Conserved arginine residues in the carboxyl terminus of the equine arteritis virus E protein may play a role in heparin binding but may not affect viral infectivity in equine endothelial cells

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• 作者：Zhengchun Lu ; Sanjay Sarkar ; Jianqiang Zhang…
• 刊名：Archives of Virology
• 出版年：2016
• 出版时间：April 2016
• 年：2016
• 卷：161
• 期：4
• 页码：873-886
• 全文大小：5,109 KB
• 参考文献：1.Asagoe T, Inaba Y, Jusa ER, Kouno M, Uwatoko K, Fukunaga Y (1997) Effect of heparin on infection of cells by equine arteritis virus. J Vet Med Sci 59:727–728CrossRef PubMed
  2.Balasuriya UB, Rossitto PV, DeMaula CD, MacLachlan NJ (1993) A 29K envelope glycoprotein of equine arteritis virus expresses neutralization determinants recognized by murine monoclonal antibodies. J Gen Virol 74(Pt 11):2525–2529CrossRef PubMed
  3.Balasuriya UB, Maclachlan NJ, De Vries AA, Rossitto PV, Rottier PJ (1995) Identification of a neutralization site in the major envelope glycoprotein (GL) of equine arteritis virus. Virology 207:518–527CrossRef PubMed
  4.Balasuriya UB, Snijder EJ, van Dinten LC, Heidner HW, Wilson WD, Hedges JF, Hullinger PJ, MacLachlan NJ (1999) Equine arteritis virus derived from an infectious cDNA clone is attenuated and genetically stable in infected stallions. Virology 260:201–208CrossRef PubMed
  5.Balasuriya UB, Heidner HW, Hedges JF, Williams JC, Davis NL, Johnston RE, MacLachlan NJ (2000) Expression of the two major envelope proteins of equine arteritis virus as a heterodimer is necessary for induction of neutralizing antibodies in mice immunized with recombinant Venezuelan equine encephalitis virus replicon particles. J Virol 74:10623–10630CrossRef PubMed PubMedCentral
  6.Balasuriya UB, Snijder EJ, Heidner HW, Zhang J, Zevenhoven-Dobbe JC, Boone JD, McCollum WH, Timoney PJ, MacLachlan NJ (2007) Development and characterization of an infectious cDNA clone of the virulent Bucyrus strain of Equine arteritis virus. J Gen Virol 88:918–924CrossRef PubMed
  7.Byrnes AP, Griffin DE (1998) Binding of Sindbis virus to cell surface heparan sulfate. J Virol 72:7349–7356PubMed PubMedCentral
  8.Calvert JG, Slade DE, Shields SL, Jolie R, Mannan RM, Ankenbauer RG, Welch SK (2007) CD163 expression confers susceptibility to porcine reproductive and respiratory syndrome viruses. J Virol 81:7371–7379CrossRef PubMed PubMedCentral
  9.Cardin AD, Weintraub HJ (1989) Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 9:21–32CrossRef PubMed
  10.Chen Y, Maguire T, Hileman RE, Fromm JR, Esko JD, Linhardt RJ, Marks RM (1997) Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat Med 3:866–871CrossRef PubMed
  11.Claros MG, von Heijne G (1994) TopPred II: an improved software for membrane protein structure predictions. Comput Appl Biosci 10:685–686PubMed
  12.Compton T, Nowlin DM, Cooper NR (1993) Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology 193:834–841CrossRef PubMed
  13.Connolly SA, Jackson JO, Jardetzky TS, Longnecker R (2011) Fusing structure and function: a structural view of the herpesvirus entry machinery. Nat Rev Microbiol 9:369–381CrossRef PubMed PubMedCentral
  14.Conrad HE (1998) Heparin-binding proteins. Academic, San Diego
  15.de Vries AA, Post SM, Raamsman MJ, Horzinek MC, Rottier PJ (1995) The two major envelope proteins of equine arteritis virus associate into disulfide-linked heterodimers. J Virol 69:4668–4674PubMed PubMedCentral
  16.Delputte PL, Vanderheijden N, Nauwynck HJ, Pensaert MB (2002) Involvement of the matrix protein in attachment of porcine reproductive and respiratory syndrome virus to a heparinlike receptor on porcine alveolar macrophages. J Virol 76:4312–4320CrossRef PubMed PubMedCentral
  17.Delputte PL, Van Breedam W, Delrue I, Oetke C, Crocker PR, Nauwynck HJ (2007) Porcine arterivirus attachment to the macrophage-specific receptor sialoadhesin is dependent on the sialic acid-binding activity of the N-terminal immunoglobulin domain of sialoadhesin. J Virol 81:9546–9550CrossRef PubMed PubMedCentral
  18.den Boon JA, Snijder EJ, Chirnside ED, de Vries AA, Horzinek MC, Spaan WJ (1991) Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily. J Virol 65:2910–2920
  19.Duan X, Nauwynck HJ, Favoreel HW, Pensaert MB (1998) Identification of a putative receptor for porcine reproductive and respiratory syndrome virus on porcine alveolar macrophages. J Virol 72:4520–4523PubMed PubMedCentral
  20.Firth AE, Zevenhoven-Dobbe JC, Wills NM, Go YY, Balasuriya UB, Atkins JF, Snijder EJ, Posthuma CC (2011) Discovery of a small arterivirus gene that overlaps the GP5 coding sequence and is important for virus production. J Gen Virol 92:1097–1106CrossRef PubMed PubMedCentral
  21.Haywood AM (1974) Characteristics of Sendai virus receptors in a model membrane. J Mol Biol 83:427–436CrossRef PubMed
  22.Haywood AM (1994) Virus receptors: binding, adhesion strengthening, and changes in viral structure. J Virol 68:1–5PubMed PubMedCentral
  23.Hedges JF, Demaula CD, Moore BD, McLaughlin BE, Simon SI, MacLachlan NJ (2001) Characterization of equine E-selectin. Immunology 103:498–504CrossRef PubMed PubMedCentral
  24.Huang YW, Dryman BA, Li W, Meng XJ (2009) Porcine DC-SIGN: molecular cloning, gene structure, tissue distribution and binding characteristics. Dev Comp Immunol 33:464–480CrossRef PubMed
  25.Huntington JA, Olson ST, Fan B, Gettins PG (1996) Mechanism of heparin activation of antithrombin. Evidence for reactive center loop preinsertion with expulsion upon heparin binding. Biochemistry 35:8495–8503CrossRef PubMed
  26.Jones DT, Taylor WR, Thornton JM (1994) A model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry 33:3038–3049CrossRef PubMed
  27.Jones DT (2007) Improving the accuracy of transmembrane protein topology prediction using evolutionary information. Bioinformatics 23:538–544CrossRef PubMed
  28.Jusa ER, Inaba Y, Kouno M, Hirose O (1997) Effect of heparin on infection of cells by porcine reproductive and respiratory syndrome virus. Am J Vet Res 58:488–491PubMed
  29.Kim JK, Fahad AM, Shanmukhappa K, Kapil S (2006) Defining the cellular target(s) of porcine reproductive and respiratory syndrome virus blocking monoclonal antibody 7G10. J Virol 80:689–696CrossRef PubMed PubMedCentral
  30.Klimstra WB, Ryman KD, Johnston RE (1998) Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J Virol 72:7357–7366PubMed PubMedCentral
  31.Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580CrossRef PubMed
  32.Krusat T, Streckert HJ (1997) Heparin-dependent attachment of respiratory syncytial virus (RSV) to host cells. Arch Virol 142:1247–1254CrossRef PubMed
  33.Lambert C, Prange R (2001) Dual topology of the hepatitis B virus large envelope protein: determinants influencing post-translational pre-S translocation. J Biol Chem 276:22265–22272CrossRef PubMed
  34.Laquerre S, Argnani R, Anderson DB, Zucchini S, Manservigi R, Glorioso JC (1998) Heparan sulfate proteoglycan binding by herpes simplex virus type 1 glycoproteins B and C, which differ in their contributions to virus attachment, penetration, and cell-to-cell spread. J Virol 72:6119–6130PubMed PubMedCentral
  35.Liu J, Thorp SC (2002) Cell surface heparan sulfate and its roles in assisting viral infections. Med Res Rev 22:1–25CrossRef PubMed
  36.Liu N, Brown DT (1993) Transient translocation of the cytoplasmic (endo) domain of a type I membrane glycoprotein into cellular membranes. J Cell Biol 120:877–883CrossRef PubMed
  37.MacLachlan NJ, Balasuriya UB, Hedges JF, Schweidler TM, McCollum WH, Timoney PJ, Hullinger PJ, Patton JF (1998) Serologic response of horses to the structural proteins of equine arteritis virus. J Vet Diagn Invest 10:229–236CrossRef PubMed
  38.McCollum WH, Timoney PJ (1999) Experimental observation on the virulence of isolates of equine arteritis virus. In: 8th international conference on equine infectious diseases, Dubai, pp 558–559
  39.McCollum WH, Doll ER, Wilson JC, Cheatham J (1962) Isolation and propagation of equine arteritis virus in monolayer cell cultures of rabbit kidney. Cornell Vet 52:452–458
  40.Moore BD, Balasuriya UB, Hedges JF, MacLachlan NJ (2002) Growth characteristics of a highly virulent, a moderately virulent, and an avirulent strain of equine arteritis virus in primary equine endothelial cells are predictive of their virulence to horses. Virology 298:39–44CrossRef PubMed
  41.Sarkar S, Balasuriya UB, Horohov DW, Chambers TM (2015) Equine herpesvirus-1 suppresses type-I interferon induction in equine endothelial cells. Vet Immunol Immunopathol 167:122–129CrossRef PubMed
  42.Sasisekharan R, Venkataraman G (2000) Heparin and heparan sulfate: biosynthesis, structure and function. Curr Opin Chem Biol 4:626–631CrossRef PubMed
  43.Skehel JJ, Wiley DC (2000) Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69:531–569CrossRef PubMed
  44.Snijder EJ, Wassenaar AL, Spaan WJ (1994) Proteolytic processing of the replicase ORF1a protein of equine arteritis virus. J Virol 68:5755–5764PubMed PubMedCentral
  45.Snijder EJ, Meulenberg JJ (1998) The molecular biology of arteriviruses. J Gen Virol 79(Pt 5):961–979CrossRef PubMed
  46.Snijder EJ, van Tol H, Pedersen KW, Raamsman MJ, de Vries AA (1999) Identification of a novel structural protein of arteriviruses. J Virol 73:6335–6345PubMed PubMedCentral
  47.Snijder EJ, Meulenberg JJ (2001) Arteriviruses. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (eds) Fields virology. Lippincott Williams & Wilkins, Philadelphia, pp 1205–1220
  48.Su CM, Liao CL, Lee YL, Lin YL (2001) Highly sulfated forms of heparin sulfate are involved in japanese encephalitis virus infection. Virology 286:206–215CrossRef PubMed
  49.Swameye I, Schaller H (1997) Dual topology of the large envelope protein of duck hepatitis B virus: determinants preventing pre-S translocation and glycosylation. J Virol 71:9434–9441PubMed PubMedCentral
  50.Thaa B, Kabatek A, Zevenhoven-Dobbe JC, Snijder EJ, Herrmann A, Veit M (2009) Myristoylation of the arterivirus E protein: the fatty acid modification is not essential for membrane association but contributes significantly to virus infectivity. J Gen Virol 90:2704–2712CrossRef PubMed
  51.Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRef PubMed PubMedCentral
  52.Tian D, Wei Z, Zevenhoven-Dobbe JC, Liu R, Tong G, Snijder EJ, Yuan S (2012) Arterivirus minor envelope proteins are a major determinant of viral tropism in cell culture. J Virol 86:3701–3712CrossRef PubMed PubMedCentral
  53.van Aken D, Zevenhoven-Dobbe J, Gorbalenya AE, Snijder EJ (2006) Proteolytic maturation of replicase polyprotein pp1a by the nsp4 main proteinase is essential for equine arteritis virus replication and includes internal cleavage of nsp7. J Gen Virol 87:3473–3482CrossRef PubMed
  54.Van Breedam W, Delputte PL, Van Gorp H, Misinzo G, Vanderheijden N, Duan X, Nauwynck HJ (2010) Porcine reproductive and respiratory syndrome virus entry into the porcine macrophage. J Gen Virol 91:1659–1667CrossRef PubMed
  55.van Dinten LC, Rensen S, Gorbalenya AE, Snijder EJ (1999) Proteolytic processing of the open reading frame 1b-encoded part of arterivirus replicase is mediated by nsp4 serine protease and is essential for virus replication. J Virol 73:2027–2037PubMed PubMedCentral
  56.Van Gorp H, Van Breedam W, Delputte PL, Nauwynck HJ (2008) Sialoadhesin and CD163 join forces during entry of the porcine reproductive and respiratory syndrome virus. J Gen Virol 89:2943–2953CrossRef PubMed
  57.Welch SK, Calvert JG (2010) A brief review of CD163 and its role in PRRSV infection. Virus Res 154:98–103CrossRef PubMed
  58.Wieringa R, De Vries AA, Post SM, Rottier PJ (2003) Intra- and intermolecular disulfide bonds of the GP2b glycoprotein of equine arteritis virus: relevance for virus assembly and infectivity. J Virol 77:12996–13004CrossRef PubMed PubMedCentral
  59.Wieringa R, de Vries AA, van der Meulen J, Godeke GJ, Onderwater JJ, van Tol H, Koerten HK, Mommaas AM, Snijder EJ, Rottier PJ (2004) Structural protein requirements in equine arteritis virus assembly. J Virol 78:13019–13027CrossRef PubMed PubMedCentral
  60.Wilson JC, Doll ER, Mc CW, Cheatham J (1962) Propagation of equine arteritis virus previously adapted to cell cultures of equine kidney in monolayer cultures of hamster kidney. Cornell Vet 52:200–205PubMed
  61.WuDunn D, Spear PG (1989) Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J Virol 63:52–58PubMed PubMedCentral
  62.Zevenhoven-Dobbe JC, Greve S, van Tol H, Spaan WJ, Snijder EJ (2004) Rescue of disabled infectious single-cycle (DISC) equine arteritis virus by using complementing cell lines that express minor structural glycoproteins. J Gen Virol 85:3709–3714CrossRef PubMed
  63.Zhang J, Timoney PJ, Maclachlan NJ, Balasuriya UB (2008) Identification of an additional neutralization determinant of equine arteritis virus. Virus Res 138:150–153CrossRef PubMed
  
• 作者单位：Zhengchun Lu (1) (2)
  Sanjay Sarkar (1)
  Jianqiang Zhang (1) (3)
  Udeni B. R. Balasuriya (1)
  
  1. 108 Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, 40546, USA
  2. J. A. Baker Institute for Animal Health, College of Veterinary Medicine, 235 Hungerford Hill Road, Cornell University, Ithaca, NY, 14853, USA
  3. Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, 1600 South 16th St, Ames, IA, 50011, USA
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Biomedicine
  Virology
  Medical Microbiology
  Infectious Diseases
  
• 出版者：Springer Wien
• ISSN：1432-8798

文摘

Equine arteritis virus (EAV), the causative agent of equine viral arteritis, has relatively broad cell tropism in vitro. In horses, EAV primarily replicates in macrophages and endothelial cells of small blood vessels. Until now, neither the cellular receptor(s) nor the mechanism(s) of virus attachment and entry have been determined for this virus. In this study, we investigated the effect of heparin on EAV infection in equine endothelial cells (EECs). Heparin, but not other glycosaminoglycans, could reduce EAV infection up to 93 %. Sequence analysis of the EAV E minor envelope protein revealed a conserved amino acid sequence (₅₂ RSLVARCSRGARYR ₆₅) at the carboxy terminus of the E protein, which was predicted to be the heparin-binding domain. The basic arginine (R) amino acid residues were subsequently mutated to glycine by site-directed mutagenesis of ORF2a in an E protein expression vector and an infectious cDNA clone of EAV. Two single mutations in E (R52G and R57G) did not affect the heparin-binding capability, whereas the E double mutation (R52,60G) completely eliminated the interaction between the E protein and heparin. Although the mutant R52,60G EAV did not bind heparin, the mutations did not completely abolish infectivity, indicating that heparin is not the only critical factor for EAV infection. This also suggested that other viral envelope protein(s) might be involved in attachment through heparin or other cell-surface molecules, and this warrants further investigation.