Porcine arterivirus entry in macrophages: Heparan sulfate-mediated attachment, sialoadhesin-mediated internalization, and a cell-specific factor mediating virus disassembly and genome release

Advances in Experimental Medicine and Biology

Volumn 581, Issue , 2006, Pages 247-252

  Delputte, Peter L ^a   Nauwynck, H J ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84934439557     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-0-387-33012-9_41     Document Type: Conference Paper

References (40)

1. K. D. Rossow, Porcine reproductive and respiratory syndrome, Vet. Pathol. 35, 1 (1998).
2. J. E. Collins, D. A. Benfield, W. T. Christianson, et al., Isolation of swine infertility and respiratory syndrome virus (isolate ATCC VR-2332) in North America and experimental reproduction of the disease in gnotobiotic pigs, J. Vet. Diagn. Invest. 4, 117 (1992).
3. J. J. Meulenberg, M. M. Hulst, E. J. de Meijer, P. L. Moonen, A. den Besten, E. P. de Kluyver, G. Wensvoort, and R. J. Moormann, Lelystad virus belongs to a new virus family, comprising lactate dehydrogenase-elevating virus, equine arteritis virus, and simian hemorrhagic fever virus, Arch. Virol. Suppl. 9, 441 (1994).
4. C. Terpstra, G. Wensvoort, and J. M. Pol, Experimental reproduction of porcine epidemic abortion and respiratory syndrome (mystery swine disease) by infection with Lelystad virus: Koch's postulates fulfilled, Vet. Q. 13, 131 (1991).
5. G. Wensvoort, C. Terpstra, J. M. Pol, et al., Mystery swine disease in The Netherlands: the isolation of Lelystad virus, Vet. Q. 13, 121 (1991).
6. . L. Enjuanes, W. J. Spaan, E. Snijder, and D. Cavanagh, in: Virus Taxonomy. Classification and Nomenclature of Viruses, edited by M. H. V. van Regenmortel, C. M. Fauquet, D. H. L. Bishop, et al. (Academia Press, San Diego, 2000), p. 827.
7. M. A. Mayo, A summary of taxonomic changes recently approved by ICTV, Arch. Virol. 147, 1655 (2002).
8. D. Cavanagh, Nidovirales: a new order comprising Coronaviridae and Arteriviridae, Arch. Virol. 142, 629 (1997).
9. J. J. Meulenberg, M. M. Hulst, E. J. de Meijer, P. L. Moonen, A. den Besten, E. P. de Kluyver, G. Wensvoort, and R. J. Moormann, Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (PEARS), is related to LDV and EAV, Virology 192, 62 (1993).
10. J. J. Meulenberg, A. Petersen-den Besten, E. P. De Kluyver, R. J. Moormann, W. M. Schaaper, and G. Wensvoort, Characterization of proteins encoded by ORFs 2 to 7 of Lelystad virus, Virology 206, 155 (1995).
11. J. J. Meulenberg and A. Petersen-den Besten, 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 (1996).
12. W. H. Wu, Y. Fang, R. Farwell, M. Steffen-Bien, R. R. Rowland, J. Christopher-Hennings, and E. A. Nelson, A 10-kDa structural protein of porcine reproductive and respiratory syndrome virus encoded by ORF2b, Virology 287, 183 (2001).
13. S. Dea, C. A. Gagnon, H. Mardassi, B. Pirzadeh, and D. Rogan, Current knowledge on the structural proteins of porcine reproductive and respiratory syndrome (PRRS) virus: comparison of the North American and European isolates, Arch. Virol. 145, 659 (2000).
14. E. J. Snijder and J. J. M. Meulenberg, in: Fields Virology (4th ed.), edited by D. M. Knipe and P. M. Howley (Lippincott Williams & Wilkins, Philadelphia, 2001), p. 1205.
15. P. G. Plagemann and V. Moennig, Lactate dehydrogenase-elevating virus, equine arteritis virus, and simian hemorrhagic fever virus: a new group of positive-strand RNA viruses, Adv. Virus Res. 41, 99 (1992).
16. E. J. Snijder and J. J. Meulenberg, The molecular biology of arteriviruses, J. Gen. Virol. 79, 961 (1998).
17. J. P. Teifke, M. Dauber, D. Fichtner, M. Lenk, U. Polster, E. Weiland, and J. Beyer, Detection of European porcine reproductive and respiratory syndrome virus in porcine alveolar macrophages by two-colour immunofluorescence and in-situ hybridization-immunohistochemistry double labelling, J. Comp. Pathol. 124, 238 (2001).
18. X. Duan, H. J. Nauwynck, and M. B. Pensaert, Virus quantification and identification of cellular targets in the lungs and lymphoid tissues of pigs at different time intervals after inoculation with porcine reproductive and respiratory syndrome virus (PRRSV), Vet. Microbiol. 56, 9 (1997).
19. X. Duan, H. J. Nauwynck, and M. B. Pensaert, Effects of origin and state of differentiation and activation of monocytes/macrophages on their susceptibility to porcine reproductive and respiratory syndrome virus (PRRSV), Arch. Virol. 142, 2483 (1997).
20. E. M. Bautista, S. M. Goyal, I. J. Yoon, H. S. Joo, and J. E. Collins, Comparison of porcine alveolar macrophages and CL 2621 for the detection of porcine reproductive and respiratory syndrome (PRRS) virus and anti-PRRS antibody, J. Vet. Diagn. Invest. 5, 163 (1993).
21. I. L. Voicu, A. Silim, M. Morin, and M. A. Elazhary, Interaction of porcine reproductive and respiratory syndrome virus with swine monocytes, Vet. Rec. 134, 422 (1994).
22. H. S. Kim, J. Kwang, I. J. Yoon, H. S. Joo, and M. L. Frey, Enhanced replication of porcine reproductive and respiratory syndrome (PRRS) virus in a homogeneous subpopulation of MA-104 cell line, Arch. Virol. 133, 477 (1993).
23. L. C. Kreutz, Cellular membrane factors are the major determinants of porcine reproductive and respiratory syndrome virus tropism, Virus Res. 53, 121 (1998).
24. J. J. Meulenberg, J. N. Bos-de Ruijter, R. van de Graaf, G. Wensvoort, and R. J. Moormann, Infectious transcripts from cloned genome-length cDNA of porcine reproductive and respiratory syndrome virus, J. Virol. 72, 380 (1998).
25. N. Vanderheijden, P. Delputte, H. Nauwynck, and M. Pensaert, Effects of heparin on the entry of porcine reproductive and respiratory syndrome virus into alveolar macrophages, Adv. Exp. Med. Biol. 494, 683 (2001).
26. P. L. Delputte, N. Vanderheijden, H. J. Nauwynck, and M. B. Pensaert, 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 (2002).
27. E. R. Jusa, Y. Inaba, M. Kouno, and O. Hirose, Effect of heparin on infection of cells by porcine reproductive and respiratory syndrome virus, Am. J. Vet. Res. 58, 488 (1997).
28. N. Vanderheijden, P. L. Delputte, H. W. Favoreel, J. Vandekerckhove, J. Van Damme, P. A. van Woensel, and H. J. Nauwynck, Involvement of sialoadhesin in entry of porcine reproductive and respiratory syndrome virus into porcine alveolar macrophages, J. Virol. 77, 8207 (2003).
29. X. Duan, H. J. Nauwynck, H. Favoreel, and M. B. Pensaert, Porcine reproductive and respiratory syndrome virus infection of alveolar macrophages can be blocked by monoclonal antibodies against cell surface antigens, Adv. Exp. Med. Biol. 440, 81 (1998).
30. X. Duan, H. J. Nauwynck, H. W. Favoreel, and M. B. Pensaert, Identification of a putative receptor for porcine reproductive and respiratory syndrome virus on porcine alveolar macrophages, J. Virol. 72, 4520 (1998).
31. P. L. Delputte, S. Costers, and H. J. Nauwynck, Analysis of porcine reproductive and respiratory syndrome virus attachment and internalization: distinctive roles for heparan sulfate and sialoadhesin, J. Gen. Virol. 86, 1441 (2005).
32. H. J. Nauwynck, X. Duan, H. W. Favoreel, P. Van Oostveldt, and M. B. Pensaert, Entry of porcine reproductive and respiratory syndrome virus into porcine alveolar macrophages via receptor-mediated endocytosis, J. Gen. Virol. 80, 297 (1999).
33. Y. Kumamoto, N. Higashi, K. Denda-Nagai, M. Tsuiji, K. Sato, P. R. Crocker, and T. Irimura, Identification of sialoadhesin as a dominant lymph node counter-receptor for mouse macrophage galactose-type C-type lectin 1, J. Biol. Chem. 279, 49274 (2004).
34. A. Hartnell, J. Steel, H. Turley, M. Jones, D. G. Jackson, and P. R. Crocker, Characterization of human sialoadhesin, a sialic acid binding receptor expressed by resident and inflammatory macrophage populations, Blood 97, 288 (2001).
35. P. R. Crocker, S. Kelm, C. Dubois, B. Martin, A. S. McWilliam, D. M. Shotton, J. C. Paulson, and S. Gordon, Purification and properties of sialoadhesin, a sialic acid-binding receptor of murine tissue macrophages, EMBO J. 10, 1661 (1991).
36. P. L. Delputte and H. J. Nauwynck, Porcine arterivirus infection of alveolar macrophages is mediated by sialic acid on the virus, J. Virol. 78, 8094 (2004).
37. L. C. Kreutz, and M. R. Ackermann, Porcine reproductive and respiratory syndrome virus enters cells through a low pH-dependent endocytic pathway, Virus Res. 42, 137 (1996).
38. D. Therrien, Y. St-Pierre, and S. Dea, Preliminary characterization of protein binding factor for porcine reproductive and respiratory syndrome virus on the surface of permissive and non-permissive cells, Arch. Virol. 145, 1099 (2000).
39. D. Therrien, and S. Dea, Monoclonal antibody directed against a membranous protein of MARC-145 cells blocks infection by PRRSV, Adv. Exp. Med. Biol. 494, 395 (2001).
40. E. H. Wissink, H. A. van Wijk, J. M. Pol, G. J. Godeke, P. A. van Rijn, P. J. Rottier, and J. J. Meulenberg, Identification of porcine alveolar macrophage glycoproteins involved in infection of porcine respiratory and reproductive syndrome virus, Arch. Virol. 148, 177 (2003).