Skip to main content
SpringerLink
Log in

Endogenous env Elements: Partners in Generation of Pathogenic Feline Leukemia Viruses

  • Chapter
Molecular Evolution of Viruses — Past and Present

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 trapping 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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  1. Jarrett W.F.H., Crawford E.M., Martin W.B., and Davie F., Nature 202, 567–568, 1964.

    PubMed  CAS  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 Res 36, 582–588, 1976.

    PubMed  Google Scholar 

  3. Hardy W.D. Jr., J Am Animal Hosp Assoc 17, 941–976, 1981.

    Google Scholar 

  4. Hardy W.D. Jr., Geering G., Old L.J., deHarven E., Brodey R.S., and McDonough S., Science 166, 1019–1021, 1969.

    PubMed  Google Scholar 

  5. Rojko J.L., Hoover E.A., Mathes L.E., Olsen R.G., and Schaller J.P., J Natl Cancer Inst 63, 759–765, 1979.

    PubMed  CAS  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., Virology 44, 352–358, 1971.

    PubMed  CAS  Google Scholar 

  8. Sarma P.S. and Log T., Virology 54, 160–169, 1973.

    PubMed  CAS  Google Scholar 

  9. Jarrett O., Hardy W.D. Jr., Golder M.C., and Hay D., Int J Cancer 21, 334–337, 1978.

    PubMed  CAS  Google Scholar 

  10. Jarrett O., Laird H.M., and Hay D., J Gen Virol 20, 169–175, 1973.

    PubMed  CAS  Google Scholar 

  11. Sarma P.S., Log T., Jain D., Hill P.R., and Huebner R.J., Virology 64, 438–446, 1975.

    PubMed  CAS  Google Scholar 

  12. Riedel N., Hoover E.A., Gasper P.W., Nicolson M.O., and Mullins J.I., J Virol 60, 242–250, 1986.

    PubMed  CAS  Google Scholar 

  13. Mathes L.E., Pandley R., Chakrabarti R., Hofman F.M., Hayes K.A., Stromberg P., and Roy-Burman P., Virology 198, 185–195, 1994.

    PubMed  CAS  Google Scholar 

  14. Mullins J.I., Chen C.S., and Hoover E.A., Nature 319, 333–336, 1986.

    PubMed  CAS  Google Scholar 

  15. Overbaugh J., Donahue P.R., Quackenbush S.L., Hoover E.A., and Mullins J.I., Science 239, 906–910, 1988.

    PubMed  CAS  Google Scholar 

  16. Mullins J.I., Hoover E.A., Quackenbush S.L., and Donahue P.R., J Acquir Immune Defic Syndr 4, 547–557, 1991.

    PubMed  CAS  Google Scholar 

  17. Poss M.L., Mullins J.I., and Hoover E.A., J Virol 63, 189–195, 1989.

    PubMed  CAS  Google Scholar 

  18. Reinhart T.A., Ghosh A.K., Hoover E.A., and Mullins J.I., J Virol 67, 5153–5162, 1993.

    PubMed  CAS  Google Scholar 

  19. Tzavaras T., Stewart M., McDougall A., Fulton R., Testa N., Onions D.E., and Neil J.C., J Gen Virol 71, 343–354, 1990.

    PubMed  CAS  Google Scholar 

  20. Sheets R.L., Pandey R., Jen W.-C., and Roy-Burman P., J Virol 67, 3118–3125, 1993.

    PubMed  CAS  Google Scholar 

  21. Tsatsanis C., Fulton R., Nishigaki K., Tsujimoto H., Levy L., Terry A., Spandidos D., Onions D., and Neil J.C., J Virol 68, 8296–8303, 1994.

    PubMed  CAS  Google Scholar 

  22. Baluda M.A. and Roy-Burman P., Nature New Biol 244, 59–62, 1973.

    PubMed  CAS  Google Scholar 

  23. Benveniste R.E. and Todaro G.J., Nature 252, 456–459, 1974.

    PubMed  CAS  Google Scholar 

  24. Sarma P.S., Tseng J., Lee Y.K., and Gilden R.V., Nature New Biol 244, 56–59, 1973.

    PubMed  CAS  Google Scholar 

  25. Spodick D.A., Soe L.H., and Roy-Burman P., Virus Res 1, 543–555, 1984.

    PubMed  CAS  Google Scholar 

  26. Reeves R.H., Nash W.G., and O’Brien S.J., J Virol 56, 303–306, 1985.

    PubMed  CAS  Google Scholar 

  27. Livingston D.M. and Todaro G.J., Virology 53, 142–151, 1973.

    PubMed  CAS  Google Scholar 

  28. Niman H.L., Stephenson J.R., Gardner M.B., and Roy-Burman P., Nature 266, 357–360, 1977.

    PubMed  CAS  Google Scholar 

  29. Niman H.L., Gardner M.B., Stephenson J.R., and Roy-Burman P., J Virol 23, 578–586, 1977.

    PubMed  CAS  Google Scholar 

  30. Niman H.L., Akhavi M., Gardner M.B., Stephenson J.R., and Roy-Burman P., J Natl Cancer Inst 64, 587–594, 1980.

    PubMed  CAS  Google Scholar 

  31. Busch M.P., Devi B.G., Soe L.H., Perbal B., and Roy-Burman P., Hematol Oncol 1, 61–75, 1983.

    PubMed  CAS  Google Scholar 

  32. Spodick D.A., Ghosh A.K., Parimoo S., and Roy-Burman P., Virus Res 9, 263–283, 1988.

    PubMed  CAS  Google Scholar 

  33. Ghosh A.K. and Roy-Burman P., J Virol 63, 4234–4241, 1989.

    PubMed  CAS  Google Scholar 

  34. Todaro A.J., Benveniste R.E., Sherwin S.A., and Sherr C.J., Cell 13, 775–782, 1978.

    PubMed  CAS  Google Scholar 

  35. Bonner T.I. and Todaro A.J., Virology 94, 224–227, 1979.

    PubMed  CAS  Google Scholar 

  36. Soe L.H., Devi B.G., Mullins J.I., and Roy-Burman P., J Virol 46, 829–840, 1983.

    PubMed  CAS  Google Scholar 

  37. Soe L.H., Shimizu R.W., Landolph J.R., and Roy-Burman P., J Virol 56, 701–710, 1985.

    PubMed  CAS  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 USA 77, 7778–7782, 1981.

    Google Scholar 

  39. Berry B.T., Ghosh A.K., Kumar D.V., Spodick D.A., and Roy-Burman P., J Virol 62, 3631–3641, 1988.

    PubMed  CAS  Google Scholar 

  40. Kumar D.V., Berry B.T., and Roy-Burman P., J Virol 63, 2379–2384, 1989.

    PubMed  CAS  Google Scholar 

  41. Pandey R., Ghosh A.K., Kumar D.V., Bachman B.A., Shibata D., and Roy-Burman P., J Virol 65, 6495–6508, 1991.

    PubMed  CAS  Google Scholar 

  42. McDougall A.S., Terry A., Tzavaras T., Cheney C, Rojko J., and Neil J.C., J Virol 68, 251–260, 1994.

    Google Scholar 

  43. Nunberg J.H., Williams M.E., and Innis M.A., J Virol 49, 629–632, 1984.

    PubMed  CAS  Google Scholar 

  44. Stewart M.A., Warnock M., Wheeler A., Wilke N., Mullins J.I., Onions D.E., and Neil J.C., J Virol 58, 825–834, 1986.

    PubMed  CAS  Google Scholar 

  45. Hu W.-S. and Temin H.M., Science 250, 1227–1233, 1990.

    PubMed  CAS  Google Scholar 

  46. Stuhlman H. and Berg P., J Virol 66, 2378–2388, 1992.

    Google Scholar 

  47. Elder J.H. and Mullins J.I., J Virol 46, 871–880, 1983.

    PubMed  CAS  Google Scholar 

  48. Overbaugh J., Reidel N., Hoover E.A., and Mullins J.I., Nature 332, 731–734, 1988.

    PubMed  CAS  Google Scholar 

  49. Brojatsch J., Kristal B.S., Viglianti G.A., Khiroya A., Hoover E.A., and Mullins J.I., Proc Natl Acad Sci USA 59, 8457–8461, 1992.

    Google Scholar 

  50. Rigby M.A., Rojko J.L., Stewart M.A., Kociba G.J., Cheney CM., Rezanka L.J., Mathes L.E., Hartka J. R., Jarrett O., and Neil J.C., J Gen Virol 73, 2839–2847, 1992.

    PubMed  CAS  Google Scholar 

  51. Johann S.V., Gibbons J.J., and O’Hara B., J Virol 66, 1635–1640, 1992.

    PubMed  CAS  Google Scholar 

  52. Takeuchi Y., Vile R.G., Simpson G., O’Hara B., Collins M.K.L., and Weiss R.A., J Virol 66, 1219–1222, 1992.

    PubMed  CAS  Google Scholar 

  53. Tailor C.S., Takeuchi Y., O’Hara B., Johann S.V., Weiss R.A., and Collins M.K.L., J Virol 67, 6737–6741, 1993.

    PubMed  CAS  Google Scholar 

  54. Bechtel M.K., Stallcup M.R., Bedgood R.M., Corey J.L., Pandey R., and Roy-Burman P., Virology 202, 329–338, 1994.

    PubMed  CAS  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 CK., and Roy-Burman P., Virology 190, 849–855, 1992.

    PubMed  CAS  Google Scholar 

  57. Rojko J.L., Fulton R., Rezanka L.J., Williams L.L., Copelan E., Cheney CM., Reichel G.S., Neil J.C, Mathes L.E., Fisher T.G., and Cloyd M.W., Lab Invest 66, 418–426, 1992.

    PubMed  CAS  Google Scholar 

  58. Rohn J.L., Linenberger M.L., Hoover E.A., and Overbaugh J., J Virol 68, 2458–2467, 1994.

    PubMed  CAS  Google Scholar 

  59. Pandey R., Bechtel M.K., Su Y., Ghosh A.K., Hayes K.A., Mathes L.E., and Roy-Burman P., Virology 214, 584–592, 1995.

    PubMed  CAS  Google Scholar 

  60. Rojko J.L., Hoover E.A., Krakowka S., Olsen R.G., and Mathes L.E., Cancer Res 39, 3789–3791, 1979.

    PubMed  CAS  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 CD., Cooper M.D., Mullins J.I., and Hoover E.A., J Virol 64, 5465–5474, 1990.

    PubMed  CAS  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., Virology 188, 558–569, 1992.

    PubMed  CAS  Google Scholar 

  64. Onions D., Jarrett O., Testa N., Frassoni F., and Toth S., Nature 296, 156–158, 1982.

    PubMed  CAS  Google Scholar 

  65. Riedel N., Hoover E.A., Dornsife R.E., and Mullins J.I., Proc Natl Acad Sci USA 85, 2758–2762, 1988.

    PubMed  CAS  Google Scholar 

  66. Abkowitz J.L., Blood 77, 1442–1451, 1991.

    PubMed  CAS  Google Scholar 

  67. Dean G.A., Groshek P.M., Mullins J.I., and Hoover E.A., J Virol 66, 5561–5568, 1992.

    PubMed  CAS  Google Scholar 

  68. Neil J.C, Fulton R., Rigby M., and Stewart M., Curr Top Microbiol Immunol 171, 68–92, 1991.

    Google Scholar 

  69. Grant CK., Ernisse B.J., Jarrett O., and Jones F.R., J Immunol 131, 3042–3048, 1983.

    PubMed  CAS  Google Scholar 

  70. Elder J.H., McGee J.S., Munson M., Houghten R.A., Kloetzer W., Bittle J.L., and Grant CK., J Virol 61, 8–15, 1987.

    PubMed  Google Scholar 

  71. Nicolaisen-Strouss K., Kumar H.P.M., Fitting T., Grant CK., and Elder J.H., J Virol 61, 3410–3415, 1987.

    PubMed  CAS  Google Scholar 

  72. Chakrabarti R., Hofman F.M., Pandey R., Mathes L.E., and Roy-Burman P., Am J Pathol 144, 348–358, 1994.

    PubMed  CAS  Google Scholar 

  73. Hardy W.D. Jr. in Gallo R.C and F. Wong-Stall (eds). Retrovirus Biology and Human Disease. Marcel Dek-ker, 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 Immunol 131, 2017–2020, 1983.

    PubMed  CAS  Google Scholar 

  75. Mathes L.E., Olsen R.G., Hebebrand L.C, Hoover E.A., and Schaller J.P., Nature 274, 687–689, 1978.

    PubMed  CAS  Google Scholar 

  76. Hebebrand L.C, Olsen R.G., Mathes L.E., and Nichols W.S., Cancer Res 39, 443–447, 1979.

    PubMed  CAS  Google Scholar 

  77. Lafrado L.J., Lewis M.G., Mathes L.E., and Olson R.G., J Gen Virol 68, 507–513, 1987.

    PubMed  CAS  Google Scholar 

  78. Fowler A.K., Twardzik D.R., Reed CD., Weislow O.S., and Hellman A., Cancer Res 37, 4529–4531, 1977.

    PubMed  CAS  Google Scholar 

  79. Cianciolo G.J., Mathews T.J., Bolognesi D.P., and Snyderman R., J Immunol 124, 2900–2905, 1980.

    PubMed  CAS  Google Scholar 

  80. Israel E., Yu M., and Wainberg M.A., Immunology 38, 41–50, 1959.

    Google Scholar 

  81. Wainberg M.A. and Israel E., J Immunol 124, 64–70, 1980.

    PubMed  CAS  Google Scholar 

  82. Weislow O.S., Fisher O.V., Twardzid D.R., Hellman A., and Fowler A.K., Proc Soc Exp Biol 166, 522–527, 1981.

    PubMed  CAS  Google Scholar 

  83. Athas G.B., Starkey CR., and Levy L.S., Crit Rev Oncogen 5, 169–199, 1994.

    CAS  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 USA 74, 4676–4680, 1977.

    PubMed  CAS  Google Scholar 

  85. Stoye J.P., Moroni C, and Coffin J.M., J Virol 65, 1273–1285, 1991.

    PubMed  CAS  Google Scholar 

  86. Li S. and Fan H., J Virol 64, 3701–3711, 1990.

    PubMed  CAS  Google Scholar 

  87. Tsichlis P. and Bear S., Proc Natl Acad Sci USA 88, 4611–4615, 1991.

    PubMed  CAS  Google Scholar 

  88. Li J.-P. and Baltimore D., J Virol 65, 2408–2414, 1991.

    PubMed  CAS  Google Scholar 

  89. Ruscetti S.K., Janesch N.J., Chakrabarti A., Sawyer S.T., and Hankins W.D., J Virol 63, 1057–1062, 1990.

    Google Scholar 

  90. Li J.-P., D’Andrea A., Lodish H.L., and Baltimore D., Nature 343, 162–164, 1990.

    Google Scholar 

  91. Peters G., Cell Growth Differ 1, 503–510, 1990.

    PubMed  CAS  Google Scholar 

  92. Russell P.H. and Jarrett O., Int J Cancer 22, 351–357, 1978.

    PubMed  CAS  Google Scholar 

  93. Fulton R, Plumb M., Shield L., and Neil L.C., J Virol 64, 1675–1682, 1990.

    PubMed  CAS  Google Scholar 

  94. Matsumoto Y., Momoi Y., Watari T., Goitsuka R., Tsujimoto H., and Hasegawa A., Virology 189, 745–749, 1992.

    PubMed  CAS  Google Scholar 

  95. Levesque K.S., Bonham L., and Levy L.S., J Virol 64, 3455–3462, 1990.

    PubMed  CAS  Google Scholar 

  96. Athas G.B., Lobelle-Rich P., and Levy L.S., J Virol 69, 3324–3332, 1995.

    PubMed  CAS  Google Scholar 

  97. Neil J.C, Hughes D., McFarlane R., Wilkie N.M., Onions D.E., Lees G., and Jarrett O., Nature 308, 814–820, 1984.

    PubMed  CAS  Google Scholar 

  98. Mullins J.I., Brody D.S., Binari R.C., Jr., and Cotter S.M., Nature 308, 856–858, 1984.

    PubMed  CAS  Google Scholar 

  99. Levy L.S., Gardner M.B., and Casey J.W., Nature 308, 853–856, 1984.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  101. Levy L.S. and Lobelle-Rich P.A., J Virol 66, 2885–2892, 1992.

    PubMed  CAS  Google Scholar 

  102. Levy L.S., Lobelle-Rich P.A., and Overbaugh J., Oncogene 8, 1833–1838, 1993.

    PubMed  CAS  Google Scholar 

  103. Haupt Y., Alexander W.S., Barri A., Klinken S.P., and Abrams J.M., Cell 65, 753–763, 1991.

    PubMed  CAS  Google Scholar 

  104. van Lohuizen M., Verbeek S., Scheijen B., Wientjens E., van der Gulden H., and Berns A., Cell 65, 737–752, 1991.

    PubMed  Google Scholar 

  105. Levy L.S., Lobelle-Rich P.A., Overbaugh J., Abkovitz J.L., Fulton R., and Roy-Burman P., Virology 196, 892–895, 1993.

    PubMed  CAS  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., Virology 196, 845–848, 1993.

    PubMed  CAS  Google Scholar 

  107. Levesque K.S., Mattei M.G., and Levy L.S., Oncogene 6, 1377–1379, 1991.

    PubMed  CAS  Google Scholar 

Download references

Author information

Author notes

  1. Pradip Roy-Burman

    Present address: Department of Pathology, University of Southern California School of Medicine, Los Angeles, CA, 90033, USA

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, University of Southern California School of Medicine, Los Angeles, CA, USA

    Pradip Roy-Burman

Authors
  1. Pradip Roy-Burman
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Molecular Virology, The Hebrew University, Hadassah Medical School, Jerusalem, Israel

    Yechiel Becker

Rights and permissions

Reprints and permissions

Copyright information

© 1996 Kluwer Academic Publishers

About this chapter

Cite this chapter

Roy-Burman, P. (1996). Endogenous env Elements: Partners in Generation of Pathogenic Feline Leukemia Viruses. In: Becker, Y. (eds) Molecular Evolution of Viruses — Past and Present. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-1407-3_7

Download citation

  • DOI: https://doi.org/10.1007/978-1-4613-1407-3_7

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-8610-3

  • Online ISBN: 978-1-4613-1407-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation