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Abstract

A retroviral etiology for malignant neoplasias in koalas has long been suspected. Evidence for retroviral involvement was bolstered in 2000 by the isolation of a koala retrovirus (KoRV), now termed KoRV-A. KoRV-A is an endogenous retrovirus—a retrovirus that infects germ cells—a feature that makes it a permanent resident of the koala genome. KoRV-A lacks the genetic diversity of an exogenous retrovirus, a quality associated with the ability of a retrovirus to cause neoplasias. In 2013, a second KoRV isolate, KoRV-B, was obtained from koalas with lymphomas in the Los Angeles Zoo. Unlike KoRV-A, which is present in the genomes of all koalas in the United States, KoRV-B is restricted in its distribution and is associated with host pathology (neoplastic disease). Here, our current understanding of the evolution of endogenous and exogenous KoRVs, and the relationship between them, is reviewed to build a perspective on the future impact of these viruses on koala sustainability.

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Koala Retroviruses: Evolution and Disease Dynamics
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2015-11-09
2024-04-24
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Literature Cited

  1. Griffiths DJ. 1.  2001. Endogenous retroviruses in the human genome sequence. Genome Biol. 2:reviews1017.1–1017.5 [Google Scholar]
  2. Bromham LD. 2.  2002. The human zoo: endogenous retroviruses in the human genome. Trends Ecol. Evol. 17:91–97 [Google Scholar]
  3. Ishida Y, Zhao K, Greenwood AD, Roca AL. 3.  2015. Proliferation of endogenous retroviruses in the early stages of a host germ line invasion. Mol. Biol. Evol. 32:109–20 [Google Scholar]
  4. Backhouse TC, Bolliger A. 4.  1961. Morbidity and mortality in the koala (Phascolarctos cinereus). Aust. J. Zool. 9:24–37 [Google Scholar]
  5. Heuschele WP, Hayes JR. 5.  1961. Acute leukemia in a New South Wales koala (Phascolarctos c. cinereus). Cancer Res. 21:1394–95 [Google Scholar]
  6. Canfield PJ, Sabine JM, Love DN. 6.  1988. Virus particles associated with leukaemia in a koala. Aust. Vet. J. 65:327–28 [Google Scholar]
  7. Martin J, Herniou E, Cook J, O'Neill RW, Tristem M. 7.  1999. Interclass transmission and phyletic host tracking in murine leukemia virus-related retroviruses. J. Virol. 73:2442–49 [Google Scholar]
  8. Hanger JJ, Bromham LD, McKee JJ, O'Brien TM, Robinson WF. 8.  2000. The nucleotide sequence of koala (Phascolarctos cinereus) retrovirus: a novel type C endogenous virus related to gibbon ape leukemia virus. J. Virol. 74:4264–72 [Google Scholar]
  9. Tarlinton RE, Meers J, Young PR. 9.  2006. Retroviral invasion of the koala genome. Nature 442:79–81 [Google Scholar]
  10. Tonjes RR, Niebert M. 10.  2003. Relative age of proviral porcine endogenous retrovirus sequences in Sus scrofa based on the molecular clock hypothesis. J. Virol. 77:12363–68 [Google Scholar]
  11. Oliveira NM, Satija H, Kouwenhoven IA, Eiden MV. 11.  2007. Changes in viral protein function that accompany retroviral endogenization. PNAS 104:17506–11 [Google Scholar]
  12. Demirov DG, Freed EO. 12.  2004. Retrovirus budding. Virus Res. 106:87–102 [Google Scholar]
  13. Marcucci KT, Martina Y, Harrison F, Wilson CA, Salomon DR. 13.  2008. Functional hierarchy of two L domains in porcine endogenous retrovirus (PERV) that influence release and infectivity. Virology 375:637–45 [Google Scholar]
  14. Bieniasz PD. 14.  2006. Late budding domains and host proteins in enveloped virus release. Virology 344:55–63 [Google Scholar]
  15. Tarlinton R, Meers J, Hanger J, Young P. 15.  2005. Real-time reverse transcriptase PCR for the endogenous koala retrovirus reveals an association between plasma viral load and neoplastic disease in koalas. J. Gen. Virol. 86:783–87 [Google Scholar]
  16. Shojima T, Hoshino S, Abe M, Yasuda J, Shogen H. 16.  et al. 2013. Construction and characterization of an infectious molecular clone of koala retrovirus. J. Virol. 87:5081–88 [Google Scholar]
  17. Xu W, Stadler CK, Gorman K, Jensen N, Kim D. 17.  et al. 2013. An exogenous retrovirus isolated from koalas with malignant neoplasias in a US zoo. PNAS 110:11547–52 [Google Scholar]
  18. Wilson CA, Eiden MV. 18.  1991. Viral and cellular factors governing hamster cell infection by murine and gibbon ape leukemia viruses. J. Virol. 65:5975–82 [Google Scholar]
  19. Ávila-Arcos MC, Ho SY, Ishida Y, Nikolaidis N, Tsangaras K. 19.  et al. 2013. One hundred twenty years of koala retrovirus evolution determined from museum skins. Mol. Biol. Evol. 30:299–304 [Google Scholar]
  20. Overbaugh J, Miller AD, Eiden MV. 20.  2001. Receptors and entry cofactors for retroviruses include single and multiple transmembrane-spanning proteins as well as newly described glycophosphatidylinositol-anchored and secreted proteins. Microbiol. Mol. Biol. Rev. 65:371–89 [Google Scholar]
  21. Oliveira NM, Farrell KB, Eiden MV. 21.  2006. In vitro characterization of a koala retrovirus. J. Virol. 80:3104–7 [Google Scholar]
  22. Fiebig U, Hartmann MG, Bannert N, Kurth R, Denner J. 22.  2006. Transspecies transmission of the endogenous koala retrovirus. J. Virol. 80:5651–54 [Google Scholar]
  23. Miyazawa T, Shojima T, Yoshikawa R, Ohata T. 23.  2011. Isolation of koala retroviruses from koalas in Japan. J. Vet. Med. Sci. 73:65–70 [Google Scholar]
  24. Xu W, Gorman K, Santiago JC, Kluska K, Eiden MV. 24.  2015. Genetic diversity of koala retroviral envelopes. Viruses 7:1258–70 [Google Scholar]
  25. Tarlinton R, Meers J, Young P. 25.  2008. Biology and evolution of the endogenous koala retrovirus. Cell. Mol. Life Sci. 65:3413–21 [Google Scholar]
  26. Denner J, Young PR. 26.  2013. Koala retroviruses: characterization and impact on the life of koalas. Retrovirology 10:108 [Google Scholar]
  27. Durand DB, Kamoun M, Norris CA, Holbrook NJ, Greengard JS. 27.  et al. 1986. Retroviral activation of interleukin 2 gene in a gibbon ape T cell lymphoma line. J. Exp. Med. 164:1723–34 [Google Scholar]
  28. Coffin J. 28.  1996. Retroviridae: the viruses and their replication. Field's Virology BN Fields, DM Knipe, PM Howley 1767–848 Philadelphia: Lippincott Williams & Wilkins, 3rd ed.. [Google Scholar]
  29. Prassolov V, Hein S, Ziegler M, Ivanov D, Münk C. 29.  et al. 2001. Mus cervicolor murine leukemia virus isolate M813 belongs to a unique receptor interference group. J. Virol. 75:4490–98 [Google Scholar]
  30. Shojima T, Yoshikawa R, Hoshino S, Shimode S, Nakagawa S. 30.  et al. 2013. Identification of a novel subgroup of koala retrovirus from koalas in Japanese zoos. J. Virol. 87:9943–48 [Google Scholar]
  31. Young P. 31.  2014. Koala retrovirus (KoRV) and its variants. Tech. Rep. Aust. Mus. 24:59–60 [Google Scholar]
  32. Shimode S, Nakagawa S, Yoshikawa R, Shojima T, Miyazawa T. 32.  2014. Heterogeneity of koala retrovirus isolates. FEBS Lett. 588:41–46 [Google Scholar]
  33. Andersen KB. 33.  1994. A domain of murine retrovirus surface protein gp70 mediates cell fusion, as shown in a novel SC-1 cell fusion system. J. Virol. 68:3175–82 [Google Scholar]
  34. Argaw T, Figueroa M, Salomon DR, Wilson CA. 34.  2008. Identification of residues outside of the receptor binding domain that influence the infectivity and tropism of porcine endogenous retrovirus. J. Virol. 82:7483–91 [Google Scholar]
  35. Tsangaras K, Siracusa MC, Nikolaidis N, Ishida Y, Cui P. 35.  et al. 2014. Hybridization capture reveals evolution and conservation across the entire koala retrovirus genome. PLOS ONE 9:e95633 [Google Scholar]
  36. Hobbs M, Pavasovic A, King AG, Prentis PJ, Eldridge MDB. 36.  et al. 2014. A transcriptome resource for the koala (Phascolarctos cinereus): insights into koala retrovirus transcription and sequence diversity. BMC Genomics 15:786 [Google Scholar]
  37. Simmons GS, Young PR, Hanger JJ, Jones K, Clarke D. 37.  et al. 2012. Prevalence of koala retrovirus in geographically diverse populations in Australia. Aust. Vet. J. 90:404–9 [Google Scholar]
  38. Masters P, Duka T, Berris S, Moss G. 38.  2004. Koalas on Kangaroo Island: from introduction to pest status in less than a century. Wildl. Res. 31:267–72 [Google Scholar]
  39. Day T, Mideo N, Alizon S. 39.  2008. Why is HIV not vector-borne?. Evol. Appl. 1:17–27 [Google Scholar]
  40. Iqbal MM. 40.  1999. Can we get AIDS from mosquito bites?. J. La. State Med. Soc. 151:429–33 [Google Scholar]
  41. Scherr CJ, Fedele L, Benveniste RE, Todaro G. 41.  1975. Interspecies antigenic determinants of the reverse transcriptases and p30 proteins of mammalian type C viruses. J. Virol. 15:1440–48 [Google Scholar]
  42. Callahan R, Scherr CJ, Todaro GJ. 42.  1977. A new class of murine retroviruses: immunological and biochemical comparison of novel isolates from Mus cervicolor and Mus caroli. Virology 80:401–16 [Google Scholar]
  43. Benveniste RE, Todaro G. 43.  1973. Homology between type-C viruses of various species as determined by molecular hybridization. PNAS 70:3316–20 [Google Scholar]
  44. Benveniste RE, Callahan R, Sherr CJ, Chapman V, Todaro GJ. 44.  1977. Two distinct endogenous type C viruses isolated from the Asian rodent Mus cervicolor: conservation of virogene sequences in related rodent species. J. Virol. 21:849–62 [Google Scholar]
  45. Hayward A, Grabherr M, Jern P. 45.  2013. Broad-scale phylogenomics provides insights into retrovirus-host evolution. PNAS 110:20146–51 [Google Scholar]
  46. Lieber M, Sherr C, Potter M, Todaro G. 46.  1975. Isolation of type-C viruses from the Asian feral mouse Mus musculus molossinus. Int. J. Cancer 15:211–20 [Google Scholar]
  47. Niwa O, Sugahara T. 47.  1981. 5-Azacytidine induction of mouse endogenous type C virus and suppression of DNA methylation. PNAS 78:6290–94 [Google Scholar]
  48. Schumann G, Moroni C. 48.  1977. Mitogen induction of murine C-type viruses. III. Effect of culture conditions, age, and genotype. Virology 79:81–87 [Google Scholar]
  49. Schlom J, Hand PH, Teramoto YA, Callahan R, Todaro G, Schidlovsky G. 49.  1978. Characterization of a new virus from Mus cervicolor immunologically related to the mouse mammary tumor virus. J. Natl. Cancer Inst. 61:1509–19 [Google Scholar]
  50. Lieber MM, Sherr CJ, Todaro GJ, Benveniste RE, Callahan R, Coon HG. 50.  1975. Isolation from the Asian mouse Mus caroli of an endogenous type C virus related to infectious primate type C viruses. PNAS 72:2315–19 [Google Scholar]
  51. Callahan R, Meade C, Todaro GJ. 51.  1979. Isolation of an endogenous type C virus related to the infectious primate type C viruses from the Asian rodent Vandeleuria oleracea. J. Virol. 30:124–31 [Google Scholar]
  52. Simmons G, Clarke D, McKee J, Young P, Meers J. 52.  2014. Discovery of a novel retrovirus sequence in an Australian native rodent (Melomys burtoni): a putative link between gibbon ape leukemia virus and koala retrovirus. PLOS ONE 9:e106954 [Google Scholar]
  53. Taylor AC, Graves JM, Murray ND, O'Brien SJ, Yuhki N, Sherwin B. 53.  1997. Conservation genetics of the koala (Phascolarctos cinereus): low mitochondrial DNA variation amongst southern Australian populations. Gen. Res. 69:25–33 [Google Scholar]
  54. Houlden BA, England PR, Taylor AC, Greville WD, Sherwin WB. 54.  1996. Low genetic variability of the koala Phascolarctos cinereus in south-eastern Australia following a severe population bottleneck. Mol. Ecol. 5:269–81 [Google Scholar]
  55. Tsangaras K, Ávila-Arcos MC, Ishida Y, Helgen KM, Roca AL, Greenwood AD. 55.  2012. Historically low mitochondrial DNA diversity in koalas (Phascolarctos cinereus). BMC Genet. 13:92 [Google Scholar]
  56. Timms P. 56.  2014. KoRV and chlamydia: Are they co-culprits?. Tech. Rep. Aust. Mus. 24:89–90 [Google Scholar]
  57. Bolin LL, Levy LS. 57.  2011. Viral determinants of FeLV infection and pathogenesis: lessons learned from analysis of a natural cohort. Viruses 3:1681–98 [Google Scholar]
  58. Fan H. 58.  2014. Leukemogenesis by murine leukemia viruses: lessons for koala retrovirus (KoRV). Tech. Rep. Aust. Mus. 24:83–88 [Google Scholar]
  59. Neil JC. 59.  2014. How does koala retrovirus (KoRV) induce disease at the genomic level?. Tech. Rep. Aust. Mus. 24:57–58 [Google Scholar]
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Author Maribeth V. Eiden, of the Laboratory of Cellular and Molecular Regulation at the National Institute of Mental Health, discusses her article.

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