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Nonhuman Primate Herpesviruses:Importance for Xenotransplantation

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Xeno-transplantation

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 278))

Abstract

Herpesviruses are found throughout the animal kingdom. Members of this family share properties including a highly orchestrated system of transcription, destruction of the host cell by active viral replication and an ability to persist in the host in a latent form. Human herpesviruses have all been implicated in causing substantial disease after allotransplantation. Often transmission of these viruses has been through the donor organ or blood products. Analogous species of herpesviruses exist in nonhuman primates. Accordingly, concern regarding the risk of their transmission and disease exists with xenotransplant procedures. This chapter reviews herpesviruses of nonhuman primates and their potential implication for causing disease after xenotransplantation.

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References

  • Alcendor DJ, Barry PA, Pratt-Lowe E, Luciw PA (1993) Analysis of the rhesus cytomegalovirus immediate-early gene promoter. Virology 194:815–821

    Article  PubMed  CAS  Google Scholar 

  • Anonymous. (1998) Fatal Cercopithecine herpesvirus 1 (B virus) infection following a mucocutaneous exposure and interim recommendations for worker protection. MMWR 47:1073–1076, 1083

    Google Scholar 

  • Baskin GB (1987) Disseminated cytomegalovirus infection in immunodeficient rhesus monkeys. Am J Pathol 129:345–352

    PubMed  CAS  Google Scholar 

  • Baskin GB, Roberts ED, Kuebler D, Martin LN, Blauw B, Heeney J, Zurcher C (1995) Squamous Epithelial proliferative lesions associated with rhesus Epstein-Barr virus in simian immunodeficiency virus-infected rhesus monkeys. J Infect Dis 172:535–539

    Article  Google Scholar 

  • Blakely GA, Lourie B, Morton WG, Evans HH, Kaufmann AF (1973) A varicella-like disease in macaque monkeys. J Infect Dis 127:617–625

    Article  PubMed  CAS  Google Scholar 

  • Brede HD, Murphy GP. (1972) Bacteriologic and virologic considerations in primate transplants. Primate Med 7:18–28

    Google Scholar 

  • Cen H, Breinig MC, Atchinson RW, Ho M, McKnight JLC (1991) Epstein-Barr virus transmission via the donor organs in solid organ transplantation: polymerase chain reaction and restriction fragment length polymorphism analysis of IR2, IR3 and IR4. J Virol 65:976

    PubMed  CAS  Google Scholar 

  • Chang Y, Cesarman E, Pessin MS et al (1994) Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi_s sarcoma. Science 265:1865–1869

    Article  Google Scholar 

  • Cho Y, Ramer J, Rivailler P, Quink C, Garber RL, Beier DR, Wang F (2001) An Epstein-Barr-related herpesvirus from marmoset lymphomas. Proc Natl Acad Sci USA 98(3):1224–1229

    Article  PubMed  CAS  Google Scholar 

  • Cohen JI, Davenport DS, StewartJA, Deitchman S, Hilliard JK, Chapman LE and the B Virus Workring Group (2002) Recommendations for Prevention of and therapy for exposure to B virus (Cercopithecine Herpesvirus 1). Clin Infect Dis 35:1191–1203

    Article  Google Scholar 

  • Deinhardt F, Falk LA, Wolfe LG. (1973) Simian herpesviruses Cancer Research 33:1424–26

    CAS  Google Scholar 

  • Del Prete G, De Carli M, D’Elios MM, Fleckenstein IM, Fickenscher H, Fleckenstein B, Almerigogna F, Romagnani S (1994) Polyclonal B cell activation induced by herpesvirus saimiri-transformed human CD4+ T cell clones: Roll for membrane TNF-a/TNF-a receptors and CD2/CD58 interactions. J Immun; pp 4872–4879

    Google Scholar 

  • Delmonico FL, Snydman DR (1998) Organ donor screening for infectious diseases. Transplantation 65:603–610

    Article  PubMed  CAS  Google Scholar 

  • Desrosiers RC, Sasseville VG, Czajak SC, Zhang X, Mansfield KG, Kaur A, Johnson RP, Lackner AA, Jung JU (1997) A herpesvirus of rhesus monkeys related to the human Kaposi_s sarcoma-associated herpesvirus. J Virol 71(12):9764–9769

    PubMed  CAS  Google Scholar 

  • Eberle R, Hilliard JK (1984) Replication of simian herpesvirus SA8 and identification of viral polypeptides in infected cells. J Virol 50:316–324

    PubMed  CAS  Google Scholar 

  • Eberle R, Hilliard JK (1989) Serological evidence for variation in the incidence of herpesvirus infections in different species of apes. J Clin Microbiol 27:1357–1366

    PubMed  CAS  Google Scholar 

  • Eberle R, Black DH, Lehenbauer TW, White GL (1998) Shedding and transmission of baboon herpesvirus papio 2 (HPV2) in a breeding colony. Lab Anim Sci 48:23–28

    PubMed  CAS  Google Scholar 

  • Falk L, Deinhardt F, Nonoyama M, Wolfe LG, Bergholf C (1976) Properties of a baboon lymphotropic herpesvirus related to Epstein-Barr virus. Int J Cancer 18:798–807

    Article  PubMed  CAS  Google Scholar 

  • Frances C, Mouquet C, Marcelin AG, et al (2000) Outcome of kidney transplant recipients with previous human herpesvirus-8 infection. Transplantation 69:1776–1779

    Article  PubMed  CAS  Google Scholar 

  • Frank AL, Bissell JA, Rowe DS, Dunnick NR, Mayner RE, Hopps HE, Parkman PD, Meyer HM Jr. (1973) Rhesus leukocyte associated herpesvirus. I. Isolation and 96 M. G. Michaels characterization of a new herpesvirus recovered from rhesus monkey leukocytes.J Infect Dis 128:618–628

    CAS  Google Scholar 

  • Franken M, Annis B, Ali AN, Wang F (1995) 5’coding and regulatory region sequence divergence with conserved function of the Epstein-Barr Virus LMP2A homolog in herpesvirus papio. J Virol 69:8011–8019

    PubMed  CAS  Google Scholar 

  • Freidfeld AG, Hilliard J, Southers J, Murray M, Savarese B, Schmitt JM, Straus SE (1995) A controlled seroprevalence survey of primate handlers for evidence of asymptomatic herpes B virus infection. J Infect Dis 171:1031–1034

    Article  Google Scholar 

  • Gibson W (1983) Protein counterparts of human and simian cytomegaloviruses. Virology 128:391–406

    Article  PubMed  CAS  Google Scholar 

  • Green M, Michaels MG (1997) Infections in solid organ transplant recipients. Principles and Practice of Pediatric Infectious Diseases Eds: Long SS, Pickering L, Prober C, Churchill Livingstone Inc. New York Greensill J, Schultz TF (2000) Rhadinoviruses (gamma-herpesviruses) of Old World primates: models for KSHV/HHV8-associated disease? AIDS 14 (Suppl 3):S11–S19

    Google Scholar 

  • Greensill J, Sheldon JA, Murthy KK, Bessonette JS, Beer BE, Schulz TF (2000) A chimpanzee rhadinovirus sequence related to Kaposi_s sarcoma-associated herpesvirus/human herpesvirus 8: increased detection after HIV-1 infection in the absence of disease. AIDS 14(17):F129–F135

    Article  PubMed  CAS  Google Scholar 

  • Hayashi K, Ohara N, Teramoto N, Onoda S, Chen HL, Oka T, Kondo E, Yoshino T, Takahashi K, Yates J, Akagi T (2001) An animal model for human EBV-associated hemphagocytic syndrome: Herpesvirus papio frequently induces fatal lymphoproliferative disorders with hemophagocytic syndrome in rabbits. Am J Pathol 158:1533–1542

    Article  PubMed  CAS  Google Scholar 

  • Heberling RL, Kalter SS 1986 Rapid dot-immunobinding assay on nitrocellulose for viral antibodies. J Clin Micro 23:109–113

    CAS  Google Scholar 

  • Hilliard JK, Soza I (1996) Rapid identification and differentiation of baboon alphaherpesvirus SA8 from closely related HSV-1 and HSV-2 in xenograft transplant recipients. Molecular Diagnosis 1:261–265

    Article  PubMed  CAS  Google Scholar 

  • Hilliard JK, Ward JA (1999) B-virus specific-pathogen-free breeding colonies of macaques (Macaca mulatta): retrospective study of seven years of testing. Lab Anim Sci 49:144–148

    PubMed  CAS  Google Scholar 

  • Hilliard JK Weigler BJ (1999) Commentary on Smith AL, Black DH, Eberle R. The existence of differing monkey B virus genotypes with possible implications for degree of virulence in humans. J Virol 72:9224–32 Lab Anim Sci 49:9224–32

    CAS  Google Scholar 

  • Hilliard JK, Black D, Eberle R (1989). Simian alphaherpesviruses and their relation to the human herpes simplex virus. Arch Virol 109:83–102

    Article  PubMed  CAS  Google Scholar 

  • Hilliard J, Lachmi B, Soza I, Brasky K, Mirkovic R (1996) PCR identification and differentiation of baboon cytomegalovirus from other human and nonhuman primate cytomegaloviruses. Molecular Diagnosis 1:267–273

    Article  PubMed  CAS  Google Scholar 

  • Ho M (1991) Cytomegalovirus: biology and infection. 2nd edn New York: Plenum Medical Book.

    Google Scholar 

  • Ho M, Miller G, Atchinson RW, et al (1985) Epstein-Barr virus infections and DNA hybridization studies in post-transplantation lymphoma and lymphoproliferative lesions: the role of primary infection. J Infect Dis 152(5):876–886

    Article  PubMed  CAS  Google Scholar 

  • Holmes GP, Hilliard JK, Klontz KC, et al (1990) B virus (herpesvirus simiae) infection in humans: Epidemiological investigation of a cluster. Ann Intern Med 112:833–839

    PubMed  CAS  Google Scholar 

  • Holmes GP, Chapman LE, Stewart JA, et al (1995) Guidelines for the prevention and treatment of B-virus infections in exposed persons. Clin Infect Dis 20:421–439

    Article  PubMed  CAS  Google Scholar 

  • Huang E, Kilpatrick B, Lakeman A, Alford CA (1978) Genetic analysis of a cytomegalovirus-like agent isolated from human brain. J Virol 26:718–723

    PubMed  CAS  Google Scholar 

  • Jenson HB, Ench Y, Gao S-J, Rice K, Carey D, Kennedy RC, Arrand JR, Mackett M (2000) Epidemiology of Herpesvirus Papio infection in a large captive baboon colony: Similarities to Epstein-Barr virus infections in humans. J Infect Dis 181:1462–1466

    Article  PubMed  CAS  Google Scholar 

  • Kalter SS, Heberling RL (1990a) Primate viral diseases in perspective. J Med Primatol 19:519–535

    CAS  Google Scholar 

  • Kalter SS, Heberling RL (1990b) Viral battery testing in nonhuman primate colony management. Lab Anim Sci 40:21–23

    CAS  Google Scholar 

  • Kalter SS, Heberling RL, Ratner JJ (1972) EBV antibody in sera of non-human primates. Nature 238:353–354

    Article  PubMed  CAS  Google Scholar 

  • Kalter SS, Ablashi D, Espana C, Heberling RL, Hull RN, Lennette EH, Malherbe, Mc-Connell S, Yohn DS (1980). Simian virus nomenclature, 1980 Intervirology 13:317–330

    CAS  Google Scholar 

  • Kessler MJ, London WT, Madden DL, Dambrosia JM, Hilliard JK, Soike KF, Rawlins RG (1989) Serological survey for viral diseases in the Cayo Santiago rhesus macaque population. Puerto Rican Health Sci J 8:95–97

    CAS  Google Scholar 

  • Kilpatrick BA, Huang E, Pagano JS (1976) Analysis of cytomegalovirus genomes with restriction endonucleases HinD III and EcoR-1. J Virology 18:1095–1105

    PubMed  CAS  Google Scholar 

  • Lacoste V, Mauclere P, Dubreuil G, Lewis J, Georges-Courbot MC, Gessain A (2000) Virology: KSHV-like herpesviruses in chimps and gorillas. Nature 407:151–152

    Article  PubMed  CAS  Google Scholar 

  • Lacoste V, Mauclere P, Dubreuil G, Lewis J, Georges-Courbot MC, Gessain A (2001) A novel gamma 2-herpesvirus of the Rhadinovirus 2 lineage in chimpanzees. Genome Research 11(9):1511–1519

    Article  PubMed  CAS  Google Scholar 

  • Levin JL, Hilliard JK, Lipper SL, Butler TM, Goodwin WJ (1988) A naturally occurring epizootic of Simian Agent 8 in the baboon. Lab Anim Sci 38:394–397

    PubMed  CAS  Google Scholar 

  • Li SL, Feichtinger H, Kaaya E, Migliorini P, Putkonen P, Biberfeld G, Middeldorp JM, Biberfeld P, Ernberg I (1993) Expression of Epstein-Barr-virus-related nuclear antigens and B-cell markers in lymphomas of SIV-immunosuppressed monkeys. Int J Cancer 55(4):609–615

    Article  PubMed  CAS  Google Scholar 

  • Ling PD, Ryon JJ, Hayward SD (1993) EBNA-2 of herpesvirus papio diverges significantly from the type A and type B EBNA-2 proteins of Epstein-Barr Virus but retains an efficient transactivation domain with a conserved hydrophobic motif. J Virol 67:2990–3003

    PubMed  CAS  Google Scholar 

  • London WT, Marinez AJ, Houff SA, Wallen WC, Curfman BL, Traub RB, Sever JL (1986) Experimental congenital disease with simian cytomegaloviruses in rhesus monkeys. Teratology 33:323–331

    Article  PubMed  CAS  Google Scholar 

  • Martin WJ (1996) Simian cytomegalovirus-related stealth virus isolated from the cerebrospinal fluid of a patient with bipolar psychosis and acute encephalopathy.Pathobiology 64:64–66

    Article  PubMed  CAS  Google Scholar 

  • Martin WJ, Zen LC, Ahmed K, Roy M (1994) Cytomegalovirus-related sequence in an atypical cytopathic virus repeatedly isolated from a patient with chronic fatigue syndrome. Am J Pathol 145(2):440–451

    PubMed  CAS  Google Scholar 

  • Martin WJ, Ahmed K, Zeng LC, Olsen JC, Seward JG, Seehrai JS (1995) African green monkey origin of the atypical cytopathic _stealth virus_ isolated from a patient with chronic fatigue syndrome. Clin and Diag Virol 4:93–103

    Article  CAS  Google Scholar 

  • Martino MA, Hubbard GB, Butler TM, Hilliard JK (1998) Clinical disease associated with simian agent 8 infection in the baboon. Lab Anim Sci 48:18–22

    PubMed  CAS  Google Scholar 

  • McCarthy K, Tosolini FA (1975) A review of primate herpes virus. Proc Roy Soc Med 68:145–149

    PubMed  CAS  Google Scholar 

  • McCarthy K, Thorpe E, Laursen AC, Heymann CS, Beale AJ (1968) Examatous disease in patas monkeys caused by a herpesvirus. Lancet 856–857

    Google Scholar 

  • Mendez JC, Dockrell DH, Espy MJ, et al (2001) Human beta herpesvirus interactions in solid organ transplant recipients. J Infect Dis 183:179–184

    Article  PubMed  CAS  Google Scholar 

  • Michaels MG, Simmons RL (1994) Xenotransplant associated zoonoses: strategies for prevention. Transplantation, 57:1–7

    Article  PubMed  CAS  Google Scholar 

  • Michaels MG, McMichael J, Brasky K, et al (1994) Screening donors for xenotransplantation: the potential for xenozoonoses. Transplantation 57:1462–1465

    PubMed  CAS  Google Scholar 

  • Michaels MG, Hilliard J, Deeks S, et al (1996) Baboon bone marrow xenotransplant in a patient with advanced HIV: A model for the evaluation of potential xenozoonoses. Institute of Human Virology Annual Meeting, Baltimore, MD. Acquired Immune Deficiency Syndromes and Human Retrovirology, Abstract #11, p 3

    Google Scholar 

  • Michaels MG, Alcendor DJ, St George K, et al (1997) Distinguishing baboon cytomegalovirus from human cytomegalovirus: importance for xenotransplantation. J Infect Dis 176:1476–1483

    Article  PubMed  CAS  Google Scholar 

  • Michaels MG, Jenkins FJ, St George K, Nalesnik MA, Starzl TE, Rinaldo CR Jr (2001) Detection of infectious baboon cytomegalovirus after baboon-to-human liver xenotransplantation. J Virol 75:2825–2828

    Article  PubMed  CAS  Google Scholar 

  • Moghaddam A, Koch J, Annis B, Wang F (1998) Infection of human B lymphocytes with lymphocryptoviruses related to Epstein-Barr virus. J Virol 72:3205–3212

    PubMed  CAS  Google Scholar 

  • Moore PS, Chang Y (2001) Kaposi’s Sarcoma - Associated Herpesvirus. In Fields Virology, 4th edn Knipe DM, Howley PM. eds Lippincott Williams &Wilkins Philadelphia. Chapter 82 pp 2835

    Google Scholar 

  • Muchmore E (1971) Possible cytomegalovirus infection in man following chimpanzee bite. Lab Anim Sci 21(6 II):1080–1081

    PubMed  CAS  Google Scholar 

  • Neubauer RH, Rabin H, Strnad BC, Lapin BA, Yakovleva LA, Indzie E (1979) Antibody responses to herpesvirus papio antigens in baboons with lymphoma. Int J Cancer 23:186–192

    Article  PubMed  CAS  Google Scholar 

  • Ohtaki S, Kodama H, Hondo R, Kurata T (1986) Activation of cytomegalovirus infection in immunosuppressed cynomologous monkeys inoculated with varicella-zoster virus. Acta Pathol Jpn 36:1537–1552

    PubMed  CAS  Google Scholar 

  • Pass RF (2001) Cytomegalovirus. In Fields Virology, 4th edn Knipe DM, Howley PM. Eds Lippincott Williams &Wilkins Philadelphia. Chapter 77, pp 2675–2706

    Google Scholar 

  • Perot K, Walker CM, Spaete RR (1992) Primary chimpanzee skin fibroblast cells are fully permissive for human cytomegalovirus replication. J Gen Virol 73:3281–3284

    Article  PubMed  Google Scholar 

  • Rickinson AB, Kieff E (2001) Epstein-Barr virus. In Fields Virology, 4th Edition.Knipe DM, Howley PM. Eds. Lippincott Williams &Wilkins Philadelphia. Chapter 75 pp 2575–2628

    Google Scholar 

  • Roizman B, Pellett PE (2001) The family Herpesviridae: A brief introduction. In Fields Virology, 4th Edition. Knipe DM, Howley PM. Eds. Lippincott Williams &Wilkins Philadelphia. Chapter 71 pp 2381–2397

    Google Scholar 

  • Roizman B, Carmichael LE, Deinhardt F, de-The G, Nahmias AJ, Plowright W, Rapp F, Sheldrick P, Takahashi M, Wolf K (1981) Herpesviridae: Definition, provisional nomenclature and taxonomy. Intervirology 16:201–217

    Article  PubMed  CAS  Google Scholar 

  • Rose TM, Strand KB, Schultz ER, Schaefer G, Rankin GW, Thouless ME, Tsai CC,Bosch ML (1997) Identification of two homologs of the Kaposi_s sarcoma-associated herpesvirus (human herpesvirus 8) in retroperitoneal fibromatosis of different macaque species. J Virol 71(5):4138–4144

    PubMed  CAS  Google Scholar 

  • Rubin RH (1990) Impact of cytomegalovirus infection on organ transplant recipients. Rev Infect Dis 12(suppl 7):S754–S766

    Article  PubMed  Google Scholar 

  • Schultz ER, Rankin GW Jr, Blanc MP, Raden BW, Tsai CC, Rose TM (2000) Characterization of two divergent lineages of macaque rhadinoviruses related to Kaposi_s sarcoma-associated herpesvirus. J Virol 74(10):4919–4928

    Article  PubMed  CAS  Google Scholar 

  • Singh N, Dummer JS, Kusne S, Breinig MK, Armstrong JA, Makowka L, Starzl TE, Ho M (1988) Infections with cytomegalovirus and other herpesviruses in 121 liver transplant recipients: transmission by donated organ and the effect of OKT3. J Infect Dis 158:124–131

    Article  PubMed  CAS  Google Scholar 

  • Smith AL, Black DH, Eberle R (1998) Molecular evidence for distinct genotypes of monkey B virus (Herpesvirus simiae) which are related to macaque host species. J Virol 72:9224–9232

    PubMed  CAS  Google Scholar 

  • Starzl TE, Fung J, Tzakis A, Todo S, Demetris AJ, Marino IR, Doyle H, Zeevi A, Warty V, Michaels M, Kusne S, Rudert WA, Trucco M (1993) Baboon-to-human liver transplantation. Lancet 341:65–71

    Article  PubMed  CAS  Google Scholar 

  • Swack NS, Liu OC, Hsiung GD (1971) Cytomegalovirus infections of monkeys and baboons. Am J Epidemiol 94:397–402

    PubMed  CAS  Google Scholar 

  • Taniguchi S, Cooper DKC (1997) Clinical xenotransplantation-a brief review of the world experience. In: Cooper DKC, et al, eds. Xenotransplantation 2nd Ed. Heidelberg, Germany: Springer, 776

    Google Scholar 

  • Van der Reit F de St J, Human PA, Cooper DKC, et al (1987) Virological consideration of the use of primates in xenotransplantation. Transplant Proc 19:4068–4069

    Google Scholar 

  • Vogel P, Weigler BJ, Kerr H, Hendrickx AG, Barry PA (1994) Seroepidemiologic studies of cytomegalovirus infection in a breeding population of rhesus macaques.Lab Anim Sci 44(1):25–30

    Google Scholar 

  • Weigler BJ (1992) Biology of B virus in macaque and human hosts: a review. Clin Infect Dis 14:555–567

    Article  PubMed  CAS  Google Scholar 

  • Weiner D, Gibson W (1981) Identification of a primate cytomegalovirus group-common protein antigen. Virology115:182–191

    Article  Google Scholar 

  • Wong SW, Bergquam EP, Swanson RM, Lee FW, Shiigi SM, Avery NA, Fanton JW, Axthelm MK (1999) Induction of B cell hyperplasia in simian immunodeficiency virus-infected Rhesus Macaques with the simian homologue of Kaposi_s Sarcomaassociated herpesvirus. J Exp Med 190(6):827–840

    Article  PubMed  CAS  Google Scholar 

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Michaels, M.G. (2003). Nonhuman Primate Herpesviruses:Importance for Xenotransplantation. In: Salomon, D.R., Wilson, C. (eds) Xeno-transplantation. Current Topics in Microbiology and Immunology, vol 278. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-55541-1_4

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