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Endogenousenv elements: Partners in generation of pathogenic feline leukemia viruses

  • Part A: Role Of Retrons, Retroelements, And Reverse Transcription In The Evolution Of Retroviruses And In Eukaryotic Genome Plasticity
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Abstract

Feline leukemia viruses (FeLVs), which are replication-competent oncoretroviruses of the domestic cat species, are contagiously transmitted in natural environments. They are capable of inducing either acute antiproliferative disease or, after prolonged latency, lymphoid malignancies in this animal population. Current knowledge of the recombinational events between infectious FeLV and noninfectious endogenously inherited FeLV-like elements is reviewed, and the potential role of the derived recombinant viruses in pathogenesis is discussed. Major observations made are as follows: (1) Up to three fourths of the exogenous FeLV envelope glycoprotein (SU), beginning from the N-terminal end, can be replaced by sequences from an endogenous FeLV to produce biologically active chimeric FeLVs. The in vitro replication efficiency or cell tropism of the recombinants appears to be influenced by the amount of SU sequences replaced by the endogenous partner, as well as by the locus of origin of the endogenous sequences. (2) Generation of FeLV recombinants in tissue culture cells corresponds closely to the findings from natural tumors. There is direct evidence, based on molecular genetic analysis, for the prevalence of recombinant proviruses in naturally arising FeLV-induced lymphomas. (3) Certain recombinants harboring an altered primary neutralizing epitope in the middle of SU corresponding to the endogenous FeLV sequence can evade immunity developed against common FeLV infection. In several other recombinants, the epitope sequence is found to be frequently mutated during the process of recombination. (4) FeLV variants with altered epitope, although they may not be efficient in replication in vivo, apparently are capable of causing focal infection in target organs. Evidence is also presented that when coinfected with an exogenous FeLV, the epitope sequence in the variants is reverted to the exogenous type, providing an explanation why this sequence is found to be conserved in all natural isolates of FeLV. (5) A prototype chimeric polyprotein containing most of the SU from the endogenous source is abnormally processed and becomes trapped in the endoplasmic reticulum. A functional consequence of such trap** is interference with specific FeLV infection. (6) Some recombinants, while only poorly replicating in the host, may have the ability to infect target erythroid progenitor cells for the induction of strong cytopathic effect. (7) Some other recombinants appear to potentiate lymphomagenesis by exogenous FeLV and others to acquire properties to infect CNS endothelial cells, an event that could potentially be related to FeLV-induced neuropathogenicity. (8) Of multiple recombinant viruses, a specific recombinant species was found to occur in each of the three cats examined in which lymphoma was experimentally induced, and it was exclusively seen in one of these cats. This recombinant FeLV may potentially be a candidate for strong leukemogenic function. In addition to commonly encountered virus envelope changes, another prominent viral factor involved in tumorigenesis is mutated FeLV transcription regulatory sequences, most frequently with enhancer duplication or triplication. Although only a limited amount of information is available in the area of insertional mutagenesis in FeLV neoplastic disease, activation of certain key nuclear transcription factor genes has been documented.

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References

  1. Jarrett W.F.H., Crawford E.M., Martin W.B., and Davie F., Nature202, 567–568, 1964.

    Google Scholar 

  2. Hardy W.D. Jr., Hess P.W., MacEwen E.G., McClelland A.J., Zuckerman E.E., Essex M., and Cotter S.M., Cancer Res36, 582–588, 1976.

    Google Scholar 

  3. Hardy W.D. Jr., J Am Animal Hosp Assoc17, 941–976, 1981.

    Google Scholar 

  4. Hardy W.D. Jr., Geering G., Old L.J., deHarven E., Brodey R.S., and McDonough S., Science166, 1019–1021, 1969.

    Google Scholar 

  5. Rojko J.L., Hoover E.A., Mathes L.E., Olsen R.G., and Schaller J.P., J Natl Cancer Inst63, 759–765, 1979.

    Google Scholar 

  6. McClelland A.J., Hardy W.D. Jr., and Zuckerman E.E. in Hardy W.D. Jr., Essex M.E., and McCelland A.J. (eds).Feline Leukemia Virus. Elsevier, New York, 1980, pp. 121–126.

    Google Scholar 

  7. Sarma P.S. and Log T., Virology44, 352–358, 1971.

    Google Scholar 

  8. Sarma P.S. and Log T., Virology54, 160–169, 1973.

    Google Scholar 

  9. Jarrett O., Hardy W.D. Jr., Golder M.C., and Hay D., Int J Cancer21, 334–337, 1978.

    Google Scholar 

  10. Jarrett O., Laird H.M., and Hay D., J Gen Virol20, 169–175, 1973.

    Google Scholar 

  11. Sarma P.S., Log T., Jain D., Hill P.R., and Huebner R.J., Virology64, 438–446, 1975.

    Google Scholar 

  12. Riedel N., Hoover E.A., Gasper P.W., Nicolson M.O., and Mullins J.I., J Virol60, 242–250, 1986.

    Google Scholar 

  13. Mathes L.E., Pandley R., Chakrabarti R., Hofman F.M., Hayes K.A., Stromberg P., and Roy-Burman P., Virology198, 185–195, 1994.

    Google Scholar 

  14. Mullins J.I., Chen C.S., and Hoover E.A., Nature319, 333–336, 1986.

    Google Scholar 

  15. Overbaugh J., Donahue P.R., Quackenbush S.L., Hoover E.A., and Mullins J.I., Science239, 906–910, 1988.

    Google Scholar 

  16. Mullins J.I., Hoover E.A., Quackenbush S.L., and Donahue P.R., J Acquir Immune Defic Syndr4, 547–557, 1991.

    Google Scholar 

  17. Poss M.L., Mullins J.I., and Hoover E.A., J Virol63, 189–195, 1989.

    Google Scholar 

  18. Reinhart T.A., Ghosh A.K., Hoover E.A., and Mullins J.I., J Virol67, 5153–5162, 1993.

    Google Scholar 

  19. Tzavaras T., Stewart M., McDougall A., Fulton R., Testa N., Onions D.E., and Neil J.C., J Gen Virol71, 343–354, 1990.

    Google Scholar 

  20. Sheets R.L., Pandey R., Jen W.-C., and Roy-Burman P., J Virol67, 3118–3125, 1993.

    Google Scholar 

  21. Tsatsanis C., Fulton R., Nishigaki K., Tsujimoto H., Levy L., Terry A., Spandidos D., Onions D., and Neil J.C., J Virol68, 8296–8303, 1994.

    Google Scholar 

  22. Baluda M.A. and Roy-Burman P., Nature New Biol244, 59–62, 1973.

    Google Scholar 

  23. Benveniste R.E. and Todaro G.J., Nature252, 456–459, 1974.

    Google Scholar 

  24. Sarma P.S., Tseng J., Lee Y.K., and Gilden R.V., Nature New Biol244, 56–59, 1973.

    Google Scholar 

  25. Spodick D.A., Soe L.H., and Roy-Burman P., Virus Res1, 543–555, 1984.

    Google Scholar 

  26. Reeves R.H., Nash W.G., and O'Brien S.J., J Virol56, 303–306, 1985.

    Google Scholar 

  27. Livingston D.M. and Todaro G.J., Virology53, 142–151, 1973.

    Google Scholar 

  28. Niman H.L., Stephenson J.R., Gardner M.B., and Roy-Burman P., Nature266, 357–360, 1977.

    Google Scholar 

  29. Niman H.L., Gardner M.B., Stephenson J.R., and Roy-Burman P., J Virol23, 578–586, 1977.

    Google Scholar 

  30. Niman H.L., Akhavi M., Gardner M.B., Stephenson J.R., and Roy-Burman P., J Natl Cancer Inst64, 587–594, 1980.

    Google Scholar 

  31. Busch M.P., Devr B.G., Soe L.H., Perbal B., and Roy-Burman P., Hematol Oncol1, 61–75, 1983.

    Google Scholar 

  32. Spodick D.A., Ghosh A.K., Parimoo S., and Roy-Burman P., Virus Res9, 263–283, 1988.

    Google Scholar 

  33. Ghosh A.K. and Roy-Burman P., J Virol63, 4234–4241, 1989.

    Google Scholar 

  34. Todaro A.J., Benveniste R.E., Sherwin S.A., and Sherr C.J., Cell13, 775–782, 1978.

    Google Scholar 

  35. Bonner T.I. and Todaro A.J., Virology94, 224–227, 1979.

    Google Scholar 

  36. Soe L.H., Devi B.G., Mullins J.I., and Roy-Burman P., J Virol46, 829–840, 1983.

    Google Scholar 

  37. Soe L.H., Shimizu R.W., Landolph J.R., and Roy-Burman P., J Virol56, 701–710, 1985.

    Google Scholar 

  38. Casey J.W., Roach A., Mullins J.I., Burck K.B., Nicolson M.O., Gardner M.B., and Davidson N., Proc Natl Acad Sci USA77, 7778–7782, 1981.

    Google Scholar 

  39. Berry B.T., Ghosh A.K., Kumar D.V., Spodick D.A., and Roy-Burman P., J Virol62, 3631–3641, 1988.

    Google Scholar 

  40. Kumar D.V., Berry B.T., and Roy-Burman P., J Virol63, 2379–2384, 1989.

    Google Scholar 

  41. Pandey R., Ghosh A.K., Kumar D.V., Bachman B.A., Shibata D., and Roy-Burman P., J Virol65, 6495–6508, 1991.

    Google Scholar 

  42. McDougall A.S., Terry A., Tzavaras T., Cheney C., Rojko J., and Neil J.C., J Virol68, 251–260, 1994.

    Google Scholar 

  43. Nunberg J.H., Williams M.E., and Innis M.A., J Virol49, 629–632, 1984.

    Google Scholar 

  44. Stewart M.A., Warnock M., Wheeler A., Wilke N., Mullins J.I., Onions D.E., and Neil J.C., J Virol58, 825–834, 1986.

    Google Scholar 

  45. Hu W.-S. and Temin H.M., Science250, 1227–1233, 1990.

    Google Scholar 

  46. Stuhlman H. and Berg P., J Virol66, 2378–2388, 1992.

    Google Scholar 

  47. Elder J.H. and Mullins J.I., J Virol46, 871–880, 1983.

    Google Scholar 

  48. Overbaugh J., Reidel N., Hoover E.A., and Mullins J.I., Nature332, 731–734, 1988.

    Google Scholar 

  49. Brojatsch J., Kristal B.S., Viglianti G.A., Khiroya A., Hoover E.A., and Mullins J.I., Proc Natl Acad Sci USA89, 8457–8461, 1992.

    Google Scholar 

  50. Rigby M.A., Rojko J.L., Stewart M.A., Kociba G.J., Cheney C.M., Rezanka L.J., Mathes L.E., Hartka J. R., Jarrett O., and Neil J.C., J Gen Virol73, 2839–2847, 1992.

    Google Scholar 

  51. Johann S.V., Gibbons J.J., and O'Hara B., J Virol66, 1635–1640, 1992.

    Google Scholar 

  52. Takeuchi Y., Vile R.G., Simpson G., O'Hara B., Collins M.K.L., and Weiss R.A., J Virol66, 1219–1222, 1992.

    Google Scholar 

  53. Tailor C.S., Takeuchi Y., O'Hara B., Johann S.V., Weiss R.A., and Collins M.K.L., J Virol67, 6737–6741, 1993.

    Google Scholar 

  54. Bechtel M.K., Stallcup M.R., Bedgood R.M., Corey J.L., Pandey R., and Roy-Burman P., Virology202, 329–338, 1994.

    Google Scholar 

  55. Hardy W.D., Jr. in Levy J.A. (ed).The Retroviridae, Vol. 2. Plenum Press, New York, 1993, pp. 109–180.

    Google Scholar 

  56. Sheets R.L., Pandey R., Klement V., Grant C.K., and Roy-Burman P., Virology190, 849–855, 1992.

    Google Scholar 

  57. Rojko J.L., Fulton R., Rezanka L.J., Williams L.L., Copelan E., Cheney C.M., Reichel G.S., Neil J.C., Mathes L.E., Fisher T.G., and Cloyd M.W., Lab Invest66, 418–426, 1992.

    Google Scholar 

  58. Rohn J.L., Linenberger M.L., Hoover E.A., and Overbaugh J., J Virol68, 2458–2467, 1994.

    Google Scholar 

  59. Pandey R., Bechtel M.K., Su Y., Ghosh A.K., Hayes K.A., Mathes L.E., and Roy-Burman P., Virology214, 584–592, 1995.

    Google Scholar 

  60. Rojko J.L., Hoover E.A., Krakowka S., Olsen R.G., and Mathes L.E., Cancer Res39, 3789–3791, 1979.

    Google Scholar 

  61. Hoover E.A., Rojko J.L., and Olsen R.G. in Olsen R.G. (ed).Feline Leukemia. CRC Press, Boca Raton, FL, 1980, pp. 69–76.

    Google Scholar 

  62. Quackenbush S.L., Donahue P.R., Dean G.A., Myles M.H., Ackley C.D., Cooper M.D., Mullins J.I., and Hoover E.A., J Virol64, 5465–5474, 1990.

    Google Scholar 

  63. Overbaugh J., Hoover E.A., Mullins J.I., Burns D.P.W., Rudensey L., Quackenbush S.L., Stallard V., and Donahue P.R., Virology188, 558–569, 1992.

    Google Scholar 

  64. Onions D., Jarrett O., Testa N., Frassoni F., and Toth S., Nature296, 156–158, 1982.

    Google Scholar 

  65. Riedel N., Hoover E.A., Dornsife R.E., and Mullins J.I., Proc Natl Acad Sci USA85, 2758–2762, 1988.

    Google Scholar 

  66. Abkowitz J.L., Blood77, 1442–1451, 1991.

    Google Scholar 

  67. Dean G.A., Groshek P.M., Mullins J.I., and Hoover E.A., J Virol66, 5561–5568, 1992.

    Google Scholar 

  68. Neil J.C., Fulton R., Rigby M., and Stewart M., Curr Top Microbiol Immunol171, 68–92, 1991.

    Google Scholar 

  69. Grant C.K., Ernisse B.J., Jarrett O., and Jones F.R., J Immunol131, 3042–3048, 1983.

    Google Scholar 

  70. Elder J.H., McGee J.S., Munson M., Houghten R.A., Kloetzer W., Bittle J.L., and Grant C.K., J Virol61, 8–15, 1987.

    Google Scholar 

  71. Nicolaisen-Strouss K., Kumar H.P.M., Fitting T., Grant C.K., and Elder J.H., J Virol61, 3410–3415, 1987.

    Google Scholar 

  72. Chakrabarti R., Hofman F.M., Pandey R., Mathes L.E., and Roy-Burman P., Am J Pathol144, 348–358, 1994.

    Google Scholar 

  73. Hardy W.D. Jr. in Gallo R.C. and F. Wong-Stall (eds).Retrovirus Biology and Human Disease. Marcel Dekker, New York, 1990, pp 33–86.

    Google Scholar 

  74. Copelan E.A., Reinhard J.J., Lewis M., Mathes L., Olsen R., and Sagone A., J Immunol131, 2017–2020, 1983.

    Google Scholar 

  75. Mathes L.E., Olsen R.G., Hebebrand L.C., Hoover E.A., and Schaller J.P., Nature274, 687–689, 1978.

    Google Scholar 

  76. Hebebrand L.C., Olsen R.G., Mathes L.E., and Nichols W.S., Cancer Res39, 443–447, 1979.

    Google Scholar 

  77. Lafrado L.J., Lewis M.G., Mathes L.E., and Olson R.G., J Gen Virol68, 507–513, 1987.

    Google Scholar 

  78. Fowler A.K., Twardzik D.R., Reed C.D., Weislow O.S., and Hellman A., Cancer Res37, 4529–4531, 1977.

    Google Scholar 

  79. Cianciolo G.J., Mathews T.J., Bolognesi D.P., and Snyderman R., J Immunol124, 2900–2905, 1980.

    Google Scholar 

  80. Israel E., Yu M., and Wainberg M.A., Immunology38, 41–50, 1959.

    Google Scholar 

  81. Wainberg M.A. and Israel E., J Immunol124, 64–70, 1980.

    Google Scholar 

  82. Weislow O.S., Fisher O.V., Twardzid D.R., Hellman A., and Fowler A.K., Proc Soc Exp Biol166, 522–527, 1981.

    Google Scholar 

  83. Athas G.B., Starkey C.R., and Levy L.S., Crit Rev Oncogen5, 169–199, 1994.

    Google Scholar 

  84. Elder J.H., Gautsch J.W., Jensen F.C., Lerner R.A., Hartley J.W., and Rowe W.P., Proc Natl Acad Sci USA74, 4676–4680, 1977.

    Google Scholar 

  85. Stoye J.P., Moroni C., and Coffin J.M., J Virol65, 1273–1285, 1991.

    Google Scholar 

  86. Li S, and Fan H., J Virol64, 3701–3711, 1990.

    Google Scholar 

  87. Tsichlis P. and Bear S., Proc Natl Acad Sci USA88, 4611–4615, 1991.

    Google Scholar 

  88. Li J.-P. and Baltimore D., J Virol65, 2408–2414, 1991.

    Google Scholar 

  89. Ruscetti S.K., Janesch N.J., Chakrabarti A., Sawyer S.T., and Hankins W.D., J Virol63, 1057–1062, 1990.

    Google Scholar 

  90. Li J.-P., D'Andrea A., Lodish H.L., and Baltimore D., Nature343, 762–764, 1990.

    Google Scholar 

  91. Peters G., Cell Growth Differ1, 503–510, 1990.

    Google Scholar 

  92. Russell P.H. and Jarrett O., Int J Cancer22, 351–357, 1978.

    Google Scholar 

  93. Fulton R, Plumb M., Shield L., and Neil L.C., J Virol64, 1675–1682, 1990.

    Google Scholar 

  94. Matsumoto Y., Momoi Y., Watari T., Goitsuka R., Tsujimoto H., and Hasegawa A., Virology189, 745–749, 1992.

    Google Scholar 

  95. Levesque K.S., Bonham L., and Levy L.S., J Virol64, 3455–3462, 1990.

    Google Scholar 

  96. Athas G.B., Lobelle-Rich P., and Levy L.S., J Virol69, 3324–3332, 1995.

    Google Scholar 

  97. Neil J.C., Hughes D., McFarlane R., Wilkie N.M., Onions D.E., Lees G., and Jarrett O., Nature308, 814–820, 1984.

    Google Scholar 

  98. Mullins J.I., Brody D.S., Binari R.C., Jr., and Cotter S.M., Nature308, 856–858, 1984.

    Google Scholar 

  99. Levy L.S., Gardner M.B., and Casey J.W., Nature308, 853–856, 1984.

    Google Scholar 

  100. Onions D.E., Lees G., Forrest D., and Neil J.C., Int J Cancer40, 40–45, 1987.

    Google Scholar 

  101. Levy L.S. and Lobelle-Rich P.A., J Virol66, 2885–2892, 1992.

    Google Scholar 

  102. Levy L.S., Lobelle-Rich P.A., and Overbaugh J., Oncongene8, 1833–1838, 1993.

    Google Scholar 

  103. Haupt Y., Alexander W.S., Barri A., Klinken S.P., and Abrams J.M., Cell65, 753–763, 1991.

    Google Scholar 

  104. van Lohuizen M., Verbeek S., Scheijen B., Wientjens E., van der Gulden H., and Berns A., Cell65, 737–752, 1991.

    Google Scholar 

  105. Levy L.S., Lobelle-Rich P.A., Overbaugh J., Abkovitz J.L., Fulton R., and Roy-Burman P., Virology196, 892–895, 1993.

    Google Scholar 

  106. Tsujimoto H., Fulton R., Nishigaki K., Matsumoto Y., Hasegawa A., Tsujimoto A., Cevario S., O'Brien S.J., Terry A., Onions D., and Neil J.C., Virology196, 845–848, 1993.

    Google Scholar 

  107. Levesque K.S., Mattei M.G., and Levy L.S., Oncogene6, 1377–1379, 1991.

    Google Scholar 

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Roy-Burman, P. Endogenousenv elements: Partners in generation of pathogenic feline leukemia viruses. Virus Genes 11, 147–161 (1995). https://doi.org/10.1007/BF01728655

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