al. (2006) Attenuating mutations in the P/C gene of human parainfluenza virus type 1 (HPIV1) vaccine candidates abrogate the inhibition of both induction and signaling of type I interferon (IFN) by wild-type HPIV1. Virology 352: 61-73. (Pubitemid 44164412)
44. Malur AG, Chattopadhyay S, Maitra RK, Banerjee AK (2005) Inhibition of STAT 1 phosphorylation by human parainfluenza virus type 3 C protein. J Virol 79: 7877-7882. (Pubitemid 40756823)
45. Komatsu T, Takeuchi K, Yokoo J, Gotoh B (2004) C and V proteins of Sendai virus target signaling pathways leading to IRF-3 activation for the negative regulation of interferon-beta production. Virology 325: 137-148. (Pubitemid 38844777)
46. Kato A, Cortese-Grogan C, Moyer SA, Sugahara F, Sakaguchi T, et al. (2004) Characterization of the amino acid residues of sendai virus C protein that are critically involved in its interferon antagonism and RNA synthesis down-regulation. J Virol 78: 7443-7454. (Pubitemid 38915890)
47. Gotoh B, Takeuchi K, Komatsu T, Yokoo J (2003) The STAT2 activation process is a crucial target of Sendai virus C protein for the blockade of alpha interferon signaling. J Virol 77: 3360-3370. (Pubitemid 36297255)
48. Garcin D, Marq JB, Goodbourn S, Kolakofsky D (2003) The amino-terminal extensions of the longer Sendai virus C proteins modulate pY701-Stat1 and bulk Stat1 levels independently of interferon signaling. J Virol 77: 2321-2329. (Pubitemid 36222755)
49. Garcin D, Marq JB, Strahle L, le Mercier P, Kolakofsky D (2002) All four Sendai Virus C proteins bind Stat1, but only the larger forms also induce its mono-ubiquitination and degradation. Virology 295: 256-265. (Pubitemid 34921311)
50. Garcin D, Curran J, Itoh M, Kolakofsky D (2001) Longer and shorter forms of Sendai virus C proteins play different roles in modulating the cellular antiviral response. J Virol 75: 6800-6807. (Pubitemid 32641565)
51. Gotoh B, Takeuchi K, Komatsu T, Yokoo J, Kimura Y, et al. (1999) Knockout of the Sendai virus C gene eliminates the viral ability to prevent the interferon-alpha/beta-mediated responses. FEBS Lett 459: 205-210. (Pubitemid 29475031)
52. Garcin D, Latorre P, Kolakofsky D (1999) Sendai virus C proteins counteract the interferon-mediated induction of an antiviral state. J Virol 73: 6559-6565. (Pubitemid 29327837)
53. Bartlett EJ, Cruz AM, Esker J, Castano A, Schomacker H, et al. (2008) Human parainfluenza virus type 1 C proteins are nonessential proteins that inhibit the host interferon and apoptotic responses and are required for efficient replication in nonhuman primates. J Virol 82: 8965-8977.
54. Irie T, Okamoto I, Yoshida A, Nagai Y, Sakaguchi T (2014) Sendai virus C proteins regulate viral genome and antigenome synthesis to dictate the negative genome polarity. J Virol 88: 690-698.
55. Caignard G, Guerbois M, Labernardiere JL, Jacob Y, Jones LM, et al. (2007) Measles virus V protein blocks Jak1-mediated phosphorylation of STAT1 to escape IFN-alpha/beta signaling. Virology 368: 351-362. (Pubitemid 350019486)
56. Devaux P, Hudacek AW, Hodge G, Reyes-Del Valle J, McChesney MB, et al. (2011) A recombinant measles virus unable to antagonize STAT1 function cannot control inflammation and is attenuated in rhesus monkeys. J Virol 85: 348-356.
57. Rothlisberger A, Wiener D, Schweizer M, Peterhans E, Zurbriggen A, et al. (2010) Two Domains of the V Protein of Virulent Canine Distemper Virus Selectively Inhibit STAT1 and STAT2 Nuclear Import. Journal of Virology 84: 6328-6343.
58. Ciancanelli MJ, Volchkova VA, Shaw ML, Volchkov VE, Basler CF (2009) Nipah virus sequesters inactive STAT1 in the nucleus via a P gene-encoded mechanism. J Virol 83: 7828-7841.
59. Rodriguez JJ, Wang LF, Horvath CM (2003) Hendra virus V protein inhibits interferon signaling by preventing STAT1 and STAT2 nuclear accumulation. J Virol 77: 11842-11845. (Pubitemid 37271681)
60. Nanda SK, Baron MD (2006) Rinderpest virus blocks type I and type II interferon action: role of structural and nonstructural proteins. J Virol 80: 7555-7568. (Pubitemid 44092577)
61. Chinnakannan SK, Nanda SK, Baron MD (2013) Morbillivirus v proteins exhibit multiple mechanisms to block type 1 and type 2 interferon signalling pathways. PLOS ONE 8: e57063.
62. Chinnakannan SK, Holzer B, Sanz Bernardo B, Nanda SK, Baron MD (2014) Different functions of the common P/V/W and V-specific domains of rinderpest virus V protein in blocking interferon signalling. J Gen Virol 95: 44-51.
63. Long M, Betran E, Thornton K, Wang W (2003) The origin of new genes: glimpses from the young and old. Nat Rev Genet 4: 865-875. (Pubitemid 37345613)
64. Taylor JS, Raes J (2004) Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet 38: 615-643. (Pubitemid 40017189)
65. Keese PK, Gibbs A (1992) Origins of genes: "big bang" or continuous creation? Proc Natl Acad Sci U S A 89: 9489-9493.
66. Carter JJ, Daugherty MD, Qi X, Bheda-Malge A, Wipf GC, et al. (2013) Identification of an overprinting gene in Merkel cell polyomavirus provides evolutionary insight into the birth of viral genes. Proc Natl Acad Sci U S A 110: 12744-12749.
67. Sabath N, Wagner A, Karlin D (2012) Evolution of viral proteins originated de novo by overprinting. Molecular Biology and Evolution 29: 3767-3780.
68. Rancurel C, Khosravi M, Dunker AK, Romero PR, Karlin D (2009) Overlapping genes produce proteins with unusual sequence properties and offer insight into de novo protein creation. J Virol 83: 10719-10736.
69. Li F, Ding SW (2006) Virus counterdefense: diverse strategies for evading the RNA-silencing immunity. Annu Rev Microbiol 60: 503-531. (Pubitemid 44627959)
70. van Knippenberg I, Carlton-Smith C, Elliott RM (2010) The N-terminus of Bunyamwera orthobunyavirus NSs protein is essential for interferon antagonism. J Gen Virol 91: 2002-2006.
71. Vargason JM, Szittya G, Burgyan J, Hall TM (2003) Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115: 799-811. (Pubitemid 38058493)
72. Meier C, Aricescu AR, Assenberg R, Aplin RT, Gilbert RJ, et al. (2006) The crystal structure of ORF-9b, a lipid binding protein from the SARS coronavirus. Structure 14: 1157-1165. (Pubitemid 44041056)
73. Zhang Y, Hubner IA, Arakaki AK, Shakhnovich E, Skolnick J (2006) On the origin and highly likely completeness of single-domain protein structures. Proc Natl Acad Sci U S A 103: 2605-2610.
74. Skolnick J, Zhou HY, Brylinski M (2012) Further Evidence for the Likely Completeness of the Library of Solved Single Domain Protein Structures. Journal of Physical Chemistry B 116: 6654-6664.
75. Miyata T, Yasunaga T (1978) Evolution of overlapping genes. Nature 272: 532-535. (Pubitemid 8312302)
76. Sander C, Schulz GE (1979) Degeneracy of the information contained in amino acid sequences: evidence from overlaid genes. Journal of Molecular Evolution 13: 245-252.
77. Mizokami M, Orito E, Ohba K, Ikeo K, Lau JY, et al. (1997) Constrained evolution with respect to gene overlap of hepatitis B virus. Journal of Molecular Evolution 44 Suppl 1: S83-90. (Pubitemid 27098532)
78. Hughes AL, Westover K, da Silva J, O'Connor DH, Watkins DI (2001) Simultaneous positive and purifying selection on overlapping reading frames of the tat and vpr genes of simian immunodeficiency virus. J Virol 75: 7966-7972. (Pubitemid 32743668)
79. Maman Y, Blancher A, Benichou J, Yablonka A, Efroni S, et al. (2011) Immune-induced evolutionary selection focused on a single reading frame in overlapping hepatitis B virus proteins. J Virol 85: 4558-4566.
80. Krakauer DC (2000) Stability and evolution of overlapping genes. Evolution 54: 731-739.
81. Simon-Loriere E, Holmes EC, Pagan I (2013) The effect of gene overlapping on the rate of RNA virus evolution. Molecular Biology and Evolution 30: 1916-1928.
82. Jaroszewski L, Li Z, Cai XH, Weber C, Godzik A (2011) FFAS server: novel features and applications. Nucleic Acids Research 39: W38-44.
83. Batts WN, Falk K, Winton JR (2008) Genetic Analysis of Paramyxovirus Isolates from Pacific Salmon Reveals Two Independently Co-circulating Lineages. Journal of Aquatic Animal Health 20: 215-224.
84. Winton JR, Lannan CN, Ranson DP, Fryer JL (1985) Isolation of a new virus from chinook salmon (Oncorhynchus tshawytscha) in Oregon, USA. Fish Pathology 20: 373-380.
85. Di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, et al. (2011) T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res 39: W13-17.
86. Taly JF, Magis C, Bussotti G, Chang JM, Di Tommaso P, et al. (2011) Using the T-Coffee package to build multiple sequence alignments of protein, RNA, DNA sequences and 3D structures. Nat Protoc 6: 1669-1682.
87. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
88. Procter JB, Thompson J, Letunic I, Creevey C, Jossinet F, et al. (2010) Visualization of multiple alignments, phylogenies and gene family evolution. Nat Methods 7: S16-25.
89. Abascal F, Zardoya R, Telford MJ (2010) TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res 38: W7-13.
90. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
91. Cole C, Barber JD, Barton GJ (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36: W197-201.
92. Pei J, Kim BH, Tang M, Grishin NV (2007) PROMALS web server for accurate multiple protein sequence alignments. Nucleic Acids Res 35: W649-652.
93. Ishida T, Kinoshita K (2008) Prediction of disordered regions in proteins based on the meta approach. Bioinformatics 24: 1344-1348. (Pubitemid 351737139)
94. Ferron F, Longhi S, Canard B, Karlin D (2006) A practical overview of protein disorder prediction methods. Proteins 65: 1-14. (Pubitemid 44320610)
95. Biegert A, Mayer C, Remmert M, Soding J, Lupas AN (2006) The MPI Bioinformatics Toolkit for protein sequence analysis. Nucleic Acids Res 34: W335-339. (Pubitemid 44529789)
96. Kaushik S, Mutt E, Chellappan A, Sankaran S, Srinivasan N, et al. (2013) Improved Detection of Remote Homologues Using Cascade PSI-BLAST: Influence of Neighbouring Protein Families on Sequence Coverage. PLoS One 8: e56449.
97. Biegert A, Soding J (2009) Sequence context-specific profiles for homology searching. Proc Natl Acad Sci U S A 106: 3770-3775.
98. Remmert M, Biegert A, Hauser A, Soding J (2012) HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nature Methods 9: 173-175.
99. Kuchibhatla DB, Sherman WA, Chung BY, Cook S, Schneider G, et al. (2014) Powerful sequence similarity search methods and in-depth manual analyses can identify remote homologs in many apparently "orphan" viral proteins. J Virol 88: 10-20.
100. Berrow NS, Alderton D, Sainsbury S, Nettleship J, Assenberg R, et al. (2007) A versatile ligation-independent cloning method suitable for high-throughput expression screening applications. Nucleic Acids Research 35: e45.
101. Bird LE, Rada H, Flanagan J, Diprose JM, Gilbert RJ, et al. (2014) Application of In-Fusion Cloning for the Parallel Construction of E. coli Expression Vectors. Methods Mol Biol 1116: 209-234.
102. Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41: 207-234.
103. Greenfield N, Fasman GD (1969) Computed circular dichroism spectra for the evaluation of protein conformation. Biochemistry 8: 4108-4116.
104. Kvellestad A, Dannevig BH, Falk K (2003) Isolation and partial characterization of a novel paramyxovirus from the gills of diseased seawater-reared Atlantic salmon (Salmo salar L). Journal of General Virology 84: 2179-2189. (Pubitemid 36927249)
105. McCarthy AJ, Goodman SJ (2010) Reassessing conflicting evolutionary histories of the Paramyxoviridae and the origins of respiroviruses with Bayesian multigene phylogenies. Infect Genet Evol 10: 97-107.
106. Fridell F, Devold M, Nylund A (2004) Phylogenetic position of a paramyxovirus from Atlantic salmon Salmo Salar. Diseases of Aquatic Organisms 59: 11-15. (Pubitemid 39588303)
107. Peeters B, Verbruggen P, Nelissen F, de Leeuw O (2004) The P gene of Newcastle disease virus does not encode an accessory X protein. Journal of General Virology 85: 2375-2378. (Pubitemid 39162610)
108. Kurath G, Batts WN, Ahne W, Winton JR (2004) Complete genome sequence of Fer-de-Lance virus reveals a novel gene in reptilian paramyxoviruses. J Virol 78: 2045-2056. (Pubitemid 38176736)
109. Soding J, Remmert M (2011) Protein sequence comparison and fold recognition: progress and good-practice benchmarking. Curr Opin Struct Biol 21: 404-411.
110. Dunbrack RL (2006) Sequence comparison and protein structure prediction. Current Opinion in Structural Biology 16: 374-384.
111. Marq JB, Brini A, Kolakofsky D, Garcin D (2007) Targeting of the Sendai virus C protein to the plasma membrane via a peptide-only membrane anchor. J Virol 81: 3187-3197. (Pubitemid 46456628)
112. Devaux P, von Messling V, Songsungthong W, Springfeld C, Cattaneo R (2007) Tyrosine 110 in the measles virus phosphoprotein is required to block STAT1 phosphorylation. Virology 360: 72-83.
113. Ohno S, Ono N, Takeda M, Takeuchi K, Yanagi Y (2004) Dissection of measles virus V protein in relation to its ability to block alpha/beta interferon signal transduction. Journal of General Virology 85: 2991-2999. (Pubitemid 39360043)
114. Komase K, Nakayama T, Iijima M, Miki K, Kawanishi R, et al. (2006) The phosphoprotein of attenuated measles AIK-C vaccine strain contributes to its temperature-sensitive phenotype. Vaccine 24: 826-834. (Pubitemid 43190090)
115. Ito M, Iwasaki M, Takeda M, Nakamura T, Yanagi Y, et al. (2013) Measles virus non-structural C protein modulates viral RNA polymerase activity by interacting with a host protein SHCBP1. J Virol 87: 9633-9642.
116. Sleeman K, Bankamp B, Hummel KB, Lo MK, Bellini WJ, et al. (2008) The C, V and W proteins of Nipah virus inhibit minigenome replication. Journal of General Virology 89: 1300-1308.
117. Kato A, Ohnishi Y, Hishiyama M, Kohase M, Saito S, et al. (2002) The amino-terminal half of Sendai virus C protein is not responsible for either counteracting the antiviral action of interferons or down-regulating viral RNA synthesis. J Virol 76: 7114-7124. (Pubitemid 41246225)
118. Grogan CC, Moyer SA (2001) Sendai virus wild-type and mutant C proteins show a direct correlation between L polymerase binding and inhibition of viral RNA synthesis. Virology 288: 96-108. (Pubitemid 32846478)
119. Caignard G, Komarova AV, Bourai M, Mourez T, Jacob Y, et al. (2009) Differential regulation of type I interferon and epidermal growth factor pathways by a human Respirovirus virulence factor. PLoS Pathog 5: e1000587.
120. Irie T, Yoshida A, Sakaguchi T (2013) Clustered Basic Amino Acids of the Small Sendai Virus C Protein Y1 Are Critical to Its Ran GTPase-Mediated Nuclear Localization. PLoS One 8: e73740.
121. Mao H, Chattopadhyay S, Banerjee AK (2010) Domain within the C protein of human parainfluenza virus type 3 that regulates interferon signaling. Gene Expr 15: 43-50.
122. Mao H, Chattopadhyay S, Banerjee AK (2009) N-terminally truncated C protein, CNDelta25, of human parainfluenza virus type 3 is a potent inhibitor of viral replication. Virology 394: 143-148.
123. Iakoucheva LM, Kimzey AL, Masselon CD, Smith RD, Dunker AK, et al. (2001) Aberrant mobility phenomena of the DNA repair protein XPA. Protein Sci 10: 1353-1362. (Pubitemid 32568102)
124. Kelly SM, Jess TJ, Price NC (2005) How to study proteins by circular dichroism. Biochimica Et Biophysica Acta-Proteins and Proteomics 1751: 119-139. (Pubitemid 41112231)
125. de Breyne S, Stalder R, Curran J (2005) Intracellular processing of the Sendai virus C' protein leads to the generation of a Y protein module: structure-functional implications. FEBS Lett 579: 5685-5690. (Pubitemid 41455649)
126. Wilkins DK, Grimshaw SB, Receveur V, Dobson CM, Jones JA, et al. (1999) Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques. Biochemistry 38: 16424-16431.
127. Kato A, Kiyotani K, Kubota T, Yoshida T, Tashiro M, et al. (2007) Importance of the anti-interferon capacity of Sendai virus C protein for pathogenicity in mice. J Virol 81: 3264-3271. (Pubitemid 46456635)
128. Sweetman DA, Miskin J, Baron MD (2001) Rinderpest virus C and V proteins interact with the major (L) component of the viral polymerase. Virology 281: 193-204. (Pubitemid 32881136)
129. Yamaguchi M, Kitagawa Y, Zhou M, Itoh M, Gotoh B (2014) An anti-interferon activity shared by paramyxovirus C proteins: Inhibition of Toll-like receptor 7/9-dependent alpha interferon induction. FEBS Lett 588: 28-34.
130. Jordan IK, Sutter BAT, McClure MA (2000) Molecular evolution of the Paramyxoviridae and Rhabdoviridae multiple-protein-encoding P gene. Mol Biol Evol 17: 75-86.
131. Pavesi A, Magiorkinis G, Karlin DG (2013) Viral proteins originated de novo by overprinting can be identified by codon usage: application to the "gene nursery" of deltaretroviruses. Plos Computational Biology 9: e1003162.
132. Curran J, Boeck R, Kolakofsky D (1991) The Sendai virus P gene expresses both an essential protein and an inhibitor of RNA synthesis by shuffling modules via mRNA editing. EMBO J 10: 3079-3085. (Pubitemid 21905328)
133. Kurotani A, Kiyotani K, Kato A, Shioda T, Sakai Y, et al. (1998) Sendai virus C proteins are categorically nonessential gene products but silencing their expression severely impairs viral replication and pathogenesis. Genes Cells 3: 111-124. (Pubitemid 28383639)
134. Radecke F, Billeter MA (1996) The nonstructural C protein is not essential for multiplication of Edmonston B strain measles virus in cultured cells. Virology 217: 418-421. (Pubitemid 26104601)
135. Leyrat C, Gerard FC, de Almeida Ribeiro E, Jr., Ivanov I, Ruigrok RW, et al. (2010) Structural disorder in proteins of the rhabdoviridae replication complex. Protein Pept Lett 17: 979-987.
136. Curran J, Marq JB, Kolakofsky D (1995) An N-Terminal Domain of the Sendai Paramyxovirus P-Protein Acts as a Chaperone for the Np Protein during the Nascent Chain Assembly Step of Genome Replication. Journal of Virology 69: 849-855.
137. Chen M, Ogino T, Banerjee AK (2007) Interaction of vesicular stomatitis virus P and N proteins: identification of two overlapping domains at the N terminus of P that are involved in N0-P complex formation and encapsidation of viral genome RNA. J Virol 81: 13478-13485. (Pubitemid 350247842)
138. Mavrakis M, Mehouas S, Real E, Iseni F, Blondel D, et al. (2006) Rabies virus chaperone: Identification of the phosphoprotein peptide that keeps nucleoprotein soluble and free from non-specific RNA. Virology 349: 422-429. (Pubitemid 43782869)
139. Shaji D, Shaila MS (1999) Domains of Rinderpest virus phosphoprotein involved in interaction with itself and the nucleocapsid protein. Virology 258: 415-424. (Pubitemid 29390251)
140. Shaw ML, Garcia-Sastre A, Palese P, Basler CF (2004) Nipah virus V and W proteins have a common STAT1-binding domain yet inhibit STAT1 activation from the cytoplasmic and nuclear compartments, respectively. J Virol 78: 5633-5641. (Pubitemid 38661650)
141. Devaux P, Priniski L, Cattaneo R (2013) The measles virus phosphoprotein interacts with the linker domain of STAT1. Virology 444: 250-256.
142. Fujii Y, Kiyotani K, Yoshida T, Sakaguchi T (2001) Conserved and non-conserved regions in the Sendai virus genome: evolution of a gene possessing overlapping reading frames. Virus Genes 22: 47-52. (Pubitemid 32108376)
143. Guyader S, Ducray DG (2002) Sequence analysis of Potato leafroll virus isolates reveals genetic stability, major evolutionary events and differential selection pressure between overlapping reading frame products. Journal of General Virology 83: 1799-1807. (Pubitemid 34716289)
144. Narechania A, Terai M, Burk RD (2005) Overlapping reading frames in closely related human papillomaviruses result in modular rates of selection within E2. J Gen Virol 86: 1307-1313. (Pubitemid 40613247)
145. Pavesi A (2006) Origin and evolution of overlapping genes in the family Microviridae. Journal of General Virology 87: 1013-1017.
146. Torres C, Fernandez MD, Flichman DM, Campos RH, Mbayed VA (2013) Influence of overlapping genes on the evolution of human hepatitis B virus. Virology 441: 40-48.
147. Peleg O, Kirzhner V, Trifonov E, Bolshoy A (2004) Overlapping messages and survivability. J Mol Evol 59: 520-527. (Pubitemid 39305143)
148. Sanjuan R, Nebot MR, Chirico N, Mansky LM, Belshaw R (2010) Viral mutation rates. J Virol 84: 9733-9748.
149. Chen P, Gan Y, Han N, Fang W, Li J, et al. (2013) Computational evolutionary analysis of the overlapped surface (S) and polymerase (P) region in hepatitis B virus indicates the spacer domain in P is crucial for survival. PLoS One 8: e60098.
150. Cento V, Mirabelli C, Dimonte S, Salpini R, Han Y, et al. (2013) Overlapping structure of hepatitis B virus (HBV) genome and immune selection pressure are critical forces modulating HBV evolution. Journal of General Virology 94: 143-149.
151. Kawano Y, Neeley S, Adachi K, Nakai H (2013) An experimental and computational evolution-based method to study a mode of co-evolution of overlapping open reading frames in the AAV2 viral genome. PLoS One 8: e66211.
152. Parks CL, Witko SE, Kotash C, Lin SL, Sidhu MS, et al. (2006) Role of V protein RNA binding in inhibition of measles virus minigenome replication. Virology 348: 96-106.
153. Bartlett EJ, Amaro-Carambot E, Surman SR, Collins PL, Murphy BR, et al. (2006) Introducing point and deletion mutations into the P/C gene of human parainfluenza virus type 1 (HPIV1) by reverse genetics generates attenuated and efficacious vaccine candidates. Vaccine 24: 2674-2684. (Pubitemid 43290400)
154. Garcin D, Itoh M, Kolakofsky D (1997) A point mutation in the sendai virus accessory C proteins attenuates virulence for mice, but not virus growth in cell culture. Virology 238: 424-431. (Pubitemid 28218159)
155. Durbin AP, McAuliffe JM, Collins PL, Murphy BR (1999) Mutations in the C, D, and V open reading frames of human parainfluenza virus type 3 attenuate replication in rodents and primates. Virology 261: 319-330. (Pubitemid 29431784)
156. Nishie T, Nagata K, Takeuchi K (2007) The C protein of wild-type measles virus has the ability to shuttle between the nucleus and the cytoplasm. Microbes Infect 9: 344-354. (Pubitemid 46341935)
157. Bartlett EJ, Amaro-Carambot E, Surman SR, Newman JT, Collins PL, et al. (2005) Human parainfluenza virus type I (HPIV1) vaccine candidates designed by reverse genetics are attenuated and efficacious in African green monkeys. Vaccine 23: 4631-4646. (Pubitemid 41132813)