Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-03T08:31:28.693Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of pulmonary intravascular macrophages in porcine reproductive and respiratory syndrome virus infection

Published online by Cambridge University Press:  28 February 2007

Roongroje Thanawongnuwech ,
Patrick G. Halbur  and
Eileen L. Thacker
Roongroje Thanawongnuwech
Affiliation:
Department of Veterinary Pathology, Chulalongkorn University, Faculty of Veterinary Science, Bangkok 10330, Thailand Veterinary Medical Research Institute, Iowa State University, Ames Iowa 50010USA
Patrick G. Halbur
Affiliation:
Department of Veterinary Diagnostic and Production Animal Medicine, Iowa State University, Ames Iowa 50011, USA
Eileen L. Thacker*
Affiliation:
Veterinary Medical Research Institute, Iowa State University, Ames Iowa 50010USA
*
*Veterinary Medical Research Institute, Iowa State University, 1802 Elwood Drive, Ames, IA 50010, USA E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The objective of this article is to summarize the current state of knowledge of the complex interaction of porcine reproductive and respiratory syndrome virus (PRRSV) and porcine pulmonary intravascular macrophages (PIMs). PIMs play an important role in pulmonary surveillance, and in the past few years we have investigated their role in PRRSV infection. PRRSV antigens and nucleic acids have been demonstrated in PIMs both in vitro and in vivo. Examination of cultured PIMs infected with PRRSV revealed the accumulation of viral particles in the smooth-walled vesicles. PRRSV-infected PIMs in vitro yielded a virus titer similar to pulmonary alveolar macrophages. PRRSV infection induces either apoptosis or cell lysis of PIMs. The in vitro bactericidal activity of PRRSV-infected PIMs is significantly decreased. Phagocytic activity of PIMs, as measured by pulmonary copper clearance, is significantly decreased in PRRSV-infected pigs. This evidence supports the hypothesis that PRRSV-induced damage to PIMs results in increased susceptibility to bacteremic diseases. Recent studies with PRRSV and Streptococcus suis coinfection confirmed that PRRSV predisposes pigs to S. suis infection and bacteremia. These results could explain the increase in bacterial respiratory diseases and septicemias observed in PRRSV-infected pigs.

Type
Research Article
Information
Animal Health Research Reviews , Volume 1 , Issue 2 , December 2000 , pp. 95 - 102
Copyright
Copyright © CAB International 2000

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Atwal, OS and Minhas, K (1992). In vivo interaction of cationised ferritin with the surface coat and endocytosis by pulmonary intravascular macrophages: a tracer kinetic study. Journal of Anatomy 181: 313–325.Google ScholarPubMed
Benfield, DA, Nelson, E, Collins, JE, Harris, L, Goyal, SM, Robinson, D, Christianson, WT, Morrison, RB, Gorcyca, D and Chladek, D (1992). Characterization of swine infertility and respiratory syndrome (SIRS) virus (isolate ATCC VR-2332). Journal of Veterinary Diagnostic Investigation 4: 127–133.CrossRefGoogle ScholarPubMed
Carman, S (1995). Assessment of seropositivity to porcine reproductive and respiratory syndrome (PRRS) virus in swine herds in Ontario 1978 to 1982. Canadian Veterinary Journal 36:776–777.Google ScholarPubMed
Carrasco, L, Gomez-Villamandos, JC and Bautista, MJ (1996). Pulmonary intravascular macrophages in deer. Veterinary Research 27: 71–77.Google ScholarPubMed
Cavanagh, D (1997). Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Archives of Virology 142: 629–633.Google ScholarPubMed
Chang, SW and Ohara, N (1996). Pulmonary intravascular phagocytosis in liver disease. Clinics in Chest Medicine 17: 137–150.CrossRefGoogle ScholarPubMed
Collins, JE, Benfield, DA, Christianson, WT, Harris, L, Henning, JC, Shaw, DP, Goyal, SM, McCullough, S, Morrison, RB, Joo, HS, Gorcyca, D and Chladek, D (1992). Isolation of swine infertility and respiratory syndrome virus (isolate ATCC VR2332) in North America and experimental reproduction of the disease in gnotobiotic pigs. Journal of Veterinary Diagnostic Investigation 4: 117–126.CrossRefGoogle ScholarPubMed
Done, SH and Paton, DJ (1995). Porcine reproductive and respiratory syndrome: clinical disease, pathology and immunosuppression. Veterinary Record 136: 32–35.CrossRefGoogle ScholarPubMed
Drew, TW (1995). Comparative serology of porcine reproductive and respiratory syndrome in eight European laboratories, using immunoperoxidase monolayer assay and enzyme-linked immunosorbent assay. Revue Scientifique et Technique 14: 761–775.CrossRefGoogle ScholarPubMed
Duan, X, Nauwynck, HJ and Pensaert, MB (1997). Effects of origin and state of differentiation and activation of monocytes/macrophages on their susceptibility to porcine reproductive and respiratory syndrome virus (PRRSV). Archives of Virology 142: 2483–2497.CrossRefGoogle ScholarPubMed
Galina, L, Pijoan, C, Sitjar, M, Christianson, WT, Rossow, K and Collins, JE (1994). Interaction between Streptococcus suis serotype 2 and PRRS virus in specific pathogen-free piglets. Veterinary Record 134: 60–64.CrossRefGoogle ScholarPubMed
Gardner, ID and Lawton, JWM (1982). Depressed human monocytes function after influenza infection in vitro. Journal of the Reticuloendothelial Society 32: 443–448.Google ScholarPubMed
Gilbert, SA, Larochelle, R, Magar, R, Cho, HJ and Deregt, D (1997). Typing of porcine reproductive and respiratory syndrome viruses by a multiplex PCR assay. Journal of Clinical Microbiology 35: 264–267.CrossRefGoogle ScholarPubMed
Goyal, SM (1993). Porcine reproductive and respiratory syndrome. Journal of Veterinary Diagnostic Investigation 5: 656–664.CrossRefGoogle ScholarPubMed
Halbur, PG, Paul, PS, Frey, ML, Landgraf, J, Eernisse, K, Meng, X-J, Lum, MA, Andrews, JJ and Rathje, JA (1995 a). Comparison of the pathogenicity of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Veterinary Pathology 32: 648–660.CrossRefGoogle ScholarPubMed
Halbur, PG, Miller, LD, Paul, PS, Meng, X-J, Huffman, EL and Andrews, JJ (1995 b). Immunohistochemical identification of porcine reproductive and respiratory syndrome virus (PRRSV) antigen in the heart and lymphoid system of three-week-old colostrum-deprived pigs. Veterinary Pathology 32: 200–204.CrossRefGoogle ScholarPubMed
Halbur, PG, Paul, PS, Frey, ML, Landgraf, J, Eernisse, K, Meng, X-J, Andrews, JJ, Lum, MA and Rathje, JA (1996 a). Comparison of the antigen distribution of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Veterinary Pathology 33: 159–170.CrossRefGoogle ScholarPubMed
Halbur, PG, Paul, PS, Meng, X-J, Lum, MA, Andrews, JJ and Rathje, JA (1996 b). Comparative pathogenicity of nine US porcine reproductive and respiratory syndrome virus (PRRSV) isolates in a five-week-old cesarean-derived colostrum-deprived pig model. Journal of Veterinary Diagnostic Investigation 8: 11–20.CrossRefGoogle Scholar
Halbur, PG, Rothschild, MF, Thacker, BJ, Meng, X-J, Paul, PS and Bruna, JD (1998). Differences in susceptibility of Duroc, Hampshire, and Meishan pigs to infection with a high virulence strain (VR 2385) of porcine reproductive and respiratory syndrome virus (PRRSV). Journal of Animal Breeding and Genetics 115: 181–189.CrossRefGoogle Scholar
Halbur, PG, Thanawongnuwech, R, Brown, GB, Kinyon, J, Roth, JA, Thacker, EL and Thacker, BJ (2000). Efficacy of antimicrobial treatments and vaccination regimens for control of porcine reproductive and respiratory syndrome virus and Streptococcus suis coinfection of nursery pigs. Journal of Clinical Microbiology 38: 1156–1160.CrossRefGoogle ScholarPubMed
Hayashi, T, Noguchi, Y and Kameyama, Y (1993). Suppression of development of anti-nuclear antibody and glomerulonephritis in NZB x NZW F1 mice by persistent infection with lactic dehydrogenase virus: possible involvement of superoxide anion as a progressive effector. International Journal of Experimental Pathology 74: 553–560.Google Scholar
Kwang, J, Kim, HS and Joo, HS (1994). Cloning, expression and sequence analysis of the ORF 4 gene of the porcine reproductive and respiratory syndrome virus MN-1b. Journal of Veterinary Diagnostic Investigation 6: 293–296.CrossRefGoogle Scholar
Leifsson, PS, Basse, A, Jensen, HE, Bloch, B and Aalbaek, B (1995). Pulmonary intravascular macrophages in the pathogenesis of bovine pulmonary lesions caused by Actinomyces pyogenes. Journal of Comparative Pathology 112: 197–206.CrossRefGoogle ScholarPubMed
Longworth, KE, Westgate, AM, Grady, MK, Westcott, JY and Staub, NC (1992). Development of pulmonary intravascular macrophage function in newborn lambs. Journal of Applied Physiology 73: 2608–2615.CrossRefGoogle ScholarPubMed
Longworth, KE, Albertine, KH and Staub, NC (1996). Ultrastructural quantification of pulmonary intravascular macrophages in newborn and 2-week-old lambs. Anatomical Record 246: 238–244.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
Magar, R, Robinson, Y, Dubuc, C and Larochelle, R (1995). Evaluation of the persistence of porcine reproductive and respiratory syndrome virus in pig carcasses. Veterinary Record 137: 559–561.CrossRefGoogle Scholar
Meng, X-J, Paul, PS, Halbur, PG and Lum, MA (1995). Phylogenetic analyses of the putative M (ORF 6) and N (ORF 7) genes of porcine reproductive and respiratory syndrome virus (PRRSV): implication for the existence of two genotypes of PRRSV in the U.S.A. and Europe. Archives of Virology 140: 745–755.CrossRefGoogle Scholar
Meulenberg, JJM, Hulst, MM, De Meijer, EJ, Moonen, PLJM, Den Besten, A, De Kluyver, EP, Wensvoort, G and Moormann, RJM (1993). Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (PEARS), is related to LDV and EAV. Virology 192: 62–72.CrossRefGoogle ScholarPubMed
Morton, D and Bertram, TA (1988). Isolation and preliminary in vitro characterization of the porcine pulmonary intravascular macrophages. Journal of Leukocyte Biology 43: 403–410.CrossRefGoogle Scholar
Murtaugh, MP, Elam, MR and Kakach, LT (1995). Comparison of the structural protein coding sequences of the VR-2332 and Lelystad virus strains of the PRRS virus. Archives of Virology 140: 1451–1460.CrossRefGoogle ScholarPubMed
Nelson, EA, Christopher-Jennings, J, Drew, T, Wensvoort, G, Collins, JE and Benfield, DA (1993). Differentiation of United States and European isolates of porcine reproductive and respiratory syndrome virus by monoclonal antibodies. Journal of Clinical Microbiology 31: 3184–3189.CrossRefGoogle ScholarPubMed
Oleksiewicz, MB and Nielsen, J (1999). Effect of porcine reproductive and respiratory syndrome virus (PRRSV) on alveolar lung macrophage survival and function. Veterinary Microbiology 66: 15–27.CrossRefGoogle Scholar
Plagemann, PGW and Moenning, V (1992). Lactate dehydrogenase-elevating virus, equine arteritis virus, and simian hemorrhagic fever virus: a new group of positive-strand RNA viruses. Advances in Virus Research 41: 99–192.CrossRefGoogle ScholarPubMed
Pol, JMA, van Dij, JE, Wensvoort, G and Terpstra, C (1991). Pathological, ultrastructural and immunohistological changes caused by Lelystad virus in experimentally induced infection of mystery swine disease (synonym: porcine epidemic abortion and respiratory syndrome (PEARS)). Veterinary Quarterly 13: 137–143.CrossRefGoogle Scholar
Rogers, RA, Tasat, DR, Warner, AE and Brain, JD (1994). Quantitative recovery of pulmonary intravascular macrophages from sheep lungs. Journal of Leukocyte Biology 56: 692–702.CrossRefGoogle ScholarPubMed
Rossow, KD (1998). Porcine reproductive and respiratory syndrome. Veterinary Pathology 35: 1–20.CrossRefGoogle ScholarPubMed
Rossow, KD, Benfield, DA, Goyal, SM, Nelson, EA, Christopher-Hennings, J and Collins, JE (1996). Chronological immunohistochemical detection and localization of porcine reproductive and respiratory syndrome virus in gnotobiotic pigs. Veterinary Pathology 33: 551–556.CrossRefGoogle ScholarPubMed
Rowland, RR, Even, C, Anderson, GW, Chen, C and Plagemann, PGW (1994). Neonatal infection of mice with lactate dehydrogenase-elevating virus results in suppression of humoral antiviral immune response but does not alter the course of viremia or the polyclonal activation of B cells and immune complex formation. Journal of General Virology 75: 1071–1081.CrossRefGoogle ScholarPubMed
Rutherfold, MS, Witsell, A and Schook, LB (1993). Mechanism generating functionally heterogeneous macrophages: chaos revisited. Journal of Leukocyte Biology 53: 602–618.CrossRefGoogle Scholar
Rybicka, K, Daly, BDT, Migliore, JJ and Norman, JC (1974). Intravascular macrophages in normal calf lung: an electron microscopic study. American Journal of Anatomy 139: 353–367.CrossRefGoogle Scholar
Schmitt, CS, Halbur, PG, Roth, JA, Kinyon, JM, Kasorndorkbua, C and Thacker, B (2000). Influence of ampicillin, ceftiofur, attenuated live PRRSV vaccine, and reduced dose Streptococcus suis exposure on disease associated with PRRSV and S. suis co-infection. Veterinary Microbiology 78: 29–37.CrossRefGoogle Scholar
Schneeberger-Kelly, EE and Burger, EJ (1970). Intravascular macrophages in cat lungs after open chest ventilation. Laboratory Investigation 22: 361–369.Google Scholar
Sierra, MA, Carrasco, L, Gomez-Villamandos, JC, de las Mulas, JM, Mendez, A and Jover, A (1990). Pulmonary intravascular macrophages in lungs of pigs inoculated with African swine fever virus of differing virulence. Journal of Comparative Pathology 102: 323–334.CrossRefGoogle ScholarPubMed
Singh, B, Minhas, KJ and Atwal, OS (1994). Ultracytochemical study of multiple dose effect of monastral blue uptake by equine pulmonary intravascular macrophages (PIMs). Journal of Submicroscopic Cytology and Pathology 26: 235–243.Google ScholarPubMed
Sirinarumitr, T, Zhang, Y, Kluge, J, Halbur, PG and Paul, PS (1998). A pneumo-virulent United States isolate of porcine reproductive and respiratory syndrome virus induces apoptosis in bystander cells both in vitro and in vivo. Journal of General Virology 79: 2989–2995.CrossRefGoogle ScholarPubMed
Smith, GF, Constable, PD, Smith, AR, Bacon, CW, Meredith, FI, Wollenberg, GK and Haschek, WM (1996). Effect of fumonisin-containing culture material on pulmonary clearance in swine. American Journal of Veterinary Research 57: 1233–1238.CrossRefGoogle ScholarPubMed
Staub, NC (1989). Pulmonary vascular reactivity: a status report. In: Staub, NC (ed.), The Pulmonary Intravascular Macrophages. Mt Kisco: Futura Publishing, pp. 123–140.Google Scholar
Staub, NC, Nicolaysen, A and Nicolaysen, G (1992). Pulmonary intravascular macrophages in reindeer. FASEB Journal 6: A1242.Google Scholar
Sur, J-H, Cooper, VL, Galeota, JA, Hesse, RA, Doster, AR and Osorio, FA (1996). In vivo detection of porcine reproductive and respiratory syndrome virus RNA by in situ hybridization at different times postinfection. Journal of Clinical Microbiology 34: 2280–2286.CrossRefGoogle ScholarPubMed
Sur, JH, Doster, AR, Christian, JS, Galeota, JA, Wills, RW, Zimmerman, JJ and Osorio, FA (1997). Porcine reproductive and respiratory syndrome virus replicates in testicular germ cells, alters spermatogenesis, and induces germ cell death by apoptosis. Journal of Virology 71: 9170–9179.CrossRefGoogle ScholarPubMed
Thacker, EL, Halbur, PG, Paul, PS and Thacker, BJ (1998). Detection of intracellular porcine reproductive and respiratory syndrome virus nucleocapsid protein in porcine macrophages by flow cytometry. Journal of Veterinary Diagnostic Laboratory Investigation 10: 308–311.CrossRefGoogle ScholarPubMed
Thacker, EL, Halbur, PG, Ross, RF, Thanawongnuwech, R and Thacker, BJ (1999). Mycoplasma hyopneumoniae potentiation of porcine reproductive and respiratory syndrome virus-induced pneumonia. Journal of Clinical Microbiology 37: 620–627.CrossRefGoogle ScholarPubMed
Thanawongnuwech, R, Halbur, PG and Andrews, JJ (1997 a). Immunohistochemical detection of porcine reproductive and respiratory syndrome virus antigen in neurovascular lesions. Journal of Veterinary Diagnostic Investigation 9: 334–337.CrossRefGoogle ScholarPubMed
Thanawongnuwech, R, Thacker, EL and Halbur, PG (1997 b). Effect of porcine reproductive and respiratory syndrome virus (PRRSV) (isolate VR-2385) infection on bactericidal activity of porcine pulmonary intravascular macrophages (PIMs): in vitro comparisons with pulmonary alveolar macrophages (PAMs). Veterinary Immunology and Immunopathology 59: 323–335.CrossRefGoogle ScholarPubMed
Thanawongnuwech, R, Halbur, PG, Ackermann, MR, Thacker, EL and Royer, RL (1998 a). Effects of low (modified-live virus vaccine) and high (VR-2385)-virulence strains of porcine reproductive and respiratory syndrome virus on pulmonary clearance of copper particles in pigs. Veterinary Pathology 35: 398–406.CrossRefGoogle ScholarPubMed
Thanawongnuwech, R, Thacker, EL and Halbur, PG (1998 b). Influence of pig age on virus titer and bactericidal activity of porcine reproductive and respiratory syndrome virus (PRRSV)-infected pulmonary intravascular macrophages (PIMs). Veterinary Microbiology 63:177–187.CrossRefGoogle ScholarPubMed
Thanawongnuwech, R, Brown, GB, Halbur, PG, Roth, JA, Royer, RL and Thacker, BJ (2000). Pathogenesis of porcine reproductive and respiratory syndrome virus-induced increase susceptibility to Streptococcus suis infection. Veterinary Pathology 37: 143–152.CrossRefGoogle ScholarPubMed
Warner, AE (1996). Pulmonary intravascular macrophages: role in acute lung injury. Clinics in Chest Medicine 17: 125–135.CrossRefGoogle ScholarPubMed
Warner, AE and Brain, JD (1984). The ruminant system includes phagocytic intravascular pulmonary macrophages. Journal of Leukocyte Biology 36: 388.Google Scholar
Wensvoort, G, Terpstra, C, Pol, JMA, ter Laak, E, Bloemraad, M, de Kluyver, EP, Kragten, C, van Buiten, L, des Besten, A, Wagnaar, F, Broekhuijsen, JM, Zetstra, PLJMM, de Boer, EA, Tibben, HJ, de Jong, MF, van't Veld, P, Groenland, GJR, van Gennep, JA, Voets, MT, Verheijden, JHM and Braamskamp, J (1991). Mystery swine disease in the Netherlands: the isolation of Lelystad virus. Veterinary Quarterly 13: 121–130.CrossRefGoogle ScholarPubMed
Wensvoort, G, de Kluyver, EP, Luijtze, EA, den Besten, A, Harris, L, Collins, JE, Christianson, WT and Chladek, D (1992). Antigenic comparison of Lelystad virus and swine infertility and respiratory syndrome virus. Journal of Veterinary Diagnostic Investigation 4: 134–138.CrossRefGoogle Scholar
Wills, RW, Gray, JT, Fedorka-Cray, PJ, Yoon, KJ, Ladely, S and Zimmerman, JJ (2000). Synergism between porcine reproductive and respiratory syndrome virus (PRRSV) and Salmonella choleraesuis. Veterinary Microbiology 71: 177–192.CrossRefGoogle ScholarPubMed
Winkler, GC (1988). Pulmonary intravascular macrophages in domestic animal species: review of structural and functional properties. American Journal of Anatomy 181: 217–234.CrossRefGoogle ScholarPubMed
Winkler, GC and Cheville, NF (1985 a). Morphometry of postnatal development in the porcine lung. Anatomical Record 211: 427–433.CrossRefGoogle ScholarPubMed
Winkler, GC and Cheville, NF (1985 b). Monocytic origin and postnatal mitosis of intravascular macrophages in the porcine lung. Journal of Leukocyte Biology 38: 471–480.CrossRefGoogle ScholarPubMed
Yoon, IJ, Joo, HS, Christianson, WT, Kim, HS, Collins, JE, Morrison, RB and Dial, GD (1992). An indirect fluorescent antibody test for the detection of antibody to swine infertility and respiratory syndrome virus in swine sera. Journal of Veterinary Diagnostic Investigation 4: 144–147.CrossRefGoogle ScholarPubMed
Zeman, D, Neiger, R, Yaeger, M, Nelson, E, Benfield, D, Leslie-Steen, P, Thomson, J, Miskimins, D, Daly, R and Minehart, R (1993). Laboratory investigation of PRRS virus infection in three swine herds. Journal of Veterinary Diagnostic Investigation 5: 522–528.CrossRefGoogle ScholarPubMed
Zimmerman, JJ, Yoon, K-J, Wills, RW and Swenson, SL (1997). General overview of PRRSV: a perspective from the United States. Veterinary Microbiology 55: 187–196.CrossRefGoogle ScholarPubMed