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Comparative antiviral and proviral factors in semen and vaccines for preventing viral dissemination from the male reproductive tract and semen

Published online by Cambridge University Press:  19 March 2008

Jane Christopher-Hennings*
Affiliation:
Veterinary Science Department, Center for Infectious Disease Research and Vaccinology, South Dakota State University, Brookings, SD 57007-1396, USA
Eric A. Nelson
Affiliation:
Veterinary Science Department, Center for Infectious Disease Research and Vaccinology, South Dakota State University, Brookings, SD 57007-1396, USA
Gary C. Althouse
Affiliation:
Department of Clinical Studies–New Boltan Center, University of Pennsylvania, Kennett Square, PA 19348, USA
Joan Lunney
Affiliation:
Animal Parasitic Diseases Laboratory, ANRI, ARS, USDA, Building 1040, Room 103, BARC-East, Beltsville, MD 20705, USA
*
*Corresponding author. E-mail: [email protected]

Abstract

Many animal and human viruses are disseminated via semen, but there is little information on how to measure and stimulate protective antiviral immunity in the male reproductive tract and semen. This information is important since successful vaccination through the stimulation of protective immune responses could be a mechanism to prevent viral contamination of semen and subsequent wide spread viral dissemination. Even control of the infection by shortening the duration of viral shedding and lowering the viral load in semen would lessen the chances of viral dissemination through this route. This review will highlight the current knowledge of immunity in the male reproductive tract and summarize ‘antiviral’ as well as ‘proviral’ factors in semen such as cytokines, cells, antibodies, antimicrobial peptides, enzymes, hormones and growth factors. These factors must provide a fine balance between ‘immunosuppression’ in semen needed to protect sperm viability and ‘immunocompetency’ to prevent pathogen contamination. The review will also suggest continuing challenges to researchers for preventing viral dissemination via semen and propose a large animal model for continued research in this important area.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2008

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References

Anderson, DJ and Pudney, J (2005). Human male genital tract immunity and experimental models. In: Mestecky, J, Lamm, ME, Strober, W, Bienenstock, J, McGhee, J and Mayer, L (eds) Mucosal Immunology. Burlington, MA: Elsevier Academic Press, pp. 16471659.CrossRefGoogle Scholar
Anderson, DJ, O'Brien, TR, Politch, JA, Martinez, A, Seage, GR, Padian, N, Horsburgh, CRJ and Mayer, KH (1992). Effects of disease stage and zidovudine therapy on the detection of human immunodeficiency virus type 1 in semen. Journal of the American Medical Association 267: 27692774.CrossRefGoogle Scholar
Anderson, DJ, Politch, JA, Tucker, L, Fichorova, R, Haimovici, RF, Tuomala, R and Mayer, K (1998). Quantitation of mediators of inflammation and immunity in genital tract secretions and their relevance to HIV type 1 transmission. AIDS Research and Human Retroviruses 14: 17.Google ScholarPubMed
Ansari, IH, Kwon, BJ, Osorio, FA and Pattnaik, AK (2006). Influence of N-linked glycosylation of porcine reproductive and respiratory syndrome virus GP5 on virus infectivity, antigenicity, and ability to induce neutralizing antibodies. Journal of Virology 80: 39944004.CrossRefGoogle ScholarPubMed
Balasuriya, U and MacLachlan, NJ (2004). The immune response to equine arteritis virus: potential lessons for other arteriviruses. Veterinary Immunology and Immunopathology 102: 107129.CrossRefGoogle ScholarPubMed
Benfield, DA, Nelson, C, Steffen, M and Rowland, RRR (2000). Transmission of PRRSV by artificial insemination using extended semen seeded with different concentrations of PRRSV. Proceedings of the Annual Meeting of the American Association of Swine Practitioners, pp. 405408.Google Scholar
Berlier, W, Bourlet, T, Levy, R, Lucht, F, Pozzetto, B and Delezay, O (2006). Amount of seminal IL-1 beta positively correlates to HIV-1 load in the semen of infected patients. Journal of Clinical Virology 36: 204207.CrossRefGoogle Scholar
Bjorck, L, Grubb, A and Kjellen, L (1990). Cystatin C, a human proteinase inhibitor, blocks replication of Herpes Simplex Virus. Journal of Virology 64: 941943.CrossRefGoogle ScholarPubMed
Bouhlal, H, Chomont, N, Haeffner-Cavaillon, N, Kazatchkine, M, Belec, L and Hocini, H (2002). Opsonization of HIV-1 by semen complement enhances infection of human epithelial cells. Journal of Immunology 169: 33013306.CrossRefGoogle ScholarPubMed
Butler, JE, Sinkora, M, Wertz, N, Holtmeier, W and Lemke, CD (2006). Development of the neonatal B and T cell repertoire in swine: implications for comparative and veterinary immunology. Veterinary Research 37: 417441.CrossRefGoogle Scholar
Christopher-Hennings, J and Nelson, EA (1997). PCR analysis for the identification of porcine reproductive and respiratory syndrome virus in boar semen. In: Meltzer, SJ (ed) PCR in Bioanalysis. Totowa: Humana Press (Methods in Molecular Biology Series). pp. 8188.Google Scholar
Christopher-Hennings, J, Nelson, EA, Nelson, JK, Hines, RJ, Swenson, SL, Hill, HT, Zimmerman, JJ, Katz, JB, Yaeger, MJ, Chase, CCL and Benfield, DA (1995a). Detection of Porcine Reproductive and Respiratory Syndrome Virus in Boar Semen by PCR. Journal of Clinical Microbiology 33: 17301734.CrossRefGoogle ScholarPubMed
Christopher-Hennings, J, Nelson, EA, Hines, R, Nelson, JK, Swenson, SL, Zimmerman, JJ, Chase, CCL, Yaeger, MJ and Benfield, DA (1995b). Persistence of porcine reproductive and respiratory syndrome virus in serum and semen of adult boars. Journal of Veterinary Diagnostic Investigation 7: 456646.CrossRefGoogle ScholarPubMed
Christopher-Hennings, J, Nelson, EA, Nelson, JK and Benfield, DA (1997). Effects of a modified-live virus vaccine against porcine reproductive and respiratory syndrome in boars. American Journal of Veterinary Research 58: 4045.CrossRefGoogle ScholarPubMed
Christopher-Hennings, J, Nelson, EA, Nelson, JK, Rossow, KR, Rowland, RR, Yaeger, MJ, Chase, CCL, Garduno, R, Collins, JE and Benfield, DA (1998). Identification of porcine reproductive and respiratory syndrome virus in semen and tissues from vasectomized and non-vasectomized boars. Veterinary Pathology 35: 260267.CrossRefGoogle Scholar
Christopher-Hennings, J, Holler, LD, Benfield, DA and Nelson, EA (2001). Detection and duration of porcine reproductive and respiratory syndrome virus in semen, serum, peri-pheral blood mononuclear cells, and tissues from Yorkshire, Hampshire and Landrace boars. Journal of Veterinary Diagnostic Investigation 13: 133142.CrossRefGoogle Scholar
Claus, R (1990). Physiological role of seminal components in the reproductive tract of the female pig. Journal of Reproduction and Fertility (Supplement) 40: 117131.Google ScholarPubMed
Cohen, MS (1998). Sexually transmitted diseases enhance HIV transmission: no longer a hypothesis. Lancet 351: (suppl. 3): 57.CrossRefGoogle ScholarPubMed
Cole, A (2005). Antimicrobial peptide microbicides targeting HIV. Protein and Peptide Letters 12: 4147.CrossRefGoogle ScholarPubMed
Collins, A and Grubb, A (1991). Inhibitory effects of recombinant human cystatin C on human coronaviruses. Antimicrobial agents and Chemotherapy 35: 24442446.CrossRefGoogle ScholarPubMed
Com, E, Bourgeon, F, Evrard, B, Ganz, T, Colleu, D, Jegou, B and Pineau, C (2003). Expression of antimicrobial defensins in the male reproductive tract of rats, mice, and humans. Biology of Reproduction 68: 95104.CrossRefGoogle ScholarPubMed
Coombs, RW, Speck, CE, Hughes, JP, Lee, W, Sampoleo, R, Ross, SO, Dragavon, J, Peterson, G, Hooton, TM, Collier, AC, Corey, L, Koutsky, L and Krieger, JN (1998). Association between culturable human immunodeficiency virus type 1 (HIV-1) in semen and HIV-1 RNA levels in semen and blood: evidence for compartmentalization of HIV-1 between semen and blood. Journal of Infectious Disease 177: 320330.CrossRefGoogle ScholarPubMed
Dawson, HD, Beshah, E, Nishi, S, Solano-Aguilar, G, Morimoto, M, Zhao, A, Madden, KB, Ledbetter, TK, Dubey, JP, Shea-Donohue, T, Lunney, JK and Urban, JF Jr. (2005). Localized multi-gene expression patterns support an evolving Th1/Th2-like paradigm in response to infections with Toxoplasma gondii and Ascaris suum in pigs. Infection and Immunity 73: 11161128.CrossRefGoogle Scholar
Dejucq, N and Jégou, B (2001). Viruses in the mammalian male genital tract and their effects on the reproductive system. Microbiology and Molecular Biology Reviews 65: 208231.CrossRefGoogle ScholarPubMed
Dejucq, N, Chousterman, S and Jėgou, B (1997). The testicular antiviral defense system: localization, expression, and regulation of 2’5’ oligoadenylate synthetase, double-stranded RNA-activated protein kinase and Mx proteins in the rat seminiferous tubule. The Journal of Cell Biology 139: 865873.CrossRefGoogle ScholarPubMed
Faaberg, KS, Hocker, JD, Erdman, MM, Harris, DL, Nelson, EA, Torremorell, M and Plagemann, PG (2006). Neutralizing antibody responses of pigs infected with natural GP5 N-glycan mutants of porcine reproductive and respiratory syndrome virus. Viral Immunology 19: 294304.CrossRefGoogle ScholarPubMed
Fang, Y, Rowland, RRR, Roof, M, Lunney, JK, Christopher-Hennings, J and Nelson, EA (2006a). A full-length cDNA infectious clone of North American Type 1 porcine reproductive and respiratory syndrome virus: expression of green fluorescent protein in the Nsp2 region. Journal of Virology 80: 1144711455.CrossRefGoogle ScholarPubMed
Fang, Y, Faaberg, KS, Christopher-Hennings, J, Rowland, RR, Pattnaik, AK, Osorio, FA and Nelson, EA (2006b). Construction of a European-like type 1 PRRSV full-length cDNA infectious clone identified in the United States. In: Pearlman, S and Holmes, K (eds) The Nidoviruses: The Control of SARS and Other Nidovirus Diseases. New York: Springer Publishers Advances in Experimental Medicine and Biology 581: 605608.CrossRefGoogle Scholar
Fideli, US, Allen, SA, Musonda, R, Trask, S, Hahn, BH, Weiss, H, Mulenga, J, Kasolo, F, Vermund, SH and Aldrovandi, GM (2001). Virologic and immunologic determinants of heterosexual transmission of human immunodeficiency virus type 1 in Africa. AIDS Research and Human Retroviruses 17: 901910.CrossRefGoogle Scholar
Francois-Xavier, M-K, Bélec, L, Dalessio, J, Legoff, J, Grésenguet, G, Mayaud, P, Brown, DW and Morrow, RA (2003). Cervicovaginal neutralizing antibodies to herpes simplex virus (HSV) in women seropositive for HSV types 1 and 2. Clinical and Diagnostic Laboratory Immunology 10: 388393.Google Scholar
Fung, K, Glode, M, Green, S and Duncan, M (2004). A comprehensive characterization of the peptide and protein constituents of human seminal fluid. The prostate 61: 171181.CrossRefGoogle ScholarPubMed
Glaser, A, Chirnside, E, Horzinek, M and de Vries, A (1997). Equine arteritis virus. Theriogenology 47: 12751295.CrossRefGoogle ScholarPubMed
Gopichandran, N, Ekbote, U, Walker, J, Brooke, D and Orsi, N (2006). Multiplex determination of murine seminal fluid cytokine profiles. Reproduction 131: 613621.CrossRefGoogle ScholarPubMed
Gray, R, Li, X, Wawer, Serwadda D, Sewankambo, NK, Wabwire-Mangen, F, Lutalo, T, Kiwanuka, N, Kigozi, G, Nalugoda, F, Meehan, MP, Robb, M and Quinn, TC (2004). Determinants of HIV-1 load in subjects with early and later HIV infections, in a general-population cohort of Rakai Uganda. Journal of Infectious Diseases 189: 12091215.CrossRefGoogle Scholar
Guerin, B and Pozzi, N (2005). Viruses in boar semen: detection and clinical as well as epidemiological consequences regarding disease transmission by artificial insemination. Theriogenology 163: 556572.CrossRefGoogle Scholar
Gupta, P, Leroux, C, Patterson, B, Kingsley, L, Rinaldo, C, Ding, M, Chen, Y, Kulka, K, Buchanan, W, McKeon, B and Montelaroet, R (2000). Human immunodeficiency virus type 1 shedding pattern in semen correlates with the compartmentalization of viral quasi species between blood and semen. Journal of Infectious Diseases 182: 7987.CrossRefGoogle Scholar
Haq, A, Ramma, N and Al-Sedairy, S (1996). Isolation, purification and characterization of human seminal plasma proteins and their immunological behavior in vitro. In: Aboul-Enein, HY (ed) Analytical and Preparative Separation Methods of Biomacromolecules. New York, NY: Mercel Dekker, Chapter 10, pp. 331352.Google Scholar
James, K and Hargreave, T (1984). Immunosuppression by seminal plasma and its possible clinical significance. Immunology Today 5: 357363.CrossRefGoogle ScholarPubMed
Jiborn, T, Abrahamson, M, Wallin, H, Malm, J, Lundwall, A, Gadaleanu, V, Abrahamsson, P-A and Bjartell, A (2004). Cystatin C is highly expressed in the human male reproductive system. Journal of Andrology 25: 564572.CrossRefGoogle ScholarPubMed
Kaiser, T, Christopher-Hennings, J and Nelson, E (2000). Measurement of immunoglobulin G, A and M concentrations in boar seminal plasma. Theriogenology 54: 11711184.CrossRefGoogle Scholar
Kazmi, S, Naglik, J, Sweet, S, Evans, R, O'Shea, S, Banatvala, J and Challacombe, S (2006). Comparison of human immunodeficiency virus type 1-specific inhibitory activities in saliva and other human mucosal fluids. Clinical and Vaccine Immunology 13: 11111118.CrossRefGoogle ScholarPubMed
Kelly, R, Carr, G and Critchley, H (1997). A cytokine switch induced by human seminal plasma. An immune modulation with implications for sexually transmitted disease. Human Reproduction 12: 677681.CrossRefGoogle ScholarPubMed
Keppie, J, Williams, AE, Witt, K and Smith, H (1965). The role of erythritol in the tissue localization of the brucellae. British Journal of Experimental Pathology 46: 104108.Google ScholarPubMed
Kiessling, A (1999). HIV-1 in semen: risks for transmission, disease progression and reproduction. The PRN notebook 4: 912.Google Scholar
Lessard, M, Lepine, M, Matte, J, Palin, M and Laforest, J (2003). Uterine immune reaction and reproductive performance of sows inseminated with extended semen and infused with pooled whole dead sperm. Journal of Animal Science 81: 28182825.CrossRefGoogle Scholar
Lunney, JK (2007). Advances in swine biomedical model genomics. International Journal of Biological Sciences 3: 179184.CrossRefGoogle ScholarPubMed
Lwaleed, BA, Greenfield, R, Stewart, A, Birch, B and Cooper, AJ (2004). Seminal clotting and fibrinolytic balance: a possible physiological role in the male reproductive system. Thrombosis and Haemostasis 92: 752766.Google ScholarPubMed
MacLachlan, N and Balasuriya, U (2006). Equine viral arteritis. In: Pearlman, S and Holmes, K (eds) The Nidovirales: Toward Control of SARS and Other Nidovirus Diseases. Vol. 581. Advances in Experimental Medicine and Biology. New York: Springer Publishers.Google Scholar
Marx, P, Smith, S and Baskin, G (2000). Estrogen protects against vaginal transmission of simian immunodeficiency virus. International Conference on AIDS 13: abstract no. MoOrA227.Google Scholar
Mayer, KH and Anderson, DJ (1995). Heterosexual HIV transmission. Infectious Agents and Disease 4: 273284.Google ScholarPubMed
McCollum, WH, Little, TV, Timoney, PJ and Swerczek, TW (1994). Resistance of castrated male horse to attempted establishment of the carrier state with equine arteritis virus. Journal of Comparative Pathology 111: 383388.CrossRefGoogle ScholarPubMed
Meikle, AW, Dorchuck, RW, Araneo, BA, Stringham, JD, Evans, TG, Spruance, SL and Daynes, RA (1992). The presence of a dehydroepiandrosterone-specific receptor binding complex in murine T cells. The Journal of Steroid Biochemistry and Molecular Biology 42: 293304.CrossRefGoogle ScholarPubMed
Mestecky, J (2006). Humoral immune responses to the human immunodeficiency virus type-1 (HIV-1) in the genital tract compared to other mucosal sites. Journal of Reproductive Immunology 72: 117.CrossRefGoogle Scholar
Mestecky, J, Jackson, S, Moldoveanu, Z, Nesbit, LR, Kulhavy, R, Prince, SJ, Sabbaj, S, Mulligan, MJ and Goepfert, PA (2004). Paucity of antigen specific IgA responses in sera and external secretions of HIV-type 1 infected individuals. AIDS Research in Human Retroviruses 20: 972988.CrossRefGoogle ScholarPubMed
Moldoveanu, Z, Huang, W-Q, Kulhavy, R, Pate, MS and Mestecky, J (2005). Human male genital tract secretions: both mucosal and systemic immune compartments contribute to the humoral immunity. The Journal of Immunology 175: 41274136.CrossRefGoogle Scholar
Münk, C, Ge Wei, G, Yang, O, Waring, AJ, Wang, W, Hong, T, Lehrer, RI, Landau, NR and Cole, AM (2003). The θ-defensin, retrocyclin, inhibits HIV-1 entry. AIDS Research and Human Retroviruses 19: 875881.CrossRefGoogle Scholar
Nielsen, TL, Nielsen, J, Have, P, Bækbo, P, Hoff-Jøorgensen, R and Bøtner, A (1997). Examination of virus shedding in semen from vaccinated and from previously infected boars after experimental challenge with porcine reproductive and respiratory syndrome virus. Veterinary Microbiology 54: 101112.CrossRefGoogle ScholarPubMed
Nocera, M and Chu, T (1993). Transforming growth factor beta as an immunosuppressive protein in human seminal plasma. American Journal of Reproductive Immunology 30: 18.CrossRefGoogle ScholarPubMed
Okinaga, T, Reeves, D and Hurley, D (2005). Suppression of PRRS virus infection by boar seminal plasma. International PRRSV Symposium, Poster no. 69.Google Scholar
Okinaga, T, Yoshii, M, Tsunemitsu, H and Hurley, D (2006). In vitro inhibition and enhancement of PRRSV infection by porcine seminal plasma is not due to the effects of complement. International PRRSV Symposium, Poster no. 34.Google Scholar
Oleksiewicz, MB, Bøtner, A and Normann, P (2001). Semen from boars infected with porcine reproductive and respiratory syndrome virus (PRRSV) contains antibodies against structural as well as nonstructural viral proteins. Veterinary Microbiology 81: 109125.CrossRefGoogle ScholarPubMed
Osorio, FA, Galeota, JA, Nelson, E, Brodersen, B, Doster, A, Wills, R, Zuckermann, F and Laegreid, WW (2002). Passive transfer of virus-specific antibodies confers protection against reproductive failure induced by a virulent strain of porcine reproductive and respiratory syndrome virus and establishes sterilizing immunity. Virology 302: 920.CrossRefGoogle ScholarPubMed
Pandya, IJ and Cohen, J (1985). The leukocytic reaction of the human uterine cervix to spermatozoa. Fertility and Sterility 43: 417421.CrossRefGoogle ScholarPubMed
Peacock, J, Nordone, S, Jackson, S, Liao, H-X, Letvin, N, Yafal, A, Gritz, L, Mazzara, G, Haynes, B and Staats, H (2004). Gender differences in human immunodeficiency virus type 1-specific CD8 responses in the reproductive tract and colon following nasal peptide priming and modified vaccinia virus Ankara boosting. Journal of Virology 78: 1316313172.CrossRefGoogle ScholarPubMed
Pohanka, M, Hampl, R, Sterzl, I and Starka, L (2002). Steroid hormones in human semen with particular respect to dehydroepiandrosterone and its immunomodulatory metabolites. Endocrine Regulations 36: 7986.Google ScholarPubMed
Quinn, TC, Wawer, MJ, Sewankambo, N, Serwadda, D, Li, C, Wabwire-Mangen, F, Meehan, M and Lutalo, T, Gray RH for the Rakai Project Study Group (2000). Viral load and heterosexual transmission of human immunodeficiency virus type 1. New England Journal of Medicine 342: 921929.CrossRefGoogle ScholarPubMed
Schook, L, Beattie, C, Beever, J, Donovan, S, Jamison, R, Zuckermann, F, Niemi, S, Rothschild, M, Rutherford, M and Smith, D (2005). Swine in biomedical research: creating the building blocks of animal models. Animal Biotechnology 16: 183190.CrossRefGoogle ScholarPubMed
Schook, LB and Tumbleson, ME (2004). Advances in Swine in Biomedical Research. 2 Volumes. New York: Springer Publishing Corporation.Google Scholar
Sedor, J, Callahan, H, Perussia, B, Lattime, E and Hirsch, I (1993). Soluble Fcγ RIII (CD16) and immunoglobulin G levels in seminal plasma of men with immunological infertility. Journal of Andrology 14: 187193.CrossRefGoogle Scholar
Selsted, ME and Harwig, SS (1987). Purification, primary structure, and antimicrobial activities of a guinea pig neutrophil defensin. Infection and Immunity 55: 22812286.CrossRefGoogle ScholarPubMed
Sheth, P, Danesh, A, Shahabi, K, Rebbapragada, A, Kovacs, C, Dimayuga, R, Halpenny, R, MacDonald, K, Mazzulli, T, Kelvin, D, Ostrowski, M and Kaul, R (2005). HIV-specific CD8 lymphocytes in semen are not associated with reduced HIV shedding. Journal of Immunology 175: 47894796.CrossRefGoogle Scholar
Shin, J, Torrison, J, Choi, C, Gonzalez, S, Crabo, B and Molitor, T (1997). Monitoring of porcine reproductive and respiratory syndrome virus infection in boars. Veterinary Microbiology 55: 337346.CrossRefGoogle ScholarPubMed
Shugars, D (1999). Endogenous mucosal antiviral factors of the oral cavity. The Journal of Infectious Diseases 179 (suppl. 3): S431S435.CrossRefGoogle ScholarPubMed
Smith, S, Baskin, G and Marx, P (2000). Estrogen protects against vaginal transmission of simian immunodeficiency virus. Journal of Infectious Diseases 182: 708715.CrossRefGoogle ScholarPubMed
Swart, PJ, Kuipers, EM, Smit, C, Van Der Strate, BW, Harmsen, MC and Meijer, DK (1998). Lactoferrin. Antiviral activity of lactoferrin. Advances in Experimental Medicine and Biology 443: 205213.CrossRefGoogle ScholarPubMed
Szabo, R and Short, R (2000). How does male circumcision protect against HIV infection? BMJ (British Medical Journal) 320: 15921594.CrossRefGoogle ScholarPubMed
Thompson, LA, Barratt, CL, Bolton, AE and Cooke, ID (1992). The leukocytic reaction of the human uterine cervix. American Journal of Reproductive Immunology 28: 8589.CrossRefGoogle ScholarPubMed
Timoney, P, Mccollum, W, Roberts, A and McDonald, M (1987). Status of equine viral arteritis in Kentucky, 1985. Journal of the American Veterinary Medical Association 191: 3639.Google ScholarPubMed
van der Meer, FJUM, Turkstra, JA, Knaap, J, Rotier, P, Meloen, RH, Teerts, KJ, Stout, TAE and Colenbrander, B (2001). Immunocastration of stallions: an investigation into the effects of anti-GnRH immunisation on reproductive parameters (preliminary results). Programme of the 3rd International Symposium on Stallion Reproduction (Abstract), p. 45.Google Scholar
Veselsky, L, Holan, V, Zajicova, A, Dostal, J and Zelezna, B (2003). Effects of boar seminal immunosuppressive fraction on production of cytokines by concanavalin A-stimulated spleen cells and on proliferation of B lymphoma cell lines. American Journal of Reproductive Immunology 49: 249254.CrossRefGoogle ScholarPubMed
Vodicka, P, Smetana, K Jr, Dvorankova, B, Emerick, T, Xu, YZ, Ourednik, J, Ourednik, V and Motlik, J (2005). The miniature pig as an animal model in biomedical research. Annals of the New York Academy of Sciences 1049: 161171.CrossRefGoogle ScholarPubMed
Wasilk, A, Callahan, JD, Christopher-Hennings, J, Gay, TA, Fang, Y, Dammen, M, Reos, ME, Torremorell, M, Polson, D, Mellencamp, M, Nelson, EA and Nelson, WM (2004). Detection of U.S., Lelystad, and European-like porcine reproductive and respiratory syndrome viruses and relative quantitation in boar semen and serum samples by real-time PCR. Journal of Clinical Microbiology 42: 44534461.CrossRefGoogle ScholarPubMed
Whittall, J and Parkhouse, R (1997). Changes in swine macrophage phenotype after infection with African swine fever virus: cytokine production and responsiveness to interferon gamma and lipopolysaccharide. Immunology 91: 444449.CrossRefGoogle ScholarPubMed
Wolff, H and Anderson, DJ (1988). Male genital tract inflammation associated with increased numbers of potential human immunodeficiency virus host cells in semen. Andrologia 20: 404410.CrossRefGoogle ScholarPubMed
Xu, C, Politch, JA, Tucker, L, Mayer, KH, Seage, GR and Anderson, DJ (1997). Factors associated with increased levels of human immunodeficiency virus type 1 DNA in semen. Journal of Infectious Diseases 176: 941947.CrossRefGoogle ScholarPubMed
Yamashita, T and Saito, K (1989). Purification, primary structure, and biological activity of guinea pig neutrophil cationic peptides. Infection and Immunity 57: 24052409.CrossRefGoogle ScholarPubMed
Yoo, D, Welch, SK, Lee, C and Calvert, JG (2004). Infectious cDNA clones of porcine reproductive and respiratory syndrome virus and their potential as vaccine vectors. Veterinary Immunology and Immunopathology 102: 143154.CrossRefGoogle ScholarPubMed
Zhang, L, Ribeiro, RM, Mascola, JR, Lewis, MG, Stiegler, G, Katinger, H, Perelson, AS and Davenport, MP (2004). Effects of antibody on viral kinetics in simian/human immunodeficiency virus infection: implications for vaccination. Journal of Virology 78: 55205522.CrossRefGoogle ScholarPubMed