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Molecular characterization of feline immunodeficiency virus genome obtained directly from organs of a naturally infected cat with marked neurological symptoms and encephalitis

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Summary

Feline immunodeficiency virus (FIV) was first isolated from cats with immunodeficiency syndrome. Recently, neurological abnormalities and brain lesions were shown in cats infected with FIV. To investigate the FIV genome associated with central nervous system (CNS) lesions, proviral DNA sequences from the V3–V6 region of the FIVenv gene were directly amplified from uncultured necropsy tissues of a 2-year-old naturally FIV-infected cat with marked neurological symptoms and encephalitis. By in situ hybridization, FIV RNA was detected mainly in the astrocytes. Fifteen clones isolated from cerebrum, bone marrow and lymph node samples showed only a small number of mutations or deletions in this region. A representative clone, JN-BR1, was distantly related to the previous Japanese strain (TM2) belonging to the subtype B. However, it was relatively close to the Petaluma strain which is known to infect feline brain-derived culture cells and induce brain lesions in inoculated cats. By phylogenetic analysis, the JN-BR1 strain was placed in subtype A that included Petaluma strain and several other American and European strains. The JN-BR1 strain derived from brain with encephalitis in this study and the Petaluma strain may share a common genetic structure that is related to their neuropathogenicity.

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References

  1. Ball JK, Holmes EC, Whitwell H, Desselberger U (1994) Genomic variation of human immunodeficiency virus type 1 (HIV-1): molecular analyses of HIV-1 in sequential blood samples and various organs obtained at autopsy. J Gen Virol 75: 867–879

    Google Scholar 

  2. Cheng MC, Shioda T, Levy JA (1991) Host range, replicative, and cytopathic properties of human immunodeficiency virus type 1 are determined by very few amino acid changes in tat and gp 120. J Virol 65: 6931–6941

    Google Scholar 

  3. Dow SW, Poss ML, Hoover EA (1990) Feline immunodeficiency virus: a neurotropic lentivirus. J Acquir Immune Defic Syndr 3: 658–668

    Google Scholar 

  4. Epstein LG, Gendelman HE (1993) Human immunodeficiency virus type 1 infection of the nervous system: pathogenetic mechanisms. Ann Neurol 33: 429–436

    Google Scholar 

  5. Felsenstein J (1991) PHYLIP Manual Version 3.5c. University Herbarium, University of California, Berkeley, CA, USA

    Google Scholar 

  6. Gurtler LG, Hauser PH, Eberle J, Von BA, Knapp S, Zekeng L, Tsague JM, Kaptue L (1994) A new subtype of human immunodeficiency virus type 1 (MVP-5180) from Cameroon. J Virol 68: 1581–1585

    Google Scholar 

  7. Hirota S, Ito A, Morii E, Wanaka A, Tohyama M, Kitamura Y, Nomura S (1992) Localization of mRNA for C-kit receptor and its ligand in the brain of adult rats: an analysis using in situ hybridization histochemistry. Mol Brain Res 15: 47–54

    Google Scholar 

  8. Hurtrel M, Ganiere JP, Guelfi JF, Chakrabarti L, Maire MA, Gray F, Montagnier L, Hurtrel B (1992) Comparison of early and late feline immunodeficiency virus encephalopathies. AIDS 6: 399–406

    Google Scholar 

  9. Kakinuma S, Motokawa K, Hohdatsu T, Yamamoto JK, 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. J Virol 69: 3639–3646

    Google Scholar 

  10. Kawaguchi Y, Maeda K, Tohya Y, Furuya T, Miyazawa T, Horimoto T, Norimine J, Kai C, Mikami T (1992) Replicative difference in early-passage feline brain cells among feline immunodeficiency virus isolates. Arch Virol 125: 347–354

    Google Scholar 

  11. Keys B, Karis J, Fadeel B, Valentin A, Norkrans G, Hagberg L, Chiodi F (1993) V3 sequences of paired HIV-1 isolates from blood and cerebrospinal fluid cluster according to host and show variation related to the clinical stage of disease. Virology 196: 475–483

    Google Scholar 

  12. Kohmoto M, Miyazawa T, Tomonaga K, Kawaguchi Y, Mori T, Tohya Y, Kai C, Mikami T (1994) Comparison of biological properties of feline immunodeficiency virus isolates using recombinant chimeric viruses. J Gen Virol 75: 1935–1942

    Google Scholar 

  13. Korber BT, Kustman KJ, Patterson BK, Furtado M, Mcevilly MM, Levy R, Wolinsky SM (1994) Genetic differences between blood-and brain-derived viral sequences from human immunodeficiency virus type 1-infected patients: evidence of conserved elements in the V3 region of the envelope protein of brain-derived sequences. J Virol 68: 7467–7481

    Google Scholar 

  14. Korber BT, Macinnes K, Smith RF, Myers G (1994) Mutational trends in V3 loop protein sequences observed in different genetic lineage of human immunodeficiency virus type 1. J Virol 68: 6730–6744

    Google Scholar 

  15. Koyanagi Y, Mitsuyasu RT, Merrill JE, Vinters HV, Chen IS (1987) Dual infection of the central nervous system by AIDS viruses with distinct cellular tropisms. Science 236: 819–822

    Google Scholar 

  16. Liu ZQ, Wood C, Levy JA, Cheng MC (1990) The viral envelope gene is involved in macrophage tropism of a human immunodeficiency virus type 1 strain isolated from brain tissue. J Virol 64: 6148–6153

    Google Scholar 

  17. Maki N, Miyazawa T, Fukasawa M, Hasegawa A, Hayami M, Miki K, Mikami T (1992) Moelcular characterization and heterogeneity of feline immunodeficiency virus isolates. Arch Virol 123: 29–45

    Google Scholar 

  18. Miyazawa T, Fukasawa M, Hesegawa A, Maki N, Ikuta K, Takashi E, Hayami M, Mikami T (1991) Molecular cloning of a novel isolate of feline immunodeficiency virus biologically and genetically different from the original U.S. isolate. J Virol 65: 1572–1577

    Google Scholar 

  19. Miyazawa T, Furuya T, Itagaki S, Tohya Y, Nakano K, Takahashi E, Mikami T (1989) Preliminary comparisons of the biological properties of two strain isolated in the United States. Arch Virol 108: 59–68

    Google Scholar 

  20. Momoi Y, Matsumoto Y, Watari T, Goitsuka R, Miyazawa T, Mikami T, Tsujimoto H, Hasegawa A (1993) Detection of feline immunodeficiency virus proviral DNA in feline peripheral blood mononuclear cells by the nested two-step polymerase chain reaction. Zbl Bakt 279: 274–282

    Google Scholar 

  21. Morikawa S, Lutz H, Aubert A, Bishop DH (1991) Identification of conserved and variable regions in the envelope glycoprotein sequences of two feline immunodeficiency viruses isolated in Zurich, Switzerland. Virus Res 21: 53–63

    Google Scholar 

  22. Olmsted RA, Barnes AK, Yamamoto JK, Hirsch VM, Purcell RH, Johnson PR (1989) Molecular cloning of feline immunodeficiency virus. Proc Natl Acad Sci USA 86: 2448–2452

    Google Scholar 

  23. Olmsted RA, Hirsch VM, Purcell RH, Johnson PR (1989) Nucleotide sequence analysis of feline immunodeficiency virus: genome organization and relationship to other lentiviruses. Proc Natl Acad Sci USA 86: 8088–8092

    Google Scholar 

  24. Pancino G, Fossati I, Chappey C, Castelot S, Hurtrel B, Moraillon A, Klatzmann D, Sonigo P (1993) Structure and variations of feline immunodeficiency virus envelope glycoproteins. Virology 192: 659–662

    Google Scholar 

  25. Pedersen NC, Ho EW, Brown ML, Yamamoto JK (1987) Isolation of a T-lymphotropic virus from domestic cats with an immunodeficiency-like syndrome. Science 235: 790–793

    Google Scholar 

  26. Philips TR, Talbott RL, Lamount C, Muir S, Lovelace K, Elder JH (1990) Comparison of two host range variants of feline immunodeficiency virus. J Virol 64: 4605–4613

    Google Scholar 

  27. Phillips TR, Prospero GO, Puaoi DL, Lerner DL, Fox HS, Olmasted RA, Bloom FE, Henriksen SJ, Elder JH (1994) Neurological abnormalities associated with feline immunodeficiency virus infection. J Gen Virol 75: 979–987

    Google Scholar 

  28. Podell M, Oglesbee M, Mathes L, Krakowka S, Olmstead R, Lafrado L (1993) AIDS-associated encephalopathy with experimental feline immunodeficiency virus infection. J Acquir Immune Defic Syndr 6: 758–771

    Google Scholar 

  29. Power C, McArthur JC, Johnson RT, Griffin DE, Glass JD, Perryman S, Chesebro B (1994) Demented and nondemented patients with AIDS differ in brain-derived human immunodeficiency virus type 1 envelope sequences. J Virol 68: 4643–4649

    Google Scholar 

  30. Price RW, Brew B, Sidtis J, Rosenblum M, Scheck AC, Cleary P (1988) The brain in AIDS: central nervous system HIV-1 infection and AIDS dementia complex. Science 239: 586–592

    Google Scholar 

  31. Rideout BA, Lowenstine LJ, Hutson CA, Moore PF, Pederson NC (1992) Characterization of morphologic changes and lymphocyte subset distribution in lymph nodes from cats with naturally acquired feline immunodeficiency virus infection. Vet Pathol 29: 391–399

    Google Scholar 

  32. Rigby MA, Holmes EC, Pistello M, Mackey A, Brown AJ, Neil JC (1993) Evolution of structural proteins of feline immunodeficiency virus: molecular epidemiology and evidency of selection for change. J Gen Virol 74: 425–436

    Google Scholar 

  33. Sharpless NE, O'Brien WA, Verdin E, Kufta CV, Chen IS, Dubois DM (1992) Human immunodeficiency virus type 1 tropism for brain microglial cells in determined by a region of the env glycoprotein that also controls macrophage tropism. J Virol 66: 2588–2593

    Google Scholar 

  34. Siebelink KH, Chu IH, Rimmelzwaan GF, Weijer K, Osterhaus AD, Bosch ML (1992) Isolation and partial characterization of infectious molecular clones of feline immunodeficiency virus obtained directly from bone marrow DNA of a naturally infected cat. J Virol 66: 1091–1097

    Google Scholar 

  35. Sodora DL, Shpaer EG, Kitchell BE, Dow SW, Hoover EA, Mullins JI (1994) Identification of three feline immunodeficiency virus (FIV) env gene subtypes and comparison of the FIV and human immunodeficiency virus type 1 evolutionary patterns. J Virol 68: 2230–2238

    Google Scholar 

  36. Takeuchi Y, Akutsu M, Murayama K, Shimizu N, Hoshino H (1991) Host range mutant of human immunodeficiency virus type 1: modification of cell tropism by a single point mutation at the neutralization epitope in the env gene. J Virol 65: 1710–1718

    Google Scholar 

  37. Talbott RL, Sparger EE, Lovelace KM, Fitch WM, Pedersen NC, Luciw PA, Elder JH (1989) Nucleotide sequence and genomic organization of feline immunodeficiency virus. Proc Natl Acad Sci USA 86: 5743–5747

    Google Scholar 

  38. Vanden HM, Decourt JL, De LR, Vanderborght B, van der Groen G, van Heuverswijn H, Saman E (1994) Genomic cloning and complete sequence analysis of a highly divergent African human immunodeficiency virus isolate. J Virol 68: 1586–1596

    Google Scholar 

  39. Verchoor EJ, Boven LE, Blaak H, van Vliet AL, Horzinek MC, de Ronde A (1995) A single mutation within the V3 envelope neutralization domain of feline immunodeficiency virus determines its tropism for CRFK cells. J Virol 69: 4752–4757

    Google Scholar 

  40. Yamamoto JK, Hansen H, Ho EW, Morishita TY, Okuda T, Sawa TR, Nakamura RM, Pedersen NC (1989) Epidemiologic and clinical aspects of feline immunodeficiency virus infection in cats from the continental United States and Canada and possible mode of transmission. J Am Vet Med Assoc 194: 213–220

    Google Scholar 

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Nishimura, Y., Nakamura, S., Goto, N. et al. Molecular characterization of feline immunodeficiency virus genome obtained directly from organs of a naturally infected cat with marked neurological symptoms and encephalitis. Archives of Virology 141, 1933–1948 (1996). https://doi.org/10.1007/BF01718205

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  • DOI: https://doi.org/10.1007/BF01718205

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