PRRSV receptors and their roles in virus infection

Archives of Microbiology

Volumn 197, Issue 4, 2015, Pages 503-512

  Shi, Chongxu ^a   Liu, Yali ^a   Ding, Yaozhong ^a   Zhang, Yongguang ^a   Zhang, Jie ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

CD151; CD163; Heparin sulfate; PRRSV; Receptors; Sialoadhesin; Vimentin

Indexed keywords

VIRUS RECEPTOR;

ANIMAL; BIOSYNTHESIS; CELL LINE; CHLOROCEBUS AETHIOPS; ENDOCYTOSIS; GENETICS; LUNG ALVEOLUS MACROPHAGE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PIG; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS; SWINE DISEASE; VIROLOGY; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS UNCOATING;

ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; ENDOCYTOSIS; MACROPHAGES, ALVEOLAR; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; RECEPTORS, VIRUS; SWINE; SWINE DISEASES; VIRUS ATTACHMENT; VIRUS INTERNALIZATION; VIRUS UNCOATING;

EID: 84939997870     PISSN: 03028933     EISSN: 1432072X     Source Type: Journal    
DOI: 10.1007/s00203-015-1088-1     Document Type: Review

References (55)

1. Cain H, Kraus B, Krauspe R, Osborn M, Weber K (1983) Vimentin filaments in peritoneal macrophages at various stages of differentiation and with altered function. Virchows Arch B Cell Pathol Incl Mol Pathol 42:65–81
2. 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 81:7371–7379. doi:10.1128/jvi.00513-07
3. Chen Y, Guo R, He S, Zhang X, Xia X, Sun H (2014) Additive inhibition of porcine reproductive and respiratory syndrome virus infection with the soluble sialoadhesin and CD163 receptors. Virus Res 179:85–92. doi:10.1016/j.virusres.2013.11.008
4. Christianson HC, Belting M (2014) Heparan sulfate proteoglycan as a cell-surface endocytosis receptor. Matrix Biol 35:51–55. doi:10.1016/j.matbio.2013.10.004
5. Das PB, Dinh PX, Ansari IH, de Lima M, Osorio FA, Pattnaik AK (2010) The minor envelope glycoproteins GP2a and GP4 of porcine reproductive and respiratory syndrome virus interact with the receptor CD163. J Virol 84:1731–1740. doi:10.1128/jvi.01774-09
6. Das PB, Vu HL, Dinh PX, Cooney JL, Kwon B, Osorio FA, Pattnaik AK (2011) Glycosylation of minor envelope glycoproteins of porcine reproductive and respiratory syndrome virus in infectious virus recovery, receptor interaction, and immune response. Virology 410:385–394. doi:10.1016/j.virol.2010.12.002
7. 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 76:4312–4320
8. Delputte PL, Costers S, Nauwynck HJ (2005) Analysis of porcine reproductive and respiratory syndrome virus attachment and internalization: distinctive roles for heparan sulphate and sialoadhesin. J Gen Virol 86:1441–1445. doi:10.1099/vir.0.80675-0
9. Delputte PL, Van Gorp H, Favoreel HW, Hoebeke I, Delrue I, Dewerchin H, Verdonck F, Verhasselt B, Cox E, Nauwynck HJ (2011) Porcine sialoadhesin (CD169/Siglec-1) is an endocytic receptor that allows targeted delivery of toxins and antigens to macrophages. PLoS One 6:e16827. doi:10.1371/journal.pone.0016827
10. Delrue I, Van Gorp H, Van Doorsselaere J, Delputte PL, Nauwynck HJ (2010) Susceptible cell lines for the production of porcine reproductive and respiratory syndrome virus by stable transfection of sialoadhesin and CD163. BMC Biotechnol 10:48. doi:10.1186/1472-6750-10-48
11. Ding Z, Li ZJ, Zhang XD, Li YG, Liu CJ, Zhang YP, Li Y (2012) Proteomic alteration of Marc-145 cells and PAMs after infection by porcine reproductive and respiratory syndrome virus. Vet Immunol Immunopathol 145:206–213. doi:10.1016/j.vetimm.2011.11.005
12. Dokland T (2010) The structural biology of PRRSV. Virus Res 154:86–97. doi:10.1016/j.virusres.2010.07.029
13. Du Y, Pattnaik AK, Song C, Yoo D, Li G (2012) Glycosyl-phosphatidylinositol (GPI)-anchored membrane association of the porcine reproductive and respiratory syndrome virus GP4 glycoprotein and its co-localization with CD163 in lipid rafts. Virology 424:18–32. doi:10.1016/j.virol.2011.12.009
14. Durocher JR, Payne RC, Conrad ME (1975) Role of sialic acid in erythrocyte survival. Blood 45:11–20
15. Fitter S, Sincock PM, Jolliffe CN, Ashman LK (1999) Transmembrane 4 superfamily protein CD151 (PETA-3) associates with beta 1 and alpha IIb beta 3 integrins in haemopoietic cell lines and modulates cell-cell adhesion. Biochem J 338(Pt 1):61–70
16. Frydas IS, Verbeeck M, Cao J, Nauwynck HJ (2013) Replication characteristics of porcine reproductive and respiratory syndrome virus (PRRSV) European subtype 1 (Lelystad) and subtype 3 (Lena) strains in nasal mucosa and cells of the monocytic lineage: indications for the use of new receptors of PRRSV (Lena). Vet Res 44:73. doi:10.1186/1297-9716-44-73
17. Gao L, Guo XK, Wang L, Zhang Q, Li N, Chen XX, Wang Y, Feng WH (2013) MicroRNA 181 suppresses porcine reproductive and respiratory syndrome virus (PRRSV) infection by targeting PRRSV receptor CD163. J Virol 87:8808–8812. doi:10.1128/jvi.00718-13
18. Huang Y, Guo R, Zhang Y, Zhang X, Xia X, Sun H (2013) Establishment of a porcine CD151 transgenic PK-15 cell line susceptible to porcine reproductive and respiratory syndrome virus. Wei Sheng Wu Xue Bao 53:507–514
19. Jiang Y, Khan FA, Pandupuspitasari NS, Kadariya I, Cheng Z, Ren Y, Chen X, Zhou A, Yang L, Kong D, Zhang S (2013) Analysis of the binding sites of porcine sialoadhesin receptor with PRRSV. Int J Mol Sci 14:23955–23979. doi:10.3390/ijms141223955
20. Johnson CR, Griggs TF, Gnanandarajah J, Murtaugh MP (2011) Novel structural protein in porcine reproductive and respiratory syndrome virus encoded by an alternative ORF5 present in all arteriviruses. J Gen Virol 92:1107–1116. doi:10.1099/vir.0.030213-0
21. 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 58:488–491
22. Karniychuk UU, Geldhof M, Vanhee M, Van Doorsselaere J, Saveleva TA, Nauwynck HJ (2010) Pathogenesis and antigenic characterization of a new East European subtype 3 porcine reproductive and respiratory syndrome virus isolate. BMC Vet Res 6:30. doi:10.1186/1746-6148-6-30
23. Kim HS, Kwang J, Yoon IJ, Joo HS, Frey ML (1993) Enhanced replication of porcine reproductive and respiratory syndrome (PRRS) virus in a homogeneous subpopulation of MA-104 cell line. Arch Virol 133:477–483
24. 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 80:689–696. doi:10.1128/jvi.80.2.689-696.2006
25. Kim S, Lee S, Shin J, Kim Y, Evnouchidou I, Kim D, Kim YK, Kim YE, Ahn JH, Riddell SR, Stratikos E, Kim VN, Ahn K (2011) Human cytomegalovirus microRNA miR-US4-1 inhibits CD8(+) T cell responses by targeting the aminopeptidase ERAP1. Nat Immunol 12:984–991. doi:10.1038/ni.2097
26. Kreuger J, Kjellen L (2012) Heparan sulfate biosynthesis: regulation and variability. J Histochem Cytochem 60:898–907. doi:10.1369/0022155412464972
27. Lee YJ, Lee C (2010) Deletion of the cytoplasmic domain of CD163 enhances porcine reproductive and respiratory syndrome virus replication. Arch Virol 155:1319–1323. doi:10.1007/s00705-010-0699-8
28. Leng CL, Tian ZJ, Zhang WC, Zhang HL, Zhai HY, An TQ, Peng JM, Ye C, Sun L, Wang Q, Sun Y, Li L, Zhao HY, Chang D, Cai XH, Zhang GH, Tong GZ (2014) Characterization of two newly emerged isolates of porcine reproductive and respiratory syndrome virus from Northeast China in 2013. Vet Microbiol 171:41–52. doi:10.1016/j.vetmic.2014.03.005
29. Lindahl U, Kjellen L (2013) Pathophysiology of heparan sulphate: many diseases, few drugs. J Intern Med 273:555–571. doi:10.1111/joim.12061
30. Martinez VG, Moestrup SK, Holmskov U, Mollenhauer J, Lozano F (2011) The conserved scavenger receptor cysteine-rich superfamily in therapy and diagnosis. Pharmacol Rev 63:967–1000. doi:10.1124/pr.111.004523
31. Martinez-Pomares L, Gordon S (2012) CD169 + macrophages at the crossroads of antigen presentation. Trends Immunol 33:66–70. doi:10.1016/j.it.2011.11.001
32. Meulenberg JJ, Petersen-den Besten A (1996) Identification and characterization of a sixth structural protein of Lelystad virus: the glycoprotein GP2 encoded by ORF2 is incorporated in virus particles. Virology 225:44–51
33. Meulenberg JJ, Petersen-den Besten A, De Kluyver EP, Moormann RJ, Schaaper WM, Wensvoort G (1995) Characterization of proteins encoded by ORFs 2 to 7 of Lelystad virus. Virology 206:155–163
34. Nagamine S, Tamba M, Ishimine H, Araki K, Shiomi K, Okada T, Ohto T, Kunita S, Takahashi S, Wismans RG, van Kuppevelt TH, Masu M, Keino-Masu K (2012) Organ-specific sulfation patterns of heparan sulfate generated by extracellular sulfatases Sulf1 and Sulf2 in mice. J Biol Chem 287:9579–9590. doi:10.1074/jbc.M111.290262
35. Nieuwenhuis N, Duinhof TF, van Nes A (2012) Economic analysis of outbreaks of porcine reproductive and respiratory syndrome virus in nine sow herds. Vet Rec 170:225. doi:10.1136/vr.100101
36. O’Neill AS, van den Berg TK, Mullen GE (2013) Sialoadhesin—a macrophage-restricted marker of immunoregulation and inflammation. Immunology 138:198–207. doi:10.1111/imm.12042
37. Patton JB, Rowland RR, Yoo D, Chang KO (2009) Modulation of CD163 receptor expression and replication of porcine reproductive and respiratory syndrome virus in porcine macrophages. Virus Res 140:161–171. doi:10.1016/j.virusres.2008.12.002
38. Peterson SB, Liu J (2010) Unraveling the specificity of heparanase utilizing synthetic substrates. J Biol Chem 285:14504–14513. doi:10.1074/jbc.M110.104166
39. Prather RS, Rowland RR, Ewen C, Trible B, Kerrigan M, Bawa B, Teson JM, Mao J, Lee K, Samuel MS, Whitworth KM, Murphy CN, Egen T, Green JA (2013) An intact sialoadhesin (Sn/SIGLEC1/CD169) is not required for attachment/internalization of the porcine reproductive and respiratory syndrome virus. J Virol 87:9538–9546. doi:10.1128/jvi.00177-13
40. Provost C, Jia JJ, Music N, Lévesque C, Lebel MÈ, del Castillo JR, Jacques M, Gagnon CA (2012) Identification of a new cell line permissive to porcine reproductive and respiratory syndrome virus infection and replication which is phenotypically distinct from MARC-145 cell line. Virol J 9:267. doi:10.1186/1743-422x-9-267
41. Robinson SR, Figueiredo MC, Abrahante JE, Murtaugh MP (2013) Immune response to ORF5a protein immunization is not protective against porcine reproductive and respiratory syndrome virus infection. Vet Microbiol 164:281–285. doi:10.1016/j.vetmic.2013.03.006
42. Shanmukhappa K, Kim JK, Kapil S (2007) Role of CD151, A tetraspanin, in porcine reproductive and respiratory syndrome virus infection. Virol J 4:62. doi:10.1186/1743-422x-4-62
43. Simon Davis DA, Parish CR (2013) Heparan sulfate: a ubiquitous glycosaminoglycan with multiple roles in immunity. Front Immunol 4:470. doi:10.3389/fimmu.2013.00470
44. Sincock PM, Fitter S, Parton RG, Berndt MC, Gamble JR, Ashman LK (1999) PETA-3/CD151, a member of the transmembrane 4 superfamily, is localised to the plasma membrane and endocytic system of endothelial cells, associates with multiple integrins and modulates cell function. J Cell Sci 112(Pt 6):833–844
45. Stadejek T, Stankevicius A, Murtaugh MP, Oleksiewicz MB (2013) Molecular evolution of PRRSV in Europe: current state of play. Vet Microbiol 165:21–28. doi:10.1016/j.vetmic.2013.02.029
46. Tian K, Yu X, Zhao T, Feng Y, Cao Z, Wang C, Hu Y, Chen X, Hu D, Tian X, Liu D, Zhang S, Deng X, Ding Y, Yang L, Zhang Y, Xiao H, Qiao M, Wang B, Hou L, Wang X, Yang X, Kang L, Sun M, Jin P, Wang S, Kitamura Y, Yan J, Gao GF (2007) Emergence of fatal PRRSV variants: unparalleled outbreaks of atypical PRRS in China and molecular dissection of the unique hallmark. PLoS One 2:e526. doi:10.1371/journal.pone.0000526
47. Van Breedam W, Verbeeck M, Christiaens I, Van Gorp H, Nauwynck HJ (2013) Porcine, murine and human sialoadhesin (Sn/Siglec-1/CD169): portals for porcine reproductive and respiratory syndrome virus entry into target cells. J Gen Virol 94:1955–1960. doi:10.1099/vir.0.053082-0
48. Van Gorp H, Van Breedam W, Van Doorsselaere J, Delputte PL, Nauwynck HJ (2010) Identification of the CD163 protein domains involved in infection of the porcine reproductive and respiratory syndrome virus. J Virol 84:3101–3105. doi:10.1128/jvi.02093-09
49. Vanderheijden N et al (2003) Involvement of sialoadhesin in entry of porcine reproductive and respiratory syndrome virus into porcine alveolar macrophages. J Virol 77:8207–8215
50. Wang L, Zhang H, Suo X, Zheng S, Feng WH (2011a) Increase of CD163 but not sialoadhesin on cultured peripheral blood monocytes is coordinated with enhanced susceptibility to porcine reproductive and respiratory syndrome virus infection. Vet Immunol Immunopathol 141:209–220. doi:10.1016/j.vetimm.2011.03.001
51. Wang WW, Zhang L, Ma XC, Gao JM, Xiao YH, Zhou EM (2011b) The role of vimentin during PRRSV infection of Marc-145 cells. Bing Du Xue Bao 27:456–461
52. Wang F, Qiu H, Zhang Q, Peng Z, Liu B (2012) Association of two porcine reproductive and respiratory syndrome virus (PRRSV) receptor genes, CD163 and SN with immune traits. Mol Biol Rep 39:3971–3976. doi:10.1007/s11033-011-1177-4
53. Weiland E, Wieczorek-Krohmer M, Kohl D, Conzelmann KK, Weiland F (1999) Monoclonal antibodies to the GP5 of porcine reproductive and respiratory syndrome virus are more effective in virus neutralization than monoclonal antibodies to the GP4. Vet Microbiol 66:171–186
54. Welch SK, Calvert JG (2010) A brief review of CD163 and its role in PRRSV infection. Virus Res 154:98–103. doi:10.1016/j.virusres.2010.07.018
55. Wu J, Peng X, Zhou A, Qiao M, Wu H, Xiao H, Liu G, Zheng X, Zhang S, Mei S (2014) MiR-506 inhibits PRRSV replication in MARC-145 cells via CD151. Mol Cell Biochem 394:275–281. doi:10.1007/s11010-014-2103-6