1887

Abstract

Two pig endogenous retroviruses (PERV), PERV-A and -B, productively infect human cells and are therefore considered to constitute a potential risk in pig-to-human xenotransplantation. A PCR-based cloning technique to isolate infectious PERV proviruses was established. Overlapping 3′ half and 5′ halves of PERV proviral genomes were amplified using DNA extracted from human 293 cells infected with PERV-A or -B. These clones were fused at a unique restriction site in the overlapping region and tested for their infectivity. Representative constructs possessed the same infectious properties as their parent isolates. We also developed a polyclonal anti-PERV serum by using recombinant PERV capsid protein derived from one of the infectious constructs as immunogen and established an immunocytological method for detection and titration of PERV infection. This detection method proved to be more sensitive than the current method of choice (transfer of MLV- vectors) for infectivity assessment of PERV. These findings should be considered for future characterization of PERV isolates.

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2002-09-01
2019-10-16
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References

  1. Akiyoshi, D. E., Denaro, M., Zhu, H., Greenstein, J. L., Banerjee, P. & Fishman, J. A. ( 1998; ). Identification of a full-length cDNA for an endogenous retrovirus of miniature swine. Journal of Virology 72, 4503-4507.
    [Google Scholar]
  2. Armstrong, J. A., Porterfield, J. S. & De Madrid, A. T. ( 1971; ). C-type virus particles in pig kidney cell lines. Journal of General Virology 10, 195-198.[CrossRef]
    [Google Scholar]
  3. Birmingham, K. ( 1999; ). FDA subcommittee finds no evidence of PERV transmission. Nature Medicine 5, 855.
    [Google Scholar]
  4. Blusch, J. H., Patience, C., Takeuchi, Y., Templin, C., Roos, C., Von Der Helm, K., Steinhoff, G. & Martin, U. ( 2000; ). Infection of nonhuman primate cells by pig endogenous retrovirus. Journal of Virology 74, 7687-7690.[CrossRef]
    [Google Scholar]
  5. Bosch, S., Arnauld, C. & Jestin, A. ( 2000; ). Study of full-length porcine endogenous retrovirus genomes with envelope gene polymorphism in a specific-pathogen-free Large White swine herd. Journal of Virology 74, 8575-8581.[CrossRef]
    [Google Scholar]
  6. Breese, S. S.Jr ( 1970; ). Virus-like particles occurring in cultures of stable pig kidney cell lines. Archiv für die Gesamte Virusforschung 30, 401-404.[CrossRef]
    [Google Scholar]
  7. Colicelli, J. & Goff, S. P. ( 1986; ). Isolation of a recombinant murine leukemia virus utilizing a new primer tRNA. Journal of Virology 57, 37-45.
    [Google Scholar]
  8. Cozzi, E., Masroor, S., Soin, B., Vial, C. & White, D. J. ( 2000; ). Progress in xenotransplantation. Clinical Nephrology 53, 13-18.
    [Google Scholar]
  9. Czauderna, F., Fischer, N., Boller, K., Kurth, R. & Tonjes, R. R. ( 2000; ). Establishment and characterization of molecular clones of porcine endogenous retroviruses replicating on human cells. Journal of Virology 74, 4028-4038.[CrossRef]
    [Google Scholar]
  10. Deng, Y. M., Tuch, B. E. & Rawlinson, W. D. ( 2000; ). Transmission of porcine endogenous retroviruses in severe combined immunodeficient mice xenotransplanted with fetal porcine pancreatic cells. Transplantation 70, 1010-1016.[CrossRef]
    [Google Scholar]
  11. Dinsmore, J. H., Manhart, C., Raineri, R., Jacoby, D. B. & Moore, A. ( 2000; ). No evidence for infection of human cells with porcine endogenous retrovirus (PERV) after exposure to porcine fetal neuronal cells. Transplantation 70, 1382-1389.[CrossRef]
    [Google Scholar]
  12. Ericsson, T., Oldmixon, B., Blomberg, J., Rosa, M., Patience, C. & Andersson, G. ( 2001; ). Identification of novel porcine endogenous betaretrovirus sequences in miniature swine. Journal of Virology 75, 2765-2770.[CrossRef]
    [Google Scholar]
  13. 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. ( 1998; ). No evidence of infection with porcine endogenous retrovirus in recipients of porcine islet-cell xenografts. Lancet 352, 695-699.[CrossRef]
    [Google Scholar]
  14. Heneine, W., Switzer, W. M., Soucie, J. M., Evatt, B. L., Shanmugam, V., Rosales, G. V., Matthews, A., Sandstrom, P. & Folks, T. M. ( 2001; ). Evidence of porcine endogenous retroviruses in porcine factor VIII and evaluation of transmission to recipients with hemophilia. Journal of Infectious Diseases 183, 648-652.[CrossRef]
    [Google Scholar]
  15. Herring, C., Cunningham, D. A., Whittam, A. J., Fernandez-Suarez, M. & Langford, G. A. ( 2001; ). Monitoring xenotransplant recipients for infection by PERV. Clinical Biochemistry 34, 23-27.[CrossRef]
    [Google Scholar]
  16. Krach, U., Fischer, N., Czauderna, F., Kurth, R. & Tonjes, R. R. ( 2000; ). Generation and testing of a highly specific anti-serum directed against porcine endogenous retrovirus nucleocapsid. Xenotransplantation 7, 221-229.[CrossRef]
    [Google Scholar]
  17. Krach, U., Fischer, N., Czauderna, F. & Tonjes, R. R. ( 2001; ). Comparison of replication-competent molecular clones of porcine endogenous retrovirus class A and class B derived from pig and human cells. Journal of Virology 75, 5465-5472.[CrossRef]
    [Google Scholar]
  18. Le Tissier, P., Stoye, J. P., Takeuchi, Y., Patience, C. & Weiss, R. A. ( 1997; ). Two sets of human-tropic pig retrovirus. Nature 389, 681-682.[CrossRef]
    [Google Scholar]
  19. Lund, A. H., Duch, M. & Pedersen, F. S. ( 2000; ). Selection of functional tRNA primers and primer binding site sequences from a retroviral combinatorial library: identification of new functional tRNA primers in murine leukemia virus replication. Nucleic Acids Research 28, 791-799.[CrossRef]
    [Google Scholar]
  20. Mang, R., Goudsmit, J. & van der Kuyl, A. C. ( 1999; ). Novel endogenous type C retrovirus in baboons: complete sequence, providing evidence for baboon endogenous virus gag–pol ancestry. Journal of Virology 73, 7021-7026.
    [Google Scholar]
  21. Martin, U., Kiessig, V., Blusch, J. H., Haverich, A., von der Helm, K., Herden, T. & Steinhoff, G. ( 1998a; ). Expression of pig endogenous retrovirus by primary porcine endothelial cells and infection of human cells. Lancet 352, 692-694.[CrossRef]
    [Google Scholar]
  22. Martin, U., Steinhoff, G., Kiessig, V., Chikobava, M., Anssar, M., Morschheuser, T., Lapin, B. & Haverich, A. ( 1998b; ). Porcine endogenous retrovirus (PERV) was not transmitted from transplanted porcine endothelial cells to baboons in vivo. Transplantation International 11, 247-251.[CrossRef]
    [Google Scholar]
  23. Martin, U., Winkler, M. E., Id, M., Radecke, H., Arseniev, L., Groteluschen, R., Simon, A. R. & Steinhoff, G. ( 2000a; ). Transmission of pig endogenous retrovirus to primary human cells. Transplantation Proceedings 32, 1157.[CrossRef]
    [Google Scholar]
  24. Martin, U., Winkler, M. E., Id, M., Radeke, H., Arseniev, L., Takeuchi, Y., Simon, A. R., Patience, C., Haverich, A. & Steinhoff, G. ( 2000b; ). Productive infection of primary human endothelial cells by pig endogenous retrovirus (PERV). Xenotransplantation 7, 138-142.[CrossRef]
    [Google Scholar]
  25. Nikbakht, K. N., Ou, C. Y., Boone, L. R., Glover, P. L. & Yang, Z. K. ( 1985; ). Nucleotide sequence analysis of endogenous murine leukemia virus-related proviral clones reveals primer-binding sites for glutamine tRNA. Journal of Virology 54, 889-893.
    [Google Scholar]
  26. Paradis, K., Langford, G., Long, Z., Heneine, W., Sandstrom, P., Switzer, W. M., Chapman, L. E., Lockey, C., Onions, D. & Otto, E. ( 1999; ). Search for cross-species transmission of porcine endogenous retrovirus in patients treated with living pig tissue. Science 285, 1236-1241.[CrossRef]
    [Google Scholar]
  27. Patience, C., Takeuchi, Y. & Weiss, R. A. ( 1997; ). Infection of human cells by an endogenous retrovirus of pigs. Nature Medicine 3, 282-286.[CrossRef]
    [Google Scholar]
  28. Patience, C., Patton, G. S., Takeuchi, Y., Weiss, R. A., McClure, M. O., Rydberg, L. & Breimer, M. E. ( 1998; ). No evidence of pig DNA or retroviral infection in patients with short- term extracorporeal connection to pig kidneys. Lancet 352, 699-701.[CrossRef]
    [Google Scholar]
  29. Patience, C., Switzer, W. M., Takeuchi, Y., Griffiths, D. J., Goward, M. E., Heneine, W., Stoye, J. P. & Weiss, R. A. ( 2001; ). Multiple groups of novel retroviral genomes in pigs and related species. Journal of Virology 75, 2771-2775.[CrossRef]
    [Google Scholar]
  30. Petersen, R., Kempler, G. & Barklis, E. ( 1991; ). A stem cell-specific silencer in the primer-binding site of a retrovirus. Molecular Cell Biology 11, 1214-1221.
    [Google Scholar]
  31. Pitkin, Z. & Mullon, C. ( 1999; ). Evidence of absence of porcine endogenous retrovirus (PERV) infection in patients treated with a bioartificial liver support system. Artificial Organs 23, 829-833.[CrossRef]
    [Google Scholar]
  32. Platt, J. L. ( 2000; ). Xenotransplantation. New risks, new gains. Nature 407, 27, 29–30.[CrossRef]
    [Google Scholar]
  33. Qari, S. H., Magre, S., Garcia-Lerma, J. G., Hussain, A. I., Takeuchi, Y., Patience, C., Weiss, R. A. & Heneine, W. ( 2001; ). Susceptibility of the porcine endogenous retrovirus to reverse transcriptase and protease inhibitors. Journal of Virology 75, 1048-1053.[CrossRef]
    [Google Scholar]
  34. Scheef, G., Fischer, N., Krach, U. & Tonjes, R. R. ( 2001; ). 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. Journal of Virology 75, 6933-6940.[CrossRef]
    [Google Scholar]
  35. Simmons, G., McKnight, A., Takeuchi, Y., Hoshino, H. & Clapham, P. R. ( 1995; ). Cell-to-cell fusion, but not virus entry in macrophages by T-cell line tropic HIV-1 strains: a V3 loop-determined restriction. Virology 209, 696-700.[CrossRef]
    [Google Scholar]
  36. Sprinzel, M., Vassilenko, K. S., Emmerich, J. & Bauer, F. (1999). Compilation of tRNA sequences and sequences of tRNA genes. http/uni-bayreuth.de/departments/biochemie/trna/, r1–r54.
  37. Stephan, O., Schwendemann, J., Specke, V., Tacke, S. J., Boller, K. & Denner, J. ( 2001; ). Porcine endogenous retroviruses (PERVs): generation of specific antibodies, development of an immunoperoxidase assay (IPA) and inhibition by AZT. Xenotransplantation 8, 310-316.[CrossRef]
    [Google Scholar]
  38. Switzer, W. M., Shanmugam, V., Chapman, L. & Heneine, W. ( 1999; ). Polymerase chain reaction assays for the diagnosis of infection with the porcine endogenous retrovirus and the detection of pig cells in human and nonhuman recipients of pig xenografts. Transplantation 68, 183-188.[CrossRef]
    [Google Scholar]
  39. Tacke, S. J., Bodusch, K., Berg, A. & Denner, J. ( 2001; ). Sensitive and specific immunological detection methods for porcine endogenous retroviruses applicable to experimental and clinical xenotransplantation. Xenotransplantation 8, 125-135.
    [Google Scholar]
  40. Takeuchi, Y. & Weiss, R. A. ( 2000; ). Xenotransplantation: reappraising the risk of retroviral zoonosis. Current Opinion in Immunology 12, 504-507.[CrossRef]
    [Google Scholar]
  41. Takeuchi, Y., Cosset, F. L., Lachmann, P. J., Okada, H., Weiss, R. A. & Collins, M. K. ( 1994; ). Type C retrovirus inactivation by human complement is determined by both the viral genome and the producer cell. Journal of Virology 68, 8001-8007.
    [Google Scholar]
  42. Takeuchi, Y., Patience, C., Magre, S., Weiss, R. A., Banerjee, P. T., Le Tissier, P. & Stoye, J. P. ( 1998; ). Host range and interference studies of three classes of pig endogenous retrovirus. Journal of Virology 72, 9986-9991.
    [Google Scholar]
  43. Templin, C., Schroder, C., Simon, A. R., Laaff, G., Kohl, J., Chikobava, M., Lapin, B., Steinhoff, G. & Martin, U. ( 2000; ). Analysis of potential porcine endogenous retrovirus transmission to baboon in vitro and in vivo. Transplantation Proceedings 32, 1163-1164.[CrossRef]
    [Google Scholar]
  44. Todaro, G. J., Benveniste, R. E., Lieber, M. M. & Sherr, C. J. ( 1974; ). Characterization of a type C virus released from the porcine cell line PK(15). Virology 58, 65-74.[CrossRef]
    [Google Scholar]
  45. van der Kuyl, A. C., Dekker, J. T. & Goudsmit, J. ( 1999; ). Discovery of a new endogenous type C retrovirus (FcEV) in cats: evidence for RD-114 being an FcEV(Gag–Pol)/baboon endogenous virus BaEV(Env) recombinant. Journal of Virology 73, 7994-8002.
    [Google Scholar]
  46. 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. & Salomon, D. R. ( 2000; ). Infection by porcine endogenous retrovirus after islet xenotransplantation in SCID mice. Nature 407, 90-94.[CrossRef]
    [Google Scholar]
  47. Wilson, C. A., Wong, S., Muller, J., Davidson, C. E., Rose, T. M. & Burd, P. ( 1998; ). Type C retrovirus released from porcine primary peripheral blood mononuclear cells infects human cells. Journal of Virology 72, 3082-3087.
    [Google Scholar]
  48. Wilson, C. A., Wong, S., VanBrocklin, M. & Federspiel, M. J. ( 2000; ). Extended analysis of the in vitro tropism of porcine endogenous retrovirus. Journal of Virology 74, 49-56.[CrossRef]
    [Google Scholar]
  49. Winkler, M. E., Martin, U., Loss, M., Arends, H., Rensing, S., Kaup, F. J., Hedrich, H. J., Klempnauer, J. & Winkler, M. ( 2000; ). Porcine endogenous retrovirus is not transmitted in a discordant porcine-to-cynomolgus xenokidney transplantation model with long-term survival of organ recipients. Transplantation Proceedings 32, 1162.[CrossRef]
    [Google Scholar]
  50. Yamauchi, M., Freitag, B., Khan, C., Berwin, B. & Barklis, E. ( 1995; ). Stem cell factor binding to retrovirus primer binding site silencers. Journal of Virology 69, 1142-1149.
    [Google Scholar]
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