Porcine endogenous retroviruses in xenotransplantation-molecular aspects

Viruses

Volumn 6, Issue 5, 2014, Pages 2062-2083

  Kimsa, Magdalena C ^a   Strzalka Mrozik, Barbara ^a   Kimsa, Malgorzata W ^a   Gola, Joanna ^a   Nicholson, Peter ^a   Lopata, Krzysztof ^a   Mazurek, Urszula ^a  

^a MEDICAL UNIVERSITY OF SILESIA   (Poland)

Author keywords

Detection; Molecular techniques; Porcine endogenous retroviruses; Xenotransplantation

Indexed keywords

BETA 2 MICROGLOBULIN; BETA ACTIN; DNA TOPOISOMERASE (ATP HYDROLYSING); ELONGATION FACTOR 1ALPHA; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; PORPHOBILINOGEN DEAMINASE; RIBOSOME PROTEIN; RNA DIRECTED DNA POLYMERASE; SUCCINATE DEHYDROGENASE; TATA BINDING PROTEIN; VIRUS ANTIGEN; VIRUS DNA; VIRUS RNA;

CHIMERA; CLINICAL TRIAL (TOPIC); DNA DETERMINATION; ENDOGENOUS RETROVIRUS; GRAFT RECIPIENT; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HYBRIDIZATION; IMMUNOCHEMISTRY; INFLUENZA VIRUS A H1N1; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; RNA ANALYSIS; RNA INTERFERENCE; SWINE; TROPISM; VIRAL TROPISM; VIRUS EXPRESSION; VIRUS GENOME; VIRUS INFECTION; VIRUS TRANSMISSION; WEST NILE FLAVIVIRUS; XENOTRANSPLANTATION; XENOZOONOTIC DISEASE; ANIMAL; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; RETROVIRIDAE INFECTIONS; VIROLOGY; XENOGRAFT;

ANIMALS; ANTIGENS, VIRAL; DNA, VIRAL; ENDOGENOUS RETROVIRUSES; HUMANS; RETROVIRIDAE INFECTIONS; RNA, VIRAL; SWINE; TRANSPLANTATION, HETEROLOGOUS;

EID: 84900798760     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v6052062     Document Type: Review

References (145)

1. PHS. U.S. Public Health Service Guideline on Infectious Disease Issues in Xenotransplantation. Morb. Mortal. Wkly. Rep. Recomm. Rep. 2001, 50, 1-46.
2. Patience, C.; Takeuchi, Y.; Weiss, R.A. Infection of human cells by an endogenous retrovirus of pigs. Nat. Med. 1997, 3, 282-286.
3. Specke, V.; Rubant, S.; Denner, J. Productive infection of human primary cells and cell lines with porcine endogenous retroviruses. Virology 2001, 285, 177-180.
4. Denner, J. Recombinant porcine endogenous retroviruses (PERV-A/C): A new risk for xenotransplantation? Xenotransplantation 2010, 17, doi:10.1111/j.1399-3089.2010.00573_21.x.
5. Denner, J. Infectious risk in xenotransplantation-What post-transplant screening for the human recipient? Xenotransplantation 2011, 18, 151-157.
6. Fishman, J.A. Infection in Xenotransplantation. J. Card. Surg. 2001, 16, 363-373.
7. Wilson, C.A. Porcine endogenous retroviruses and xenotransplantation. Cell. Mol. Life Sci. 2008, 65, 3399-33412.
8. Chari, R.S.; Collins, B.H.; Magee, J.C.; DiMaio, J.M.; Kirk, A.D.; Harland, R.C.; McCann, R.L.; Platt, J.L.; Meyers, W.C. Brief report: Treatment of hepatic failure with ex vivo pig-liver perfusion followed by liver transplantation. N. Engl. J. Med. 1994, 331, 234-237.
9. Groth, C.G.; Korsgren, O.; Tibell, A.; Tollemar, J.; Moller, E.; Bolinder, J.; Ostman, J.; Reinholt, F.P.; Hellerstrom, C.; Andersson, A. Transplantation of porcine fetal pancreas to diabetic patients. Lancet 1994, 344, 1402-1404.
10. Deacon, T.; Schumacher, J.; Dinsmore, J.; Thomas, C.; Palmer, P.; Kott, S.; Edge, A.; Penney, D.; Kassissieh, S.; Dempsey, P.; et al. Histological evidence of fetal pig neural cell survival after transplantation into a patient with Parkinson's disease. Nat. Med. 1997, 3, 350-353.
11. Fink, J.S.; Schumacher, J.M.; Ellias, S.L.; Palmer, E.P.; Saint-Hilaire, M.; Shannon, K.; Penn, R.; Starr, P.; VanHorne, C.; Kott, H.S.; et al. Porcine xenografts in Parkinson's disease and Huntington's disease patients: Preliminary results. Cell Transplant. 2000, 9, 273-278.
12. Sasaki, S.; Funamoto, S.; Hashimoto, Y.; Kimura, T.; Honda, T.; Hattori, S.; Kobayashi, H.; Kishida, A.; Mochizuki, M. In vivo evaluation of a novel scaffold for artificial corneas prepared by using ultrahigh hydrostatic pressure to decellularize porcine corneas. Mol. Vis. 2009, 15, 2022-2028.
13. Gu, C.; Wei, X.; Wang, Y.; Chen, Y.; Liu, J.; Wang, H.; Sun, G.; Yi, D. No infection with porcine endogenous retrovirus in recipients of acellular porcine aortic valves: A two-year study. Xenotransplantation 2008, 15, 121-128.
14. O'Connell, P.J.; Cowan, P.J.; Hawthorne, W.J.; Yi, S.; Lew, A.M. Transplantation of xenogeneic islets: Are we there yet? Curr. Diabetes Rep. 2013, 13, 687-694.
15. Heneine, W.; Tibell, A.; Switzer, W.M.; Sandstrom, P.; Rosales, G.V.; Mathews, A.; Korsgren, O.; Chapman, L.E.; Folks, T.M.; Groth, C.G. No evidence of infection with porcine endogenous retrovirus in recipients of porcine islet-cell xenografts. Lancet 1998, 352, 695-699.
16. Patience, C.; Patton, G.S.; Takeuchi, Y.; Weiss, R.A.; McClure, M.O.; Rydberg, L.; Breimer, M.E. No evidence of pig DNA or retroviral infection in patients with short-term extracorporeal connection to pig kidneys. Lancet 1998, 352, 699-701.
17. Paradis, K.; Langford, G.; Long, Z.; Heneine, W.; Sandstrom, P.; Switzer, W.M.; Chapman, L.E.; Lockey, C.; Onions, D.; Otto, E. Search for cross-species transmission of porcine endogenous retrovirus in patients treated with living pig tissue. The XEN 111 Study Group. Science 1999, 285, 1236-1241.
18. Elliott, R.B.; Escobar, L.; Garkavenko, O.; Croxson, M.C.; Schroeder, B.A.; McGregor, M.; Ferguson, G.; Beckman, N.; Ferguson, S. No evidence of infection with porcine endogenous retrovirus in recipients of encapsulated porcine islet xenografts. Cell Transplant. 2000, 9, 895-901.
19. Clémenceau, B.; Jégou, D.; Martignat, L.; Saï, P. Long-term follow-up failed to detect in vitro transmission of full-length porcine endogenous retroviruses from specific pathogen-free pig islets to human cells. Diabetologia 2001, 44, 2044-2055.
20. Cunningham, D.A.; Herring, C.; Fernández-Suárez, X.M.; Whittam, A.J.; Paradis, K.; Langford, G.A. Analysis of patients treated with living pig tissue for evidence of infection by porcine endogenous retroviruses. Trends Cardiovasc. Med. 2001, 11, 190-196.
21. Scobie, L.; Padler-Karavani, V.; Le Bas-Bernardet, S.; Crossan, C.; Blaha, J.; Matouskova, M.; Hector, R.D.; Cozzi, E.; Vanhove, B.; Charreau, B.; et al. Long-term IgG response to porcine Neu5Gc antigens without transmission of PERV in burn patients treated with porcine skin xenografts. J. Immunol. 2013, 191, 2907-2915.
22. Specke, V.; Tacke, S.J.; Boller, K.; Schwendemann, J.; Denner, J. Porcine endogenous retroviruses: In vitro host range and attempts to establish small animal models. J. Gen. Virol. 2001, 82, 837-844.
23. Li, Z.; Ping, Y.; Shengfu, L.; Yangzhi, Z.; Jingqiu, C.; Youping, L.; Hong, B. Variation of host cell tropism of porcine endogenous retroviruses expressed in chinese Banna minipig inbred. Intervirology 2006, 49, 185-191.
24. Donahue, R.E.; Kessler, S.W.; Bodine, D.; McDonagh, K.; Dunbar, C.; Goodman, S.; Agricola, B.; Byrne, E.; Raffeld, M.; Moen, R.; et al. Helper virus induced T cell lymphoma in nonhuman primates after retroviral mediated gene transfer. J. Exp. Med. 1992, 176, 1125-1135.
25. Fiebig, U.; Hartmann, M.G.; Bannert, N.; Kurth, R.; Denner, J. Transspecies transmission of the endogenous koala retrovirus. J. Virol. 2006, 80, 5651-5654.
26. Denner, J. Transspecies transmissions of retroviruses: New cases. Virology 2007, 369, 229-233.
27. Denner, J.; Tönjes, R.R. Infection barriers to successful xenotransplantation focusing on porcine endogenous retroviruses. Clin. Microbiol. Rev. 2012, 25, 318-343.
28. Paton, N.I.; Leo, Y.S.; Zaki, S.R.; Auchus, A.P.; Lee, K.E.; Ling, A.E.; Chew, S.K.; Ang, B.; Rollin, P.E.; Umapathi, T.; et al. Outbreak of Nipahvirus infection among abattoir workers in Singapore. Lancet 1999, 354, 1253-1256.
29. Keele, B.F.; van Heuverswyn, F.; Li, Y.; Bailes, E.; Takehisa, J.; Santiago, M.L.; Bibollet-Ruche, F.; Chen, Y.; Wain, L.V.; Liegeois, F.; et al. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 2006, 313, 523-526.
30. Kramer, L.D.; Li, J.; Shi, P.Y. West Nile virus. Lancet Neurol. 2007, 6, 171-181.
31. De Wit, E.; Fouchier, R.A. Emerging influenza. J. Clin. Virol. 2008, 41, 1-6.
32. Smith, G.J.; Vijaykrishna, D.; Bahl, J.; Lycett, S.J.; Worobey, M.; Pybus, O.G.; Ma, S.K.; Cheung, C.L.; Raghwani, J.; Bhatt, S.; et al. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 2009, 459, 1122-1125.
33. Garten, R.J.; Davis, C.T.; Russell, C.A.; Shu, B.; Lindstrom, S.; Balish, A.; Sessions, W.M.; Xu, X.; Skepner, E.; Deyde, V.; et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 2009, 325, 197-201.
34. Welin, S. Starting clinical trials of xenotransplantation-Reflections on the ethics of the early phase. J. Med. Ethics 2000, 26, 231-236.
35. Le Tissier, P.; Stoye, J.P.; Takeuchi, Y.; Patience, C.; Weiss, R. Two sets of human-tropic pig retrovirus. Nature 1997, 389, 681-682.
36. Wilson, C.A.; Wong, S.; VanBrocklin, M.; Federspiel, M.J. Extended analysis of the in vitro tropism of porcine endogenous retrovirus. J. Virol. 2000, 74, 49-56.
37. Gemeniano, M.; Mpanju, O.; Salomon, D.; Eiden, M.V.; Wilson, C.A. The infectivity and host range of the ectopic porcine endogenous retrovirus, PERV-C, is modulated by residues in the C-terminal region of its surface envelope protein. Virology 2006, 346, 108-117.
38. Denner, J. Recombinant porcine endogenous retroviruses (PERV-A/C): A new risk for xenotransplantation? Arch. Virol. 2008, 153, 1421-1426.
39. Takeuchi, Y.; Patience, C.; Magre, S.; Weiss, R.A.; Banerjee, P.T.; Le Tissier, P.; Stoye, J.P. Host range and interference studies of three classes of pig endogenous retrovirus. J. Virol. 1998, 72, 9986-9991.
40. Akiyoshi, D.E.; Denaro, M.; Zhu, H.; Greenstein, J.L.; Banerjee, P.; Fishman, J.A. Identification of a full-length cDNA for an endogenous retrovirus of miniature swine. J. Virol. 1998, 72, 4503-4507.
41. Bartosch, B.; Stefanidis, D.; Myers, R.; Weiss, R.; Patience, C.; Takeuchi, Y. Evidence and consequence of porcine endogenous retrovirus recombination. J. Virol. 2004, 78, 13880-13890.
42. Harrison, I.; Takeuchi, Y.; Bartosch, B.; Stoye, J.P. Determinants of high titer in recombinant porcine endogenous retroviruses. J. Virol. 2004, 78, 13871-13879.
43. Denner, J.; Specke, V.; Thiesen, U.; Karlas, A.; Kurth, R. Genetic alterations of the long terminal repeat of an ecotropic porcine endogenous retrovirus during passage in human cells. Virology 2003, 314, 125-133.
44. Denner, J. Is porcine endogenous retrovirus (PERV) transmission still relevant? Transplant. Proc. 2008, 40, 587-589.
45. Clémenceau, B.; Lalain, S.; Martignat, L.; Saï, P. Porcine endogenous retroviral mRNAs in pancreas and a panel of tissues from specific pathogen-free pigs. Diabetes MeTable 1999, 25, 518-525.
46. Tacke, S.J.; Specke, V.; Denner, J. Differences in release and determination of subtype of porcine endogenous retroviruses produced by stimulated normal pig blood cells. Intervirology 2003, 46, 17-24.
47. Sypniewski, D.; Machnik, G.; Mazurek, U.; Wilczok, T.; Smorag, Z.; Jura, J.; Gajda, B. Distribution of porcine endogenous retroviruses (PERVs) DNA in organs of a domestic pig. Ann. Transplant. 2005, 10, 46-51.
48. Yu, P.; Zhang, L.; Li, S.F.; Cheng, J.Q.; Lu, Y.R.; Zeng, Y.Z.; Li, Y.P.; Bu, H. A rapid method for detection of the copy number of porcine endogenous retrovirus in swine. J. Rapid Meth. Auto. Micro. 2007, 15, 199-205.
49. Prabha, M.S.; Verghese, S. Polymerase chain reaction in detection of porcine endogenous retrovirus (PERV) from porcine tissues. Indian J. Microbiol. 2009, 49, 68-71.
50. Ma, Y.; Yang, Y.; Lv, M.; Yan, Q.; Zheng, L.; Ding, F.; Wu, J.; Tian, K.; Zhang, J. Real-time quantitative polymerase chain reaction with SYBR green I detection for estimating copy numbers of porcine endogenous retrovirus from Chinese miniature pigs. Transplant. Proc. 2010, 42, 1949-1952.
51. Zhang, P.; Yu, P.; Wang, W.; Zhang, L.; Li, S.; Bu, H. An effective method for the quantitative detection of porcine endogenous retrovirus in pig tissues. In Vitro Cell. Dev. Biol. Anim. 2010, 46, 408-410.
52. Bittmann, I.; Mihica, D.; Pleskerm R.; Denner, J. Expression of porcine endogenous retroviruses (PERV) in different organs of a pig. Virology 2012, 433, 329-336.
53. Mazurek, U.; Kimsa, M.C.; Strzalka-Mrozik, B.; Kimsa, M.W.; Adamska, J.; Lipinski, D.; Zeyland, J.; Szalata, M.; Slomski, R.; Jura, J.; et al. Quantitative analysis of porcine endogenous retroviruses in different organs of transgenic pigs generated for xenotransplantation. Curr. Microbiol. 2013, 67, 505-514.
54. Patience, C.; Switzer, W.M.; Takeuchi, Y.; Griffiths, D.J.; Goward, M.E.; Heneine, W.; Stoye, J.P.; Weiss, R.A. Multiple groups of novel retroviral genomes in pigs and related species. J. Virol. 2001, 75, 2771-2775.
55. Klymiuk, N.; Müller, M.; Brem, G.; Aigner, B. Phylogeny, recombination and expression of porcine endogenous retroviruses gamma2 nucleotide sequences. J. Gen. Virol. 2006, 87, 977-986.
56. Lee, J.H.; Webb, G.C.; Allen, R.D.; Moran, C. Characterizing and mapping porcine endogenous retroviruses in Westran pigs. J. Virol. 2002, 76, 5548-5556.
57. Gorbovitskaia, M.; Liu, Z.; Bourgeaux, N.; Li, N.; Lian, Z.; Chardon, P.; Rogel-Gaillard, C. Characterization of two porcine endogenous retrovirus integration loci and variability in pigs. Immunogenetics. 2003, 55, 262-270.
58. Yu, S.L.; Jung, W.Y.; Jung, K.C.; Cho, I.C.; Lim, H.T.; Jin, D.I.; Lee, J.H. Characterization of porcine endogenous retrovirus clones from the NIH miniature pig BAC library. J. Biomed. Biotechnol. 2012, 2012, 482568.
59. Groenen, M.A.; Archibald, A.L.; Uenishi, H.; Tuggle, C.K.; Takeuchi, Y.; Rothschild, M.F.; Rogel-Gaillard, C.; Park, C.; Milan, D.; Megens, H.J.; et al. Analyses of pig genomes provide insight into porcine demography and evolution. Nature 2012, 491, 393-398.
60. Scobie, L.; Taylor, S.; Wood, J.C.; Suling, K.M.; Quinn, G.; Meikle, S.; Patience, C.; Schuurman, H.J.; Onions, D.E. Absence of replication-competent human-tropic porcine endogenous retrovirus in the germ line DNA of inbred miniature swine. J. Virol. 2004, 78, 2502-2509.
61. Wood, J.C.; Quinn, G.; Suling, K.M.; Oldmixon, B.A.; Van Tine, B.A.; Cina, R.; Arn, S.; Huang, C.; Scobie, L.; Onions, D.; et al. Identification of exogenous forms of human-tropic porcine endogenous retrovirus in miniature swine. J. Virol. 2004, 78, 2494-2501.
62. Scobie, L.; Taylor, S.; Logan, N.A.; Meikle, S.; Onions, D.; Patience, C.; Quinn, G. Characterization of germline porcine endogenous retroviruses from Large White pig. J. Gen. Virol. 2004, 85, 2421-2428.
63. Martin, S.I.; Wilkinson, R.; Fishman, J.A. Genomic presence of recombinant porcine endogenous retrovirus in transmitting miniature swine. Virol. J. 2006, 3, 91.
64. Herring, C.; Quinn, G.; Bower, R.; Parsons, N.; Logan, N.A.; Brawley, A.; Elsome, K.; Whittam, A.; Fernandez-Suarez, X.M.; Cunningham, D.; et al. Mapping full-length porcine endogenous retroviruses in a large white pig. J. Virol. 2001, 75, 12252-12265.
65. Machnik, G.; Sypniewski, D.; Wydmuch, Z.; Cholewa, K.; Mazurek, U.; Wilczok, T.; Smorag, Z.; Pacha, J. Sequence analysis of proviral DNA of porcine endogenous retroviruses. Transplant. Proc. 2005, 37, 4610-4614.
66. Pal, N.; Baker, R.; Schalk, S.; Scobie, L.; Tucker, A.W.; Opriessnig, T. Detection of porcine endogenous retrovirus (PERV) viremia in diseased versus healthy US pigs by qualitative and quantitative real-time RT-PCR. Transbound. Emerg. Dis. 2011, 58, 344-351.
67. Dieckhoff, B.; Puhlmann, J.; Büscher, K.; Hafner-Marx, A.; Herbach, N.; Bannert, N.; Büttner, M.; Wanke, R.; Kurth, R.; Denner, J. Expression of porcine endogenous retroviruses (PERVs) in melanomas of Munich miniature swine (MMS) Troll. Vet. Microbiol. 2007, 123, 53-68.
68. Denner, J.; Schuurman, H.J.; Patience, C. The International Xenotransplantation Association consensus statement on conditions for undertaking clinical trials of porcine islet products in type 1 diabetes-Chapter 5: Strategies to prevent transmission of porcine endogenous retroviruses. Xenotransplantation. 2009, 16, 239-248.
69. Deng, Y.M.; Tuch, B.E.; Rawlinson, W.D. Transmission of porcine endogenous retroviruses in severe combined immunodeficient mice xenotransplanted with fetal porcine pancreatic cells. Transplantation 2000, 70, 1010-1016.
70. Van der Laan, L.J.; Lockey, C.; Griffeth, B.C.; Frasier, F.S.; Wilson, C.A.; Onions, D.E.; Hering, B.J.; Long, Z.; Otto, E.; Torbett, B.E.; et al. Infection by porcine endogenous retrovirus after islet xenotransplantation in SCID mice. Nature 2000, 407, 90-94.
71. Clémenceau, B.; Jégou, D.; Martignat, L.; Saï, P. Microchimerism and transmission of porcine endogenous retrovirus from a pig cell line or specific pathogen-free pig islets to mouse tissues and human cells during xenografts in nude mice. Diabetologia 2002, 45, 914-923.
72. Yu, P.; Zhang, L.; Li, S.F.; Cheng, J.Q.; Lu, Y.R.; Li, Y.P.; Bu, H. Transmission of porcine endogenous retrovirus to human cells in nude mouse. Acta Virol. 2008, 52, 257-260.
73. Kuddus, R.H.; Metes, D.M.; Nalesnik, M.A.; Logar, A.J.; Rao, A.S.; Fung, J.J. Porcine cell microchimerism but lack of productive porcine endogenous retrovirus (PERV) infection in naive and humanized SCID-beige mice treated with porcine peripheral blood mononuclear cells. Transpl. Immunol. 2004, 13, 15-24.
74. Yang, Y.G.; Wood, J.C.; Lan, P.; Wilkinson, R.A.; Sykes, M.; Fishman, J.A.; Patience, C. Mouse retrovirus mediates porcine endogenous retrovirus transmission into human cells in long-term human-porcine chimeric mice. J. Clin. Invest. 2004, 114, 695-700.
75. Irgang, M.; Karlas, A.; Laue, C.; Specke, V.; Tacke, S.J.; Kurth, R.; Schrezenmeir, J.; Denner, J. Porcine endogenous retroviruses PERV-A and PERV-B infect neither mouse cells in vitro nor SCID mice in vivo. Intervirology 2005, 48, 167-173.
76. Martina, Y.; Kurian, S.; Cherqui, S.; Evanoff, G.; Wilson, C.; Salomon, D.R. Pseudotyping of porcine endogenous retrovirus by xenotropic murine leukemia virus in a pig islet xenotransplantation model. Am. J. Transplant. 2005, 5, 1837-1847.
77. Argaw, T.; Figueroa, M.; Salomon, D.R.; Wilson, C.A. Identification of residues outside of the receptor binding domain that influence the infectivity and tropism of porcine endogenous retrovirus. J. Virol. 2008, 82, 7483-7491.
78. Cyganek-Niemiec, A.; Strzalka-Mrozik, B.; Pawlus-Lachecka, L.; Wszolek, J.; Adamska, J.; Kudrjavtseva, J.; Zhuravleva, I.; Kimsa, M.; Okla, H.; Kimsa, M.; et al. The degradation effect of diepoxide fixation on porcine endogenous retrovirus DNA in heart valves-Molecular aspects. Int. J. Artif. Organs 2012, 35, 25-33.
79. Li, Z.G.; Liu, G.B.; Pan, M.X.; Wu, Q.S.; Ge, M.; Du, J.; Wang, Y.; Gao, Y. Knockdown of porcine endogenous retroviruses by RNA interference in Chinese experimental miniature pig fibroblasts. Transplant. Proc. 2013, 45, 748-755.
80. Herring, C.; Cunningham, D.A.; Whittam, A.J.; Fernandez-Suárez, X.M.; Langford, G.A. Monitoring xenotransplant recipients for infection by PERV. Clin. Biochem. 2001, 34, 23-27.
81. Moalic, Y.; Blanchard, Y.; Félix, H.; Jestin, A. Porcine endogenous retrovirus integration sites in the human genome: Features in common with those of murine leukemia virus. J. Virol. 2006, 80, 10980-10988.
82. Moalic, Y.; Félix, H.; Takeuchi, Y.; Jestin, A.; Blanchard, Y. Genome areas with high gene density and CpG island neighborhood strongly attract porcine endogenous retrovirus for integration and favor the formation of hot spots. J. Virol. 2009, 83, 1920-1929.
83. U.S. Food and Drug Administration. Draft Guidance for Industry: Source Animal, Product, Preclinical and Clinical Issues Concerning the Use of Xenotransplantation Products in Humans. Fed. Regist. 2003, 68, 16542-16543.
84. Prabha, S.; Verghese, S. Existence of proviral porcine endogenous retrovirus in fresh and decellularised porcine tissues. Indian J. Med. Micro. 2008, 26, 228-232.
85. Kim, J.H.; Jung, E.S.; Hwang, E.S. Detection of human cytomegalovirus (HCMV) and porcine endogenous retrovirus (PERV) with one step extraction method. Infect. Chemother. 2010, 42, 12-16.
86. Wang, H.H.; Wang, Y.J.; Liu, H.L.; Liu, J.; Huang, Y.P.; Guo, H.T.; Wang, Y.M. Detection of PERV by polymerase chain reaction and its safety in bioartificial liver support system. World J. Gastroenterol. 2006, 12, 1287-1291.
87. Wynyard, S.; Garkavenko, O.; Elliot, R. Multiplex high resolution melting assay for estimation of porcine endogenous retrovirus (PERV) relative gene dosage in pigs and detection of PERV infection in xenograft recipients. J. Virol. Methods 2011, 175, 95-100.
88. Argaw, T.; Ritzhaupt, A.; Wilson, C.A. Development of a real time quantitative PCR assay for detection of porcine endogenous retrovirus. J. Virol. Methods 2002, 106, 97-106.
89. Bösch, S.; Arnauld, C.; Jestin, A. Study of full-length porcine endogenous retrovirus genomes with envelope gene polymorphism in a specific-pathogen-free Large White swine herd. J. Virol. 2000, 74, 8575-8581.
90. Mang, R.; Maas, J.; Chen, X.; Goudsmit, J.; van Der Kuyl, A.C. Identification of a novel type C porcine endogenous retrovirus: Evidence that copy number of endogenous retroviruses increases during host inbreeding. J. Gen. Virol. 2001, 82, 1829-1834.
91. Kim, J.H.; Choi, E.Y.; Jung, E.S.; Kwon, Y.; Lee, D.S.; Hwang, D.Y.; Hwang, E.S. Characterization of clones of human cell line infected with porcine endogenous retrovirus (PERV) from porcine cell line, PK-15. Infect. Chemother. 2009, 41, 1-8.
92. Ma, Y.; Lv, M.; Xu, S.; Wu, J.; Tian, K.; Zhang, J. Identification of full-length proviral DNA of porcine endogenous retrovirus from Chinese Wuzhishan miniature pigs inbred. Comp. Immunol. Microbiol. Infect. Dis. 2010, 33, 323-331.
93. Chun, J.Y.; Kim, K.J.; Hwang, I.T.; Kim, Y.J.; Lee, D.H.; Lee, I.K.; Kim, J.K. Dual priming oligonucleotide system for the multiplex detection of respiratory viruses and SNP genotyping of CYP2C19 gene. Nucleic Acids Res. 2007, 35, e40.
94. Moon, H.J.; Park, S.J.; Kim, H.K.; Ann, S.K.; Rho, S.; Keum, H.O.; Park, B.K. Simultaneous detection and subtyping of porcine endogenous retroviruses proviral DNA using the dual priming oligonucleotide system. J. Vet. Sci. 2010, 11, 269-271.
95. Oldmixon, B.A.; Wood, J.C.; Ericsson, T.A.; Wilson, C.A.; White-Scharf, M.E.; Andersson, G.; Greenstein, J.L.; Schuurman, H.J.; Patience, C. Porcine endogenous retrovirus transmission characteristics of an inbred herd of miniature swine. J. Virol. 2002, 76, 3045-3048.
96. Jung, K.C.; Yu, S.L.; Kim, T.H.; Jeon, J.T.; Rogel-Gaillard, C.; Park, S.; Jin, D.I.; Moran, C.; Lee, J.H. Insertional variations of two porcine endogenous retroviruses (PERVs) in Korean native pigs and Asian wild boars. Asian Aust. J. Anim. Sci. 2007, 20, 461-465.
97. Niebert, M.; Tönjes, R.R. Analyses of prevalence and polymorphisms of six-replication competent and chromosomally assigned porcine endogenous retroviruses in individual pigs and pig subspecies. Virology 2003, 313, 427-434.
98. Scheef, G.; Fischer, N.; Krach, U.; Tönjes, R.R. The number of a U3 repeat box acting as an enhancer in long terminal repeats of polytropic replication-competent porcine endogenous retroviruses dynamically fluctuates during serial virus passages in human cells. J. Virol. 2001, 75, 6933-6940.
99. Wilson, C.A.; Laeeq, S.; Ritzhaupt, A.; Colon-Moran, W.; Yoshimura, F.K. Sequence analysis of porcine endogenous retrovirus long terminal repeats and identification of transcriptional regulatory regions. J. Virol. 2003, 77, 142-149.
100. DesGroseillers, L.; Jolicoeur, P. The tandem direct repeats within the long terminal repeat of murine leukemia viruses are the primary determinant of their leukemogenic potential. J. Virol. 1984, 52, 945-952.
101. Athas, G.B.; Choi, B.; Prabhu, S.; Lobelle-Rich, P.A.; Levy, L.S. Genetic determinants of feline leukemia virus-induced multicentric lymphomas. Virology 1995, 214, 431-438.
102. Denner, J.; Young, P.R. Koala retroviruses: Characterization and impact on the life of koalas. Retrovirology 2013, 10, 108.
103. Jung, K.C.; Simond, D.M.; Moran, C.; Hawthorne, W.J.; Jeon, J.T.; Jin, D.I.; Lee, J.H. Investigation of deletion variation and methylation patterns in the 5' LTR of porcine endogenous retroviruses. Asian Aust. J. Anim. Sci. 2008, 21, 1572-1584.
104. Jung, Y.D.; Lee, J.R.; Kim, Y.J.; Ha, H.S.; Oh, K.B.; Im, G.S.; Choi, B.H.; Kim, H.S. Promoter activity analysis and methylation characterization of LTR elements of PERVs in NIH miniature pig. Genes Genet. Syst. 2013, 88, 135-142.
105. Jung, Y.D.; Ha, H.S.; Park, S.J.; Oh, K.B.; Im, G.S.; Kim, T.H.; Seong, H.H.; Kim, H.S. Identification and promoter analysis of PERV LTR subtypes in NIH-miniature pig. Mol. Cells 2013, 35, 99-105.
106. Matousková, M.; Vesely, P.; Daniel, P.; Mattiuzzo, G.; Hector, R.D.; Scobie, L.; Takeuchi, Y.; Hejnar, J. Role of DNA methylation in expression and transmission of porcine endogenous retroviruses. J. Virol. 2013, 87, 12110-12120.
107. Park, S.J.; Huh, J.W.; Kim, D.S.; Ha, H.S.; Jung, Y.D.; Ahn, K.; Oh, K.B.; Park, E.W.; Chang, K.T.; Kim, H.S. Analysis of the molecular and regulatory properties of active porcine endogenous retrovirus gamma-1 long terminal repeats in kidney tissues of the NIH-Miniature pig. Mol. Cells 2010, 30, 319-325.
108. Ha, H.S.; Lee, Y.C.; Park, S.J.; Jung, Y.D.; Ahn, K.; Moon, J.W.; Han, K.; Oh, K.B.; Kim, T.H.; Seong, H.H.; et al. In vitro CpG methylation and garcinol reduce PERV LTR promoter activity. Genes Genomics 2012, 34, 217-222.
109. Nakaya, Y.; Shojima, T.; Yasuda, J.; Imakawa, K.; Miyazawa, T. Epigenetic regulation on the 5'-proximal CpG island of human porcine endogenous retrovirus subgroup A receptor 2/GPR172B. Microbes Infect. 2011, 13, 49-57.
110. Moon, H.J.; Kim, H.K.; Park, S.J.; Lee, C.S.; Song, D.S.; Kang, B.K.; Park, B.K. Comparison of the age-related porcine endogenous retrovirus (PERV) expression using duplex RT-PCR. J. Vet. Sci. 2009, 10, 317-322.
111. Chung, H.C.; Nguyen, V.G.; Moon, H.J.; Kim, H.K.; Park, S.J.; Lee, J.H.; Choi, M.G.; Kim, A.R.; Park, B.K. Inhibition of porcine endogenous retrovirus in PK15 cell line by efficient multitargeting RNA interference. Transpl. Int. 2014, 27, 96-105.
112. Karlas, A.; Kurth, R.; Denner, J. Inhibition of porcine endogenous retroviruses by RNA interference: Increasing the safety of xenotransplantation. Virology 2004, 325, 18-23.
113. Miyagawa, S.; Nakatsu, S.; Nakagawa, T.; Kondo, A.; Matsunami, K.; Hazama, K.; Yamada, J.; Tomonaga, K.; Miyazawa, T.; Shirakura, R. Prevention of PERV infections in pig to human xenotransplantation by the RNA interference silences gene. J. Biochem. 2005, 137, 503-508.
114. Dieckhoff, B.; Petersen, B.; Kues, W.A.; Kurth, R.; Niemann, H.; Denner, J. Knockdown of porcine endogenous retrovirus (PERV) expression by PERV-specific shRNA in transgenic pigs. Xenotransplantation 2008, 15, 36-45.
115. Ramsoondar, J.; Vaught, T.; Ball, S.; Mendicino, M.; Monahan, J.; Jobst, P.; Vance, A.; Duncan, J.; Wells, K.; Ayares, D. Production of transgenic pigs that express porcine endogenous retrovirus small interfering RNAs. Xenotransplantation 2009, 16, 164-180.
116. Bustin, S.A.; Mueller, R. Real-time reverse transcription PCR (qRT-PCR) and its potential use in clinical diagnosis. Clin. Sci. 2005, 109, 365-379.
117. Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-. CT method. Methods 2001, 25, 402-408.
118. Nygard, A.B.; Jørgensen, C.B.; Cirera, S.; Fredholm, M. Selection of reference genes for gene expression studies in pig tissues using SYBR green qPCR. BMC Mol. Biol. 2007, 8, 67.
119. Svobodová, K.; Bílek, K.; Knoll, A. Verification of reference genes for relative quantification of gene expression by real-time reverse transcription PCR in the pig. J. Appl. Genet. 2008, 49, 263-265.
120. Dieckhoff, B.; Kessler, B.; Jobst, D.; Kues, W.; Petersen, B.; Pfeifer, A.; Kurth, R.; Niemann, H.; Wolf, E.; Denner, J. Distribution and expression of porcine endogenous retroviruses in multi-transgenic pigs generated for xenotransplantation. Xenotransplantation 2009, 16, 64-73.
121. Kaulitz, D.; Mihica, D.; Dorna, J.; Rodrigues Costa, M.; Petersen, B.; Niemann, H.; Tönjes, R.R.; Denner, J. Development of sensitive methods for detection of porcine endogenous retrovirus-C (PERV-C) in the genome of pigs. J. Virol. Methods 2011, 175, 60-65.
122. Smith, R.A. Contamination of clinical specimens with MLV-encoding nucleic acids: Implications for XMRV and other candidate human retroviruses. Retrovirology 2010, 7, 112.
123. EASL international consensus conference on hepatitis B, 13-14 September 2002, Geneva, Switzerland, consensus statement (short version). J. Hepatol. 2003, 38, 533-540.
124. Bustin, S.A. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol. 2000, 25, 169-193.
125. Bustin, S.A. Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): Trends and problems. J. Mol. Endocrinol. 2002, 29, 23-39.
126. Karlas, A.; Irgang, M.; Votteler, J.; Specke, V.; Ozel, M.; Kurth, R.; Denner, J. Characterisation of a human cell-adapted porcine endogenous retrovirus PERV-A/C. Ann. Transplant. 2010, 15, 45-54.
127. Liu, Q.; Liu, Z.; Dalakas, E. Prevalence of porcine endogenous retrovirus in Chinese pig breeds and in patients treated with a porcine liver cell-based bioreactor. World J. Gastroenterol. 2005, 11, 4727-4730.
128. Krach, U.; Fischer, N.; Czauderna, F.; Tönjes, R.R. Comparison of replication-competent molecular clones of porcine endogenous retrovirus class A and class B derived from pig and human cells. J. Virol. 2001, 75, 5465-5472.
129. Takefman, D.M.; Spear, G.T.; Saifuddin, M.; Wilson, C.A. Human CD59 incorporation into porcine endogenous retrovirus particles: Implications for the use of transgenic pigs for xenotransplantation. J. Virol. 2002, 76, 1999-2002.
130. Hector, R.D.; Meickle, S.; Grant, L.; Wilkinson, R.A.; Fishman, J.A.; Scobie, L. Pre-screening of miniature swine may reduce the risk of transmitting human tropic recombinant porcine endogenous retroviruses. Xenotransplantation 2007, 14, 222-226.
131. Li, Z.; Ping, Y.; Shengfu, L.; Youping, L.; Jingqiu, C.; Hong, B. In vivo screening of porcine endogenous retrovirus in Chinese Banna minipig inbred. Transplant. Proc. 2006, 38, 2261-2263.
132. Xing, X.W.; Hawthorne, W.J.; Yi, S.; Simond, D.M.; Dong, Q.; Ye, B.; Tong, Q.J.; Ye, Z.; Wang, W. Investigation of porcine endogenous retrovirus in the conservation population of Ningxiang pig. Transplant. Proc. 2009, 41, 4389-4393.
133. Blusch, J.H.; Roos, C.; Nitschko, H. A polymerase chain reaction-based protocol for the detection of transmission of pig endogenous retroviruses in pig to human xenotransplantation. Transplantation 2000, 69, 2167-2172.
134. Garkavenko, O.; Durbin, K.; Tan, P.; Elliott, R. Islets transplantation: New Zealand experience. Xenotransplantation 2011, 18, doi:10.1111/j.1399-3089.2010.00607_3.x.
135. Kaulitz, D.; Fiebig, U.; Eschrichtm, M.; Wurzbacher, C.; Kurth, R.; Denner, J. Generation of neutralising antibodies against porcine endogenous retroviruses (PERVs). Virology 2011, 411, 78-86.
136. Lee, J.E.; Kim, G.W.; Kim, Y.B.; Park, H.Y. Construction of the porcine endogenous retrovirus envelope glycoprotein A and B specific antibody. J. Bacteriol. Virol. 2009, 39, 137-143.
137. Tacke, S.J.; Bodusch, K.; Berg, A.; Denner, J. Sensitive and specific immunological detection methods for porcine endogenous retroviruses applicable to experimental and clinical xenotransplantation. Xenotransplantation 2001, 8, 125-135.
138. Chiang, C.Y.; Chang, J.T.; Lin, M.S.; Wang, S.R.; Chang, H.Y. Characterization of a monoclonal antibody specific to the Gag protein of porcine endogenous retrovirus and its application in detecting the virus infection. Virus Res. 2005, 108, 139-148.
139. Jones, J.O.; Arvin, A.M. Microarray analysis of host cell gene transcription in response to varicella-zoster virus infection of human T cells and fibroblasts in vitro and SCIDhu skin xenografts in vivo. J. Virol. 2003, 77, 1268-1280.
140. Woodhouse, S.D.; Narayan, R.; Latham, S.; Lee, S.; Antrobus, R.; Gangadharan, B.; Luo, S.; Schroth, G.P.; Klenerman, P.; Zitzmann, N. Transcriptome sequencing, microarray, and proteomic analyses reveal cellular and metabolic impact of hepatitis C virus infection in vitro. Hepatology 2010, 52, 443-453.
141. Wang, D.; Coscoy, L.; Zylberberg, M.; Avila, P.C.; Boushey, H.A.; Ganem, D.; DeRisi, J.L. Microarray-based detection and genotyping of viral pathogens. Proc. Natl. Acad. Sci. USA 2002, 99, 15687-15692.
142. Seifarth, W.; Spiess, B.; Zeilfelder, U.; Speth, C.; Hehlmann, R.; Leib-Mösch, C. Assessment of retroviral activity using a universal retrovirus chip. J. Virol. Methods 2003, 112, 79-91.
143. Tan, S.L.; Ganji, G.; Paeper, B.; Proll, S.; Katze, M.G. Systems biology and the host response to viral infection. Nat. Biotechnol. 2007, 25, 1383-1389.
144. Fishman, J.A.; Scobie, L.; Takeuchi, Y. Xenotransplantation-associated infectious risk: A WHO consultation. Xenotransplantation 2012, 19, 72-81.
145. Kimsa, M.C.; Strzalka-Mrozik, B.; Kimsa, M.W.; Kruszniewska-Rajs, C.; Gola, J.; Adamska, J.; Rajs, A.; Mazurek, U. Porcine endogenous retrovirus infection changes the expression of inflammation-related genes in lipopolysaccharide-stimulated human dermal fibroblasts. Ann. Transplant. 2013, 18, 576-586.