Phylogenetic Classification of Feline Immunodeficiency Virus

Autores

  • Diezza Biondo Programa de Pós-Graduação em Biotecnologia, Universidade de Caxias do Sul (UCS), Caxias do Sul, RS, Brazil. Laboratório de Diagnóstico em Medicina Veterinária, Universidade de Caxias do Sul (UCS), Caxias do Sul, RS, Brazil. https://orcid.org/0000-0003-4852-1836
  • Diéssy Kipper UCS https://orcid.org/0000-0003-1615-3290
  • Jessica Gomes Maciel Programa de Pós-Graduação em Biotecnologia, Universidade de Caxias do Sul (UCS), Caxias do Sul, RS, Brazil. Laboratório de Diagnóstico em Medicina Veterinária, Universidade de Caxias do Sul (UCS), Caxias do Sul, RS, Brazil. https://orcid.org/0000-0002-0133-6839
  • Weslei de Oliveira Santana Programa de Pós-Graduação em Biotecnologia, Universidade de Caxias do Sul (UCS), Caxias do Sul, RS, Brazil. Laboratório de Diagnóstico em Medicina Veterinária, Universidade de Caxias do Sul (UCS), Caxias do Sul, RS, Brazil.
  • André Felipe Streck Programa de Pós-Graduação em Biotecnologia, Universidade de Caxias do Sul (UCS), Caxias do Sul, RS, Brazil. Laboratório de Diagnóstico em Medicina Veterinária, Universidade de Caxias do Sul (UCS), Caxias do Sul, RS, Brazil. https://orcid.org/0000-0002-4798-0777
  • Vagner Ricardo Lunge Programa de Pós-Graduação em Biotecnologia, Universidade de Caxias do Sul (UCS), Caxias do Sul, RS, Brazil. Laboratório de Diagnóstico em Medicina Veterinária, Universidade de Caxias do Sul (UCS), Caxias do Sul, RS, Brazil. https://orcid.org/0000-0003-4012-8650

DOI:

https://doi.org/10.22456/1679-9216.129530

Resumo

Background: The feline immunodeficiency virus (FIV) is responsible for a retroviral disease that affects domestic and wild cats worldwide, causing Feline Acquired Immunodeficiency Syndrome (FAIDS). FIV is a lentivirus from the family Retroviridae and its genome has 3 main structural genes: gag, pol and env. Phylogenetic studies have classified FIV into 7 subtypes according to the diversity among strains from the World, mainly in the env gene. Epidemiological analyses have demonstrated the high predominance of FIV-A and FIV-B. This in silico study aimed to perform a phylogenetic analysis to study FIV diversity worldwide.

Materials, Methods & Results: A total of 60 whole genome sequences (WGS) and 122 FIV env gene sequences were included in 2 datasets, which were aligned using MAFFT version 7. Recombination among genomes and/or env genes was analyzed with RDP5 software. Phylogenetic analyses with both datasets were performed, after removing the recombinant sequences, by the W-IQ-TREE and constructed and edited by the FigTree. A total of 12 recombination events involving 19 WGS were detected. In addition, 27 recombination events involving 49 sequences were observed in the env gene. A high rate of recombinants was observed inter-subtypes (A/B and B/D) and intra-subtypes (A/A). All recombinants were removed from the subsequent phylogenetic analyses. Phylogenies demonstrated 6 distinct main clades, 5 from domestic cats (A, B, C, E, U) and 1 from wild cat sequences (W) in the WGS, as well as in the specific env gene analyses. Most clustered with subtype B sequences. In the WGS analysis, clade B had a prevalence of 65.9% Brazilian sequences (27/41) and 2.4% Japanese sequences (1/41). In the env gene analyses, clade B showed a prevalence of 43.8% of Brazilian sequences (32/73) and 20.5% of USA sequences (15/73). The results of both analyses also confirm the FIV-wide geographical distribution around the world. In the phylogenetic analyses carried out with WGS, sequences from China (1/41; 2.4%), Colombia (1/41; 2.4%) and the USA (1/41; 2.4%) were identified in clade A; sequence from Canada in clade C (1/41; 2.4%); sequence from Botswana belonged to clade E (1/41; 2.4%); sequences from Brazil clustered into clade U (2/41; 5% - data not yet published); and sequences belonging to the clade W were from Canada (1/41; 2.4%) and the USA (5/41; 12.3%). Specific env gene phylogenetic analyses showed sequences from Colombia (1/73; 1.4%), France (2/73; 2.7%), the Netherlands (3/73; 4.1%), Switzerland (2/73; 2.7%), EUA (6/73; 8.3%), belonging to clade A; sequence from Canada belonging to clade C (1/73; 1.4%); sequences from Brazil belonging to clade U (2/73; 5% - data not yet published); and sequences belonging to clade W from the USA (6/73; 8.3%).

Discussion: The results presented here demonstrate that FIV has a rapid viral evolution due to recombination and mutation events, more specifically in the env gene, which is highly variable. Currently, this retrovirus is classified into 7 subtypes (A, B, C, D, E, F and U-NZenv) according to their high genomic diversity. It also highlighted the importance of in silico sequence and phylogeny studies to demonstrate evolutionary processes. This was the first study to address the WGS FIV diversity with a phylogenetic approach.

Keywords: FIV, in silico, phylogeny, subtypes, recombination.

 

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Referências

Bachmann M.H., Mathiason-Dubard C., Learn G.H., Rodrigo A.G., Sodora D.L., Mazzetti P., Hoover E.A. & Mullins J.I. 1997. Genetic diversity of feline immunodeficiency virus: dual infection, recombination, and distinct evolutionary rates among envelope sequence clades. Journal of Virology. 71(6): 4241-4253. DOI: 10.1128/JVI.71.6.4241-4253.1997. DOI: https://doi.org/10.1128/jvi.71.6.4241-4253.1997

Bęczkowski P.M., Hughes J., Biek R., Litster A., Willett B.J. & Hosie M.J. 2014. Feline immunodeficiency virus (FIV) env recombinants are common in natural infections. Retrovirology. 11: 80. DOI: 10.1186/s12977-014-0080-1. DOI: https://doi.org/10.1186/s12977-014-0080-1

Bruen T.C. & Poss M. 2007. Recombination in feline immunodeficiency virus genomes from naturally infected cougars. Virology. 364(2): 362-370. DOI: 10.1016/j.virol.2007.03.023. DOI: https://doi.org/10.1016/j.virol.2007.03.023

Cano-Ortiz L., Junqueira D.M., Comerlato J., Costa C.S., Zani A., Duda N.B., Tochetto C., Santos R.N., Costa F.V.A., Roehe P.M. & Franco A.C. 2017. Phylodynamics of the Brazilian feline immunodeficiency virus. Infection, Genetics and Evolution : Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases. 55: 166-171. DOI: 10.1016/j.meegid.2017.09.011. DOI: https://doi.org/10.1016/j.meegid.2017.09.011

Caxito F.A., Coelho F.M., Oliveira M.E. & Resende M. 2006. Feline immunodeficiency virus subtype B in domestic cats in Minas Gerais, Brazil. Veterinary Research Communications. 30(8): 953-956. DOI: 10.1007/s11259-006-3363-8. DOI: https://doi.org/10.1007/s11259-006-3363-8

Duarte A. & Tavares L. 2006. Phylogenetic analysis of Portuguese Feline Immunodeficiency Virus sequences reveals high genetic diversity. Veterinary Microbiology. 114(1-2): 25-33. DOI: 10.1016/j.vetmic.2005.11.056. DOI: https://doi.org/10.1016/j.vetmic.2005.11.056

Elder J.H., Lin Y.-C., Fink E. & Grant C.K. 2010. Feline immunodeficiency virus (FIV) as a model for study of lentivirus infections: parallels with HIV. Current HIV Research. 8(1): 73-80. DOI: 10.2174/157016210790416389. DOI: https://doi.org/10.2174/157016210790416389

Hartmann K. 2012. Clinical aspects of feline retroviruses: a review. Viruses. 4(11): 2684-2710. DOI: 10.3390/v4112684. DOI: https://doi.org/10.3390/v4112684

Hayward J.J. & Rodrigo A.G. 2008. Recombination in feline immunodeficiency virus from feral and companion domestic cats. Virology Journal. 5: 76. DOI: 10.1186/1743-422X-5-76. DOI: https://doi.org/10.1186/1743-422X-5-76

Hosie M.J., Addie D., Belák S., Boucraut-Baralon C., Egberink H., Frymus T., Gruffydd-Jones T., Hartmann K., Lloret A., Lutz H., Marsilio F., Pennisi M.G., Radford A.D., Thiry E., Truyen U. & Horzinek M.C. 2009. Feline immunodeficiency. ABCD guidelines on prevention and management. Journal of Feline Medicine and Surgery. 11(7): 575-584. DOI: 10.1016/j.jfms.2009.05.006. DOI: https://doi.org/10.1016/j.jfms.2009.05.006

Huguet M., Novo S.G. & Bratanich A. 2019. Detection of feline immunodeficiency virus subtypes A and B circulating in the city of Buenos Aires. Archives of Virology. 164(11): 2769-2774. DOI: 10.1007/s00705-019-04363-1. DOI: https://doi.org/10.1007/s00705-019-04363-1

Iwata D. & Holloway S.A. 2008. Molecular subtyping of feline immunodeficiency virus from cats in Melbourne. Australian Veterinary Journal. 86(10): 385-389. DOI: 10.1111/j.1751-0813.2008.00336.x. DOI: https://doi.org/10.1111/j.1751-0813.2008.00336.x

Kakinuma S., Motokawa K., Hohdatsu T., Yamamoto J.K., Koyama H. & Hashimoto H. 1995. Nucleotide sequence of feline immunodeficiency virus: classification of Japanese isolates into two subtypes which are distinct from non-Japanese subtypes. Journal of Virology. 69(6): 3639-3646. DOI: 10.1128/JVI.69.6.3639-3646.1995. DOI: https://doi.org/10.1128/jvi.69.6.3639-3646.1995

Katoh K. & Standley D.M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution. 30(4): 772-780. DOI: 10.1093/molbev/mst010. DOI: https://doi.org/10.1093/molbev/mst010

Kenyon J.C. & Lever A.M.L. 2011. The molecular biology of feline immunodeficiency virus (FIV). Viruses. 3(11): 2192-2213. DOI: 10.3390/v3112192. DOI: https://doi.org/10.3390/v3112192

Kiwelu I.E., Novitsky V., Margolin L., Baca J., Manongi R., Sam N., Shao J., McLane M.F., Kapiga S.H. & Essex M. 2013. Frequent intra-subtype recombination among HIV-1 circulating in Tanzania. PloS One. 8(8): e71131. DOI: 10.1371/journal.pone.0071131. DOI: https://doi.org/10.1371/journal.pone.0071131

Koç B.T. & Oğuzoğlu T.Ç. 2020. A phylogenetic study of Feline Immunodeficiency Virus (FIV) among domestic cats in Turkey. Comparative Immunology, Microbiology and Infectious Diseases. 73: 101544. DOI: 10.1016/j.cimid.2020.101544. DOI: https://doi.org/10.1016/j.cimid.2020.101544

Lau K.A. & Wong J.J.L. 2013. Current Trends of HIV Recombination Worldwide. Infectious Disease Reports. 5(Suppl 1): e4. DOI: 10.4081/idr.2013.s1.e4. DOI: https://doi.org/10.4081/idr.2013.s1.e4

Marçola T.G., Gomes C.P.C., Silva P.A., Fernandes G.R., Paludo G.R. & Pereira R.W. 2013. Identification of a novel subtype of feline immunodeficiency virus in a population of naturally infected felines in the Brazilian Federal District. Virus Genes. 46(3): 546-550. DOI: 10.1007/s11262-013-0877-3. DOI: https://doi.org/10.1007/s11262-013-0877-3

Martin D.P., Varsani A., Roumagnac P., Botha G., Maslamoney S., Schwab T., Kelz Z., Kumar V. & Murrell B. 2021. RDP5: a computer program for analyzing recombination in, and removing signals of recombination from, nucleotide sequence datasets. Virus Evolution. 7(1): veaa087. DOI: 10.1093/ve/veaa087. DOI: https://doi.org/10.1093/ve/veaa087

Martins A.N., Medeiros S.O., Simonetti J.P., Schatzmayr H.G., Tanuri A. & Brindeiro R.M. 2008. Phylogenetic and genetic analysis of feline immunodeficiency virus gag, pol, and env genes from domestic cats undergoing nucleoside reverse transcriptase inhibitor treatment or treatment-naïve cats in Rio de Janeiro, Brazil. Journal of Virology. 82(16): 7863-7874. DOI: 10.1128/JVI.00310-08. DOI: https://doi.org/10.1128/JVI.00310-08

Martins N.D.S., Rodrigues A.P.S., Luz L.A., Reis L.L., Oliveira R.M., Oliveira R.A., Abreu-Silva A.L., Reis J.K.P. & Melo F.A. 2018. Feline immudeficiency virus subtypes B and A in cats from São Luis, Maranhão, Brazil. Archives of Virology. 163(2): 549-554. DOI: 10.1007/s00705-017-3636-2. DOI: https://doi.org/10.1007/s00705-017-3636-2

Muz D., Can H., Karakavuk M., Döşkaya M., Özdemir H.G., Değirmenci Döşkaya A., Atalay Şahar E., Pektaş B., Karakuş M., Töz S., Özbel Y., Gürüz A.Y. & Muz M.N. 2021. The molecular and serological investigation of Feline immunodeficiency virus and Feline leukemia virus in stray cats of Western Turkey. Comparative Immunology, Microbiology and Infectious Diseases. 78: 101688. DOI: 10.1016/j.cimid.2021.101688. DOI: https://doi.org/10.1016/j.cimid.2021.101688

Pecon-Slattery J., Troyer J.L., Johnson W.E. & O’Brien S.J. 2008. Evolution of feline immunodeficiency virus in Felidae: implications for human health and wildlife ecology. Veterinary Immunology and Immunopathology. 123(1-2): 32-44. DOI: 10.1016/j.vetimm.2008.01.010. DOI: https://doi.org/10.1016/j.vetimm.2008.01.010

Pedersen N.C., Ho E.W., Brown M.L. & Yamamoto J.K. 1987. Isolation of a T-lymphotropic virus from domestic cats with an immunodeficiency-like syndrome. Science (New York, N.Y.). 235(4790): 790-793. DOI: 10.1126/science.3643650. DOI: https://doi.org/10.1126/science.3643650

Reggeti F. & Bienzle D. 2004. Feline immunodeficiency virus subtypes A, B and C and intersubtype recombinants in Ontario, Canada. The Journal of General Virology. 85(Pt 7): 1843-1852. DOI: 10.1099/vir.0.19743-0. DOI: https://doi.org/10.1099/vir.0.19743-0

Robertson D.L., Hahn B.H. & Sharp P.M. 1995. Recombination in AIDS viruses. Journal of Molecular Evolution. 40(3): 249-259. DOI: 10.1007/BF00163230. DOI: https://doi.org/10.1007/BF00163230

Roukaerts I.D.M., Theuns S., Taffin E.R.L., Daminet S. & Nauwynck H.J. 2015. Phylogenetic analysis of feline immunodeficiency virus strains from naturally infected cats in Belgium and The Netherlands. Virus Research. 196: 30-36. DOI: 10.1016/j.virusres.2014.10.023. DOI: https://doi.org/10.1016/j.virusres.2014.10.023

Sabino E.C., Shpaer E.G., Morgado M.G., Korber B.T., Diaz R.S., Bongertz V., Cavalcante S., Galvão-Castro B., Mullins J.I. & Mayer A. 1994. Identification of human immunodeficiency virus type 1 envelope genes recombinant between subtypes B and F in two epidemiologically linked individuals from Brazil. Journal of Virology. 68(10): 6340-6346. DOI: 10.1128/JVI.68.10.6340-6346.1994. DOI: https://doi.org/10.1128/jvi.68.10.6340-6346.1994

Samman A., McMonagle E.L., Logan N., Willett B.J., Biek R. & Hosie M.J. 2011. Phylogenetic characterisation of naturally occurring feline immunodeficiency virus in the United Kingdom. Veterinary Microbiology. 150(3–4): 239-247. DOI: 10.1016/j.vetmic.2011.01.027. DOI: https://doi.org/10.1016/j.vetmic.2011.01.027

Seibert S.A., Howell C.Y., Hughes M.K. & Hughes A.L. 1995. Natural selection on the gag, pol, and env genes of human immunodeficiency virus 1 (HIV-1). Molecular Biology and Evolution. 12(5): 803-813. DOI: 10.1093/oxfordjournals.molbev.a040257. DOI: https://doi.org/10.1093/oxfordjournals.molbev.a040257

Steinrigl A., Ertl R., Langbein I. & Klein D. 2010. Phylogenetic analysis suggests independent introduction of feline immunodeficiency virus clades A and B to Central Europe and identifies diverse variants of clade B. Veterinary Immunology and Immunopathology. 134(1-2): 82-89. DOI: 10.1016/j.vetimm.2009.10.013. DOI: https://doi.org/10.1016/j.vetimm.2009.10.013

Szilasi A., Dénes L., Krikó E., Heenemann K., Ertl R., Mándoki M., Vahlenkamp T.W. & Balka G. 2019. Prevalence of feline immunodeficiency virus and feline leukaemia virus in domestic cats in Hungary. JFMS Open Reports. 5(2): 2055116919892094. DOI: 10.1556/004.2020.00056. DOI: https://doi.org/10.1177/2055116919892094

Szilasi A., Dénes L., Krikó E., Murray C., Mándoki M. & Balka G. 2021. Prevalence of feline leukaemia virus and feline immunodeficiency virus in domestic cats in Ireland. Acta Veterinaria Hungarica. 68(4): 413-420. DOI: 10.1556/004.2020.00056. PMID: 33459612. DOI: https://doi.org/10.1556/004.2020.00056

Teixeira B.M., Logan N., Samman A., Miyashiro S.I., Brandão P.E., Willett B.J., Hosie M.J. & Hagiwara M.K. 2011. Isolation and partial characterization of Brazilian samples of feline immunodeficiency virus. Virus Research. 160(1–2): 59-65. DOI: 10.1016/j.virusres.2011.05.007. DOI: https://doi.org/10.1016/j.virusres.2011.05.007

Teixeira B.M., Taniwaki S.A., Menezes P.M.M., Rodrigues A.K.P.P., Mouta A.N., Arcebispo T.L.M., Braz G.F., da Cruz J.C.M., Brandão P.E., Heinemann M.B., Silva M.X. & Hosie M.J. 2019. Feline immunodeficiency virus in Northern Ceará, Brazil. JFMS Open Reports. 5(2): 2055116919859112. DOI: 10.1177/2055116919859112. DOI: https://doi.org/10.1177/2055116919859112

Trifinopoulos J., Nguyen L.-T., von Haeseler A. & Minh B.Q. 2016. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research. 44(W1): W232-5. DOI: 10.1093/nar/gkw256. DOI: https://doi.org/10.1093/nar/gkw256

Weaver E.A. 2010. A detailed phylogenetic analysis of FIV in the United States. PloS One. 5(8): e12004. DOI: 10.1371/journal.pone.0012004. DOI: https://doi.org/10.1371/journal.pone.0012004

Weaver E.A., Collisson E.W., Slater M. & Zhu G. 2004. Phylogenetic analyses of Texas isolates indicate an evolving subtype of the clade B feline immunodeficiency viruses. Journal of Virology. 78(4): 2158-2163. DOI: 10.1128/jvi.78.4.2158-2163.2004. DOI: https://doi.org/10.1128/JVI.78.4.2158-2163.2004

Westman M.E., Coggins S.J., van Dorsselaer M., Norris J.M., Squires R.A., Thompson M. & Malik R. 2022. Feline immunodeficiency virus (FIV) infection in domestic pet cats in Australia and New Zealand: Guidelines for diagnosis, prevention and management. Australian Veterinary Journal. 100(8): 345-359. DOI: 10.1111/avj.13166. DOI: https://doi.org/10.1111/avj.13166

Yang H., Peng Q., Lang Y., Du S., Cao S., Wu R., Zhao Q., Huang X., Wen Y., Lin J., Zhao S. & Yan Q. 2022. Phylogeny, Evolution, and Transmission Dynamics of Canine and Feline Coronaviruses: A Retro-Prospective Study. Frontiers in Microbiology. 13: 850516. DOI: 10.3389/fmicb.2022.850516. DOI: https://doi.org/10.3389/fmicb.2022.850516

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Publicado

2023-05-17

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Biondo, D., Kipper, D., Gomes Maciel, J., de Oliveira Santana, W., Felipe Streck, A., & Ricardo Lunge, V. (2023). Phylogenetic Classification of Feline Immunodeficiency Virus. Acta Scientiae Veterinariae, 51. https://doi.org/10.22456/1679-9216.129530

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