Skip to main content
Erschienen in: Medical Microbiology and Immunology 1/2019

05.10.2018 | Original Investigation

Macaca arctoides gammaherpesvirus 1 (strain herpesvirus Macaca arctoides): virus sequence, phylogeny and characterisation of virus-transformed macaque and rabbit cell lines

verfasst von: Andi Krumbholz, Janine Roempke, Thomas Liehr, Marco Groth, Astrid Meerbach, Michael Schacke, Gregor Maschkowitz, Helmut Fickenscher, Wolfram Klapper, Andreas Sauerbrei, Peter Wutzler, Roland Zell

Erschienen in: Medical Microbiology and Immunology | Ausgabe 1/2019

Einloggen, um Zugang zu erhalten

Abstract

Herpesvirus Macaca arctoides (HVMA) has the propensity to transform macaque lymphocytes to lymphoblastoid cells (MAL-1). Inoculation of rabbits with cell-free virus-containing supernatant resulted in the development of malignant lymphomas and allowed isolation of immortalised HVMA-transformed rabbit lymphocytes (HTRL). In this study, the HVMA genome sequence (approx. 167 kbp), its organisation, and novel aspects of virus latency are presented. Ninety-one open reading frames were identified, of which 86 were non-repetitive. HVMA was identified as a Lymphocryptovirus closely related to Epstein–Barr virus, suggesting the designation as ‘Macaca arctoides gammaherpesvirus 1’ (MarcGHV-1). In situ lysis gel and Southern blot hybridisation experiments revealed that the MAL-1 cell line contains episomal and linear DNA, whereas episomal DNA is predominantly present in HTRL. Integration of viral DNA into macaque and rabbit host cell genomes was demonstrated by fluorescence in situ hybridisation on chromosomal preparations. Analysis of next-generation sequencing data confirmed this finding. Approximately 400 read pairs represent the overlap between macaque and MarcGHV-1 DNA. Both, MAL-1 cells and HTRL show characteristics of a polyclonal tumour with B- and T-lymphocyte markers. Based on analysis of viral gene expression and immunohistochemistry, the persistence of MarcGHV-1 in MAL-1 cells resemble the latency type III, whereas the expression pattern observed in HTRL was more comparable with latency type II. There was no evidence of the presence of STLV-1 proviral DNA in MAL-1 and HTRL. Due to the similarity to EBV-mediated cell transformation, MarcGHV-1 expands the available in vitro models by simian and rabbit cell lines.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
10.
Zurück zum Zitat Blossom D (2007) EBV and KSHV-related herpesviruses in non-human primates. In: Arvin A, Campadelli-Fiume G, Mocarski E et al (eds) Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, pp 1093–1114 Blossom D (2007) EBV and KSHV-related herpesviruses in non-human primates. In: Arvin A, Campadelli-Fiume G, Mocarski E et al (eds) Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, pp 1093–1114
12.
Zurück zum Zitat Pellett P, Davison A, Eberle R, Ehlers B, Hayward G, Lacoste V, Minson A, Nicholas J, Roizman B, Studdert M (2012) Order herpesvirales. Virus taxonomy: Classification and nomenclature of viruses: ninth report of the International Committee on Taxonomy of Viruses, King AMQ, Adams MJA, Carstens EB, Lefkowitz EJ, Academic Press, Waltham, pp 99–123 Pellett P, Davison A, Eberle R, Ehlers B, Hayward G, Lacoste V, Minson A, Nicholas J, Roizman B, Studdert M (2012) Order herpesvirales. Virus taxonomy: Classification and nomenclature of viruses: ninth report of the International Committee on Taxonomy of Viruses, King AMQ, Adams MJA, Carstens EB, Lefkowitz EJ, Academic Press, Waltham, pp 99–123
13.
Zurück zum Zitat Rivailler P, Carville A, Kaur A, Rao P, Quink C, Kutok JL, Westmoreland S, Klumpp S, Simon M, Aster JC, Wang F (2004) Experimental rhesus lymphocryptovirus infection in immunosuppressed macaques: an animal model for Epstein–Barr virus pathogenesis in the immunosuppressed host. Blood 104(5):1482–1489. https://doi.org/10.1182/blood-2004-01-0342 CrossRefPubMed Rivailler P, Carville A, Kaur A, Rao P, Quink C, Kutok JL, Westmoreland S, Klumpp S, Simon M, Aster JC, Wang F (2004) Experimental rhesus lymphocryptovirus infection in immunosuppressed macaques: an animal model for Epstein–Barr virus pathogenesis in the immunosuppressed host. Blood 104(5):1482–1489. https://​doi.​org/​10.​1182/​blood-2004-01-0342 CrossRefPubMed
14.
Zurück zum Zitat Voevodin AF, Marx PA (2009) Lymphocryptoviruses. simian virology:323–346 Voevodin AF, Marx PA (2009) Lymphocryptoviruses. simian virology:323–346
15.
Zurück zum Zitat Rivailler P, Jiang H, Cho YG, Quink C, Wang F (2002) Complete nucleotide sequence of the rhesus lymphocryptovirus: genetic validation for an Epstein–Barr virus animal model. J Virol 76(1):421–426CrossRefPubMedPubMedCentral Rivailler P, Jiang H, Cho YG, Quink C, Wang F (2002) Complete nucleotide sequence of the rhesus lymphocryptovirus: genetic validation for an Epstein–Barr virus animal model. J Virol 76(1):421–426CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat Lapin BA, Timanovskaya VV, Yakovleva LA (1985) Herpesvirus HVMA: a new representative in the group of the EBV-like B-lymphotropic herpesviruses of primates. Haematol Blood Transfus 29:312–313PubMed Lapin BA, Timanovskaya VV, Yakovleva LA (1985) Herpesvirus HVMA: a new representative in the group of the EBV-like B-lymphotropic herpesviruses of primates. Haematol Blood Transfus 29:312–313PubMed
20.
Zurück zum Zitat Iakovleva LA, Timanovskaia VV, Indzhiia LV, Lapin BA, Voevodin AF (1987) Modelling of malignant lymphoma in rabbits using primate oncogenic viruses. Preliminary report. Biull Eksp Biol Med 103(3):336–338CrossRefPubMed Iakovleva LA, Timanovskaia VV, Indzhiia LV, Lapin BA, Voevodin AF (1987) Modelling of malignant lymphoma in rabbits using primate oncogenic viruses. Preliminary report. Biull Eksp Biol Med 103(3):336–338CrossRefPubMed
21.
Zurück zum Zitat Timanovskaia VV, Voevodin AF, Iakovleva LA, Markarian DS, Ivanov MT (1988) Malignant lymphoma in rabbits induced by the administration of herpes virus-containing material from brown macaques. Eksp Onkol 10(3):47–51PubMed Timanovskaia VV, Voevodin AF, Iakovleva LA, Markarian DS, Ivanov MT (1988) Malignant lymphoma in rabbits induced by the administration of herpes virus-containing material from brown macaques. Eksp Onkol 10(3):47–51PubMed
22.
Zurück zum Zitat Wutzler P, Meerbach A, Farber I, Wolf H, Scheibner K (1995) Malignant lymphomas induced by an Epstein–Barr virus-related herpesvirus from Macaca arctoides—a rabbit model. Arch Virol 140(11):1979–1995CrossRefPubMed Wutzler P, Meerbach A, Farber I, Wolf H, Scheibner K (1995) Malignant lymphomas induced by an Epstein–Barr virus-related herpesvirus from Macaca arctoides—a rabbit model. Arch Virol 140(11):1979–1995CrossRefPubMed
23.
Zurück zum Zitat Yakovleva LA, Timanovskaya VV, Voevodin AF, Indzhiia LV, Lapin BA, Ivanov MT, Markaryan DS (1987) Modelling of malignant lymphoma in rabbits, using oncogenic viruses of non-human primates. Haematol Blood Transfus 31:445–447PubMed Yakovleva LA, Timanovskaya VV, Voevodin AF, Indzhiia LV, Lapin BA, Ivanov MT, Markaryan DS (1987) Modelling of malignant lymphoma in rabbits, using oncogenic viruses of non-human primates. Haematol Blood Transfus 31:445–447PubMed
24.
Zurück zum Zitat Schatzl H, Tschikobava M, Rose D, Voevodin A, Nitschko H, Sieger E, Busch U, von der Helm K, Lapin B (1993) The Sukhumi primate monkey model for viral lymphomogenesis: high incidence of lymphomas with presence of STLV-I and EBV-like virus. Leukemia 7(Suppl 2):S86–S92PubMed Schatzl H, Tschikobava M, Rose D, Voevodin A, Nitschko H, Sieger E, Busch U, von der Helm K, Lapin B (1993) The Sukhumi primate monkey model for viral lymphomogenesis: high incidence of lymphomas with presence of STLV-I and EBV-like virus. Leukemia 7(Suppl 2):S86–S92PubMed
25.
Zurück zum Zitat Pulvertaft RJV (1964) Cytology of Burkitt’s tumor (African lymphoma). Lancet 1(7327):238–240CrossRefPubMed Pulvertaft RJV (1964) Cytology of Burkitt’s tumor (African lymphoma). Lancet 1(7327):238–240CrossRefPubMed
27.
Zurück zum Zitat Klein G, Giovanella B, Westman A, Stehlin JS, Mumford D (1975) An EBV-genome-negative cell line established from an American Burkitt lymphoma; receptor characteristics. EBV infectibility and permanent conversion into EBV-positive sublines by in vitro infection. Intervirology 5(6):319–334. https://doi.org/10.1159/000149930 CrossRefPubMed Klein G, Giovanella B, Westman A, Stehlin JS, Mumford D (1975) An EBV-genome-negative cell line established from an American Burkitt lymphoma; receptor characteristics. EBV infectibility and permanent conversion into EBV-positive sublines by in vitro infection. Intervirology 5(6):319–334. https://​doi.​org/​10.​1159/​000149930 CrossRefPubMed
28.
Zurück zum Zitat Davies AH, Grand RJ, Evans FJ, Rickinson AB (1991) Induction of Epstein–Barr virus lytic cycle by tumor-promoting and non-tumor-promoting phorbol esters requires active protein kinase C. J Virol 65(12):6838–6844PubMedPubMedCentral Davies AH, Grand RJ, Evans FJ, Rickinson AB (1991) Induction of Epstein–Barr virus lytic cycle by tumor-promoting and non-tumor-promoting phorbol esters requires active protein kinase C. J Virol 65(12):6838–6844PubMedPubMedCentral
30.
Zurück zum Zitat d’Offay JM, Eberle R, Sucol Y, Schoelkopf L, White MA, Valentine BD, White GL, Lerche NW (2007) Transmission dynamics of simian T-lymphotropic virus type 1 (STLV1) in a baboon breeding colony: predominance of female-to-female transmission. Comp Med 57(1):105–114PubMed d’Offay JM, Eberle R, Sucol Y, Schoelkopf L, White MA, Valentine BD, White GL, Lerche NW (2007) Transmission dynamics of simian T-lymphotropic virus type 1 (STLV1) in a baboon breeding colony: predominance of female-to-female transmission. Comp Med 57(1):105–114PubMed
32.
Zurück zum Zitat Dehee A, Cesaire R, Desire N, Lezin A, Bourdonne O, Bera O, Plumelle Y, Smadja D, Nicolas JC (2002) Quantitation of HTLV-I proviral load by a TaqMan real-time PCR assay. J Virol Methods 102(1–2):37–51CrossRefPubMed Dehee A, Cesaire R, Desire N, Lezin A, Bourdonne O, Bera O, Plumelle Y, Smadja D, Nicolas JC (2002) Quantitation of HTLV-I proviral load by a TaqMan real-time PCR assay. J Virol Methods 102(1–2):37–51CrossRefPubMed
37.
Zurück zum Zitat Gardella T, Medveczky P, Sairenji T, Mulder C (1984) Detection of circular and linear herpesvirus DNA molecules in mammalian cells by gel electrophoresis. J Virol 50(1):248–254PubMedPubMedCentral Gardella T, Medveczky P, Sairenji T, Mulder C (1984) Detection of circular and linear herpesvirus DNA molecules in mammalian cells by gel electrophoresis. J Virol 50(1):248–254PubMedPubMedCentral
40.
43.
Zurück zum Zitat Weise A, Gross M, Mrasek K, Mkrtchyan H, Horsthemke B, Jonsrud C, Von Eggeling F, Hinreiner S, Witthuhn V, Claussen U, Liehr T (2008) Parental-origin-determination fluorescence in situ hybridization distinguishes homologous human chromosomes on a single-cell level. Int J Mol Med 21(2):189–200PubMed Weise A, Gross M, Mrasek K, Mkrtchyan H, Horsthemke B, Jonsrud C, Von Eggeling F, Hinreiner S, Witthuhn V, Claussen U, Liehr T (2008) Parental-origin-determination fluorescence in situ hybridization distinguishes homologous human chromosomes on a single-cell level. Int J Mol Med 21(2):189–200PubMed
44.
Zurück zum Zitat Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, Brown CG, Hall KP,Evers DJ, Barnes CL, Bignell HR, Boutell JM, Bryant J, Carter RJ, Keira Cheetham R,Cox AJ, Ellis DJ, Flatbush MR, Gormley NA, Humphray SJ, Irving LJ, Karbelashvili MS,Kirk SM, Li H, Liu X, Maisinger KS, Murray LJ, Obradovic B, Ost T, Parkinson ML, Pratt MR, Rasolonjatovo IM, Reed MT, Rigatti R, Rodighiero C, Ross MT, Sabot A, Sankar SV, Scally A, Schroth GP, Smith ME, Smith VP, Spiridou A, Torrance PE, Tzonev SS, Vermaas EH, Walter K, Wu X, Zhang L, Alam MD, Anastasi C, Aniebo IC, Bailey DM, Bancarz IR, Banerjee S, Barbour SG, Baybayan PA, Benoit VA, Benson KF, Bevis C, Black PJ, Boodhun A, Brennan JS, Bridgham JA, Brown RC, Brown AA, Buermann DH, Bundu AA, Burrows JC,Carter NP, Castillo N, Chiara ECM, Chang S, Neil Cooley R, Crake NR, Dada OO, Diakoumakos KD, Dominguez-Fernandez B, Earnshaw DJ, Egbujor UC, Elmore DW, Etchin SS, Ewan MR,Fedurco M, Fraser LJ, Fuentes Fajardo KV, Scott Furey W, George D, Gietzen KJ, Goddard CP, Golda GS, Granieri PA, Green DE, Gustafson DL, Hansen NF, Harnish K, Haudenschild CD, Heyer NI, Hims MM, Ho JT, Horgan AM, Hoschler K, Hurwitz S, Ivanov DV, Johnson MQ, James T, Huw Jones TA, Kang GD, Kerelska TH, Kersey AD, Khrebtukova I, Kindwall AP, Kingsbury Z, Kokko-Gonzales PI, Kumar A, Laurent MA, Lawley CT, Lee SE, Lee X,Liao AK, Loch JA, Lok M, Luo S, Mammen RM, Martin JW, McCauley PG, McNitt P, Mehta P, Moon KW, Mullens JW, Newington T, Ning Z, Ling Ng B, Novo SM, O’Neill MJ, Osborne MA, Osnowski A, Ostadan O, Paraschos LL, Pickering L, Pike AC, Pike AC, Chris Pinkard D, Pliskin DP, Podhasky J, Quijano VJ, Raczy C, Rae VH, Rawlings SR, Chiva Rodriguez A, Roe PM, Rogers J, Rogert Bacigalupo MC, Romanov N, Romieu A, Roth RK, Rourke NJ,Ruediger ST, Rusman E, Sanches-Kuiper RM, Schenker MR, Seoane JM, Shaw RJ, Shiver MK, Short SW, Sizto NL, Sluis JP, Smith MA, Ernest Sohna Sohna J, Spence EJ, Stevens K, Sutton N, Szajkowski L, Tregidgo CL, Turcatti G, Vandevondele S, Verhovsky Y, Virk SM, Wakelin S, Walcott GC, Wang J, Worsley GJ, Yan J, Yau L, Zuerlein M, Rogers J,Mullikin JC, Hurles ME, McCooke NJ, West JS, Oaks FL, Lundberg PL, Klenerman D, Durbin R, Smith AJ (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456(7218):53–59. https://doi.org/10.1038/nature07517 Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, Brown CG, Hall KP,Evers DJ, Barnes CL, Bignell HR, Boutell JM, Bryant J, Carter RJ, Keira Cheetham R,Cox AJ, Ellis DJ, Flatbush MR, Gormley NA, Humphray SJ, Irving LJ, Karbelashvili MS,Kirk SM, Li H, Liu X, Maisinger KS, Murray LJ, Obradovic B, Ost T, Parkinson ML, Pratt MR, Rasolonjatovo IM, Reed MT, Rigatti R, Rodighiero C, Ross MT, Sabot A, Sankar SV, Scally A, Schroth GP, Smith ME, Smith VP, Spiridou A, Torrance PE, Tzonev SS, Vermaas EH, Walter K, Wu X, Zhang L, Alam MD, Anastasi C, Aniebo IC, Bailey DM, Bancarz IR, Banerjee S, Barbour SG, Baybayan PA, Benoit VA, Benson KF, Bevis C, Black PJ, Boodhun A, Brennan JS, Bridgham JA, Brown RC, Brown AA, Buermann DH, Bundu AA, Burrows JC,Carter NP, Castillo N, Chiara ECM, Chang S, Neil Cooley R, Crake NR, Dada OO, Diakoumakos KD, Dominguez-Fernandez B, Earnshaw DJ, Egbujor UC, Elmore DW, Etchin SS, Ewan MR,Fedurco M, Fraser LJ, Fuentes Fajardo KV, Scott Furey W, George D, Gietzen KJ, Goddard CP, Golda GS, Granieri PA, Green DE, Gustafson DL, Hansen NF, Harnish K, Haudenschild CD, Heyer NI, Hims MM, Ho JT, Horgan AM, Hoschler K, Hurwitz S, Ivanov DV, Johnson MQ, James T, Huw Jones TA, Kang GD, Kerelska TH, Kersey AD, Khrebtukova I, Kindwall AP, Kingsbury Z, Kokko-Gonzales PI, Kumar A, Laurent MA, Lawley CT, Lee SE, Lee X,Liao AK, Loch JA, Lok M, Luo S, Mammen RM, Martin JW, McCauley PG, McNitt P, Mehta P, Moon KW, Mullens JW, Newington T, Ning Z, Ling Ng B, Novo SM, O’Neill MJ, Osborne MA, Osnowski A, Ostadan O, Paraschos LL, Pickering L, Pike AC, Pike AC, Chris Pinkard D, Pliskin DP, Podhasky J, Quijano VJ, Raczy C, Rae VH, Rawlings SR, Chiva Rodriguez A, Roe PM, Rogers J, Rogert Bacigalupo MC, Romanov N, Romieu A, Roth RK, Rourke NJ,Ruediger ST, Rusman E, Sanches-Kuiper RM, Schenker MR, Seoane JM, Shaw RJ, Shiver MK, Short SW, Sizto NL, Sluis JP, Smith MA, Ernest Sohna Sohna J, Spence EJ, Stevens K, Sutton N, Szajkowski L, Tregidgo CL, Turcatti G, Vandevondele S, Verhovsky Y, Virk SM, Wakelin S, Walcott GC, Wang J, Worsley GJ, Yan J, Yau L, Zuerlein M, Rogers J,Mullikin JC, Hurles ME, McCooke NJ, West JS, Oaks FL, Lundberg PL, Klenerman D, Durbin R, Smith AJ (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456(7218):53–59. https://​doi.​org/​10.​1038/​nature07517
46.
47.
Zurück zum Zitat Roizman B, Baines J (1991) The diversity and unity of herpesviridae. Comp Immunol Microbiol Infect Dis 14(2):63–79CrossRefPubMed Roizman B, Baines J (1991) The diversity and unity of herpesviridae. Comp Immunol Microbiol Infect Dis 14(2):63–79CrossRefPubMed
50.
Zurück zum Zitat Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
54.
Zurück zum Zitat Hurley EA, Agger S, McNeil JA, Lawrence JB, Calendar A, Lenoir G, Thorley-Lawson DA (1991) When Epstein–Barr virus persistently infects B-cell lines, it frequently integrates. J Virol 65(3):1245–1254PubMedPubMedCentral Hurley EA, Agger S, McNeil JA, Lawrence JB, Calendar A, Lenoir G, Thorley-Lawson DA (1991) When Epstein–Barr virus persistently infects B-cell lines, it frequently integrates. J Virol 65(3):1245–1254PubMedPubMedCentral
55.
Zurück zum Zitat Watanabe T, Seiki M, Tsujimoto H, Miyoshi I, Hayami M, Yoshida M (1985) Sequence homology of the simian retrovirus genome with human T-cell leukemia virus type I. Virology 144(1):59–65CrossRefPubMed Watanabe T, Seiki M, Tsujimoto H, Miyoshi I, Hayami M, Yoshida M (1985) Sequence homology of the simian retrovirus genome with human T-cell leukemia virus type I. Virology 144(1):59–65CrossRefPubMed
57.
Zurück zum Zitat Pezzutto A, Ulrichs T, Burmester G-R (2007) Taschenatlas der Immunologie, vol 2. Georg Thieme Verlag, Stuttgart Pezzutto A, Ulrichs T, Burmester G-R (2007) Taschenatlas der Immunologie, vol 2. Georg Thieme Verlag, Stuttgart
59.
Zurück zum Zitat Wienberg J, Stanyon R, Jauch A, Cremer T (1992) Homologies in human and Macaca fuscata chromosomes revealed by in situ suppression hybridization with human chromosome specific DNA libraries. Chromosoma 101(5–6):265–270CrossRefPubMed Wienberg J, Stanyon R, Jauch A, Cremer T (1992) Homologies in human and Macaca fuscata chromosomes revealed by in situ suppression hybridization with human chromosome specific DNA libraries. Chromosoma 101(5–6):265–270CrossRefPubMed
60.
Zurück zum Zitat Fan X, Sangpakdee W, Tanomtong A, Chaveerach A, Pinthong K, Pornnarong S, Supiwong W, Trifonov V, Hovhannisyan G, Aroutouinian R (2014) Molecular cytogenetic analysis of Thai southern pig-tailed macaque (Macaca nemestrina) by multicolor banding. Proceedings of Yerevan State University 2014:46–50 Fan X, Sangpakdee W, Tanomtong A, Chaveerach A, Pinthong K, Pornnarong S, Supiwong W, Trifonov V, Hovhannisyan G, Aroutouinian R (2014) Molecular cytogenetic analysis of Thai southern pig-tailed macaque (Macaca nemestrina) by multicolor banding. Proceedings of Yerevan State University 2014:46–50
61.
Zurück zum Zitat Fan X, Sangpakdee W, Tanomtong A, Chaveerach A, Pinthong K, Pornnarong S, Supiwong W, Trifonov V, Hovhannisyan G, Loth K (2014) Comprehensive molecular cytogenetic analysis of Barbary macaque (Macaca sylvanus). J Armenia 66(1):98–102 Fan X, Sangpakdee W, Tanomtong A, Chaveerach A, Pinthong K, Pornnarong S, Supiwong W, Trifonov V, Hovhannisyan G, Loth K (2014) Comprehensive molecular cytogenetic analysis of Barbary macaque (Macaca sylvanus). J Armenia 66(1):98–102
62.
Zurück zum Zitat O’Brien SJ, Menninger JC, Nash WG (2006) Atlas of mammalian chromosomes. Wiley, HobokenCrossRef O’Brien SJ, Menninger JC, Nash WG (2006) Atlas of mammalian chromosomes. Wiley, HobokenCrossRef
67.
Zurück zum Zitat Kakubava VV, Agrba VZ, Timanovskaia VV, Brzhikhachek B (1990) Analysis of B-lymphotropic oncogenic herpesvirus of Macaca arctoides. Eksp Onkol 12(6):44–46PubMed Kakubava VV, Agrba VZ, Timanovskaia VV, Brzhikhachek B (1990) Analysis of B-lymphotropic oncogenic herpesvirus of Macaca arctoides. Eksp Onkol 12(6):44–46PubMed
68.
Zurück zum Zitat Gillet L, Minner F, Detry B, Farnir F, Willems L, Lambot M, Thiry E, Pastoret PP, Schynts F, Vanderplasschen A (2004) Investigation of the susceptibility of human cell lines to bovine herpesvirus 4 infection: demonstration that human cells can support a nonpermissive persistent infection which protects them against tumor necrosis factor alpha-induced apoptosis. J Virol 78(5):2336–2347CrossRefPubMedPubMedCentral Gillet L, Minner F, Detry B, Farnir F, Willems L, Lambot M, Thiry E, Pastoret PP, Schynts F, Vanderplasschen A (2004) Investigation of the susceptibility of human cell lines to bovine herpesvirus 4 infection: demonstration that human cells can support a nonpermissive persistent infection which protects them against tumor necrosis factor alpha-induced apoptosis. J Virol 78(5):2336–2347CrossRefPubMedPubMedCentral
69.
Zurück zum Zitat Agrba VZ, Lapin BA, Medvedeva NM, Yakovleva LA (2004) Immunophenotypical characteristics of permanent cultures of lymphoid cells from Papio hamadryas and Macaca arctoides. Bull Exp Biol Med 137(2):190–194CrossRefPubMed Agrba VZ, Lapin BA, Medvedeva NM, Yakovleva LA (2004) Immunophenotypical characteristics of permanent cultures of lymphoid cells from Papio hamadryas and Macaca arctoides. Bull Exp Biol Med 137(2):190–194CrossRefPubMed
71.
Zurück zum Zitat Blake NW, Moghaddam A, Rao P, Kaur A, Glickman R, Cho YG, Marchini A, Haigh T, Johnson RP, Rickinson AB, Wang F (1999) Inhibition of antigen presentation by the glycine/alanine repeat domain is not conserved in simian homologues of Epstein–Barr virus nuclear antigen 1. J Virol 73(9):7381–7389PubMedPubMedCentral Blake NW, Moghaddam A, Rao P, Kaur A, Glickman R, Cho YG, Marchini A, Haigh T, Johnson RP, Rickinson AB, Wang F (1999) Inhibition of antigen presentation by the glycine/alanine repeat domain is not conserved in simian homologues of Epstein–Barr virus nuclear antigen 1. J Virol 73(9):7381–7389PubMedPubMedCentral
75.
Zurück zum Zitat Lestou VS, De Braekeleer M, Strehl S, Ott G, Gadner H, Ambros PF (1993) Non-random integration of Epstein–Barr virus in lymphoblastoid cell lines. Genes Chromosomes Cancer 8(1):38–48CrossRefPubMed Lestou VS, De Braekeleer M, Strehl S, Ott G, Gadner H, Ambros PF (1993) Non-random integration of Epstein–Barr virus in lymphoblastoid cell lines. Genes Chromosomes Cancer 8(1):38–48CrossRefPubMed
76.
Zurück zum Zitat Caporossi D, Vernole P, Porfirio B, Tedeschi B, Frezza D, Nicoletti B, Calef E (1988) Specific sites for EBV association in the Namalwa Burkitt lymphoma cell line and in a lymphoblastoid line transformed in vitro with EBV. Cytogenet Cell Genet 48(4):220–223. https://doi.org/10.1159/000132632 CrossRefPubMed Caporossi D, Vernole P, Porfirio B, Tedeschi B, Frezza D, Nicoletti B, Calef E (1988) Specific sites for EBV association in the Namalwa Burkitt lymphoma cell line and in a lymphoblastoid line transformed in vitro with EBV. Cytogenet Cell Genet 48(4):220–223. https://​doi.​org/​10.​1159/​000132632 CrossRefPubMed
78.
Zurück zum Zitat Davison AJ (2007) Comparative analysis of the genomes. In: Arvin A, Campadelli-Fiume G, Mocarski E et al (eds) Human herpesviruses—biology, therapy and immunoprophylaxis. Cambridge University Press, Cambridge, pp 10–26CrossRef Davison AJ (2007) Comparative analysis of the genomes. In: Arvin A, Campadelli-Fiume G, Mocarski E et al (eds) Human herpesviruses—biology, therapy and immunoprophylaxis. Cambridge University Press, Cambridge, pp 10–26CrossRef
79.
Zurück zum Zitat Young LS, Arrand JR, Murray PG (2007) EBV gene expression and regulation. In: Arvin A, Campadelli-Fiume G, Mocarski E et al (eds) Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, pp 461–489CrossRef Young LS, Arrand JR, Murray PG (2007) EBV gene expression and regulation. In: Arvin A, Campadelli-Fiume G, Mocarski E et al (eds) Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, pp 461–489CrossRef
82.
Zurück zum Zitat Fossum E, Friedel CC, Rajagopala SV, Titz B, Baiker A, Schmidt T, Kraus T, Stellberger T, Rutenberg C, Suthram S, Bandyopadhyay S, Rose D, von Brunn A, Uhlmann M, Zeretzke C, Dong YA, Boulet H, Koegl M, Bailer SM, Koszinowski U, Ideker T, Uetz P, Zimmer R, Haas J (2009) Evolutionarily conserved herpesviral protein interaction networks. PLoS Pathog 5(9):e1000570. https://doi.org/10.1371/journal.ppat.1000570 CrossRefPubMedPubMedCentral Fossum E, Friedel CC, Rajagopala SV, Titz B, Baiker A, Schmidt T, Kraus T, Stellberger T, Rutenberg C, Suthram S, Bandyopadhyay S, Rose D, von Brunn A, Uhlmann M, Zeretzke C, Dong YA, Boulet H, Koegl M, Bailer SM, Koszinowski U, Ideker T, Uetz P, Zimmer R, Haas J (2009) Evolutionarily conserved herpesviral protein interaction networks. PLoS Pathog 5(9):e1000570. https://​doi.​org/​10.​1371/​journal.​ppat.​1000570 CrossRefPubMedPubMedCentral
84.
Zurück zum Zitat Thompson MP, Kurzrock R (2004) Epstein–Barr virus and cancer. Clin Cancer Res 10(3):803–821CrossRefPubMed Thompson MP, Kurzrock R (2004) Epstein–Barr virus and cancer. Clin Cancer Res 10(3):803–821CrossRefPubMed
Metadaten
Titel
Macaca arctoides gammaherpesvirus 1 (strain herpesvirus Macaca arctoides): virus sequence, phylogeny and characterisation of virus-transformed macaque and rabbit cell lines
verfasst von
Andi Krumbholz
Janine Roempke
Thomas Liehr
Marco Groth
Astrid Meerbach
Michael Schacke
Gregor Maschkowitz
Helmut Fickenscher
Wolfram Klapper
Andreas Sauerbrei
Peter Wutzler
Roland Zell
Publikationsdatum
05.10.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
Medical Microbiology and Immunology / Ausgabe 1/2019
Print ISSN: 0300-8584
Elektronische ISSN: 1432-1831
DOI
https://doi.org/10.1007/s00430-018-0565-y

Weitere Artikel der Ausgabe 1/2019

Medical Microbiology and Immunology 1/2019 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.