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Viruses 2012, 4(3), 383-396; doi:10.3390/v4030383
Published: 14 March 2012
Abstract: The rapid emergence of AIDS in humans during the period between 1980 and 2000 has led to extensive efforts to understand more fully similar etiologic agents of chronic and progressive acquired immunodeficiency disease in several mammalian species. Lentiviruses that have gene sequence homology with human immunodeficiency virus (HIV) have been found in different species (including sheep, goats, horses, cattle, cats, and several Old World monkey species). Lentiviruses, comprising a genus of the Retroviridae family, cause persistent infection that can lead to varying degrees of morbidity and mortality depending on the virus and the host species involved. Feline immunodeficiency virus (FIV) causes an immune system disease in domestic cats (Felis catus) involving depletion of the CD4+ population of T lymphocytes, increased susceptibility to opportunistic infections, and sometimes death. Viruses related to domestic cat FIV occur also in a variety of nondomestic felids. This is a brief overview of the current state of knowledge of this large and ancient group of viruses (FIVs) in South America.
Feline immunodeficiency virus (FIV) is a Lentivirus, closely related to HIV and SIV, which infects members of Felidae family. FIV is an important viral pathogen worldwide in the domestic cat (Felis catus), causes a slow progressive degeneration of immune functions that eventually leads to a disease. FIV is unique among the nonprimate lentiviruses because in its natural host species it induces a disease similar to AIDS in humans infected with human immunodeficiency virus type 1 (HIV-1), characterized by a progressive depletion of CD4+ T lymphocytes [5,28,35,48,77]. Species-specific strains, related to domestic cat FIV, have been isolated from a variety of nondomestic Felidae [11,43]. Like HIV, FIV can be transmitted via mucosal exposure, blood transfer, and vertically either prenatally or postnatally . For these reasons, FIV has been studied widely as both an important veterinary pathogen and an animal model for HIV/AIDS.
Although FIV was first recognized in 1993 in Brazil  and in 1994 in Argentina , there are few data describing the prevalence, ecology, clinical aspects, or genetic analyses of FIV in South America (Figure 1). The prevalence of FIV within the continent is summarized in Table 1. A better characterization of FIV strains circulating within South America will be required to augment our understanding of the importance of this lentivirus in felids. This paper provides an overview of the current state of knowledge of this large and ancient group of viruses (FIVs) in South America, grouped according to domestic and nondomestic felids. The data obtained allow a better understanding on FIV epidemiology and distribution. Efforts were made to gather and review all of the available information for each country.
|Table 1. Epidemiologic studies of Feline immunodeficiency virus (FIV) from South America.|
|Reference||Year||Country / Geographical distribution||Technique||Felid species||No tested||% Positive|
|(43)||1992||Brazil/Chile||Western Blot||Puma concolor||18||0|
|(65)||1994||Argentina||Western Blot||Felis catus||26||34.6|
|(52)||1997||Brazil—São Paulo||ELISA||Felis catus||401||11.7|
|(9)||2000||Brazil—Rio Grande do Sul||PCR||Felis catus||40||37.5|
|(61)||2002||Brazil—Rio de Janeiro||ELISA||Felis catus||126||16.6|
|(18)||2003||Brazil—São Paulo||ELISA||Leopardus pardalis, L. tigrinus, L. wiedii, Herpaiturus yaguarondi, Oncifelis geoffroyi||104||0|
|(12)||2003||Brazil—Minas Gerais||PCR||Felis catus||450||2.66|
|(64)||2007||Brazil—Minas Gerais||PCR||Felis catus||145||4.14|
|(19)||2006||Brazil—Roraima; Acre; Mato Grosso; Mato Grosso do Sul; São Paulo; Rio de Janeiro||ELISA/Western Blot||Puma concolor; Leopardus pardalis; Leopardus tigrinus||21||4.76/9.52|
|(21)||2007||Bolivia—Chaco||ELISA||Leopardus pardalis, Oncifelis geoffroyi, Herpaiturus yaguarondi||20||0|
|(31)||2008||Brazil—São Paulo||PCR||Felis catus||454||14.7|
|(20)||2011||Brazil—São Paulo||ELISA/Western Blot||Different species of neotropic and exotic felids||145||6.9 *|
*9 lions and 1 Geoffroy’s cat.
2. Felis Catus
FIV infection, in domestic cats, causes a variable immunodeficiency syndrome characterized by recurrent gingivitis-stomatitis, cachexia, wasting, neurology, and an increased incidence of tumor development [1,4,48,76]. In contrast, the ungulate lentiviruses cause diseases reminiscent of chronic inflammatory conditions while infection with the bovine lentivirus seems to be inapparent . The rate of progression of the disease can depend on the genotype of the infecting FIV and is also likely influenced by undefined genetic determinants of the particular host . FIV infection in domestic cats is associated with early robust humoral and cellular anti-viral immune responses, followed by a progressive immune suppression that results eventually in AIDS. The outcome of infection depends on the balance between the viral destruction of the immune system and the ability of the remaining immune system to eliminate the virus. Although the decrease in numbers of CD4+ cells is the hallmark of FIV infection, the virus has been shown to infect a variety of cell types in their respective hosts including CD4+ and CD8+ lymphocytes, B lymphocytes, cells of neuronal lineage and monocyte/macrophage lineage [15,17,29]. Joshi et al. (2005) have characterized feline CD4+ CD25+ T regulatory cells that support FIV replication. Recently, Reggeti, Ackerley and Bienzle (2008) have shown that feline dendritic cells express specific viral receptors and are infected productively by FIV . FIV shares a similar pattern of receptor usage to HIV-1; however, CD 134 rather than CD4 is the primary binding partner, and subsequent interaction with the secondary receptor CXCR4 permits cells entry [58,72,73]. Differences in pathogenicity have been demonstrated among genetically distinct subtypes of FIV that circulate in domestic cats [14,16,49,63,68,73]. On the basis of the analysis of envelope glycoprotein (Env), focusing on the third to fifth variable regions (V3-V5), FIV has been classified into five subtypes [30,46,60] a number that should be expected to increase as further studies reveal additional diversity. Recent studies identified distinct groups of FIV isolates from the United States and New Zealand [24,69] (Figure 2).
Data regarding FIV infection in domestic felids in South America are sparse and have not been well evaluated. Expanded surveys of South American isolates will be required to determine the FIV isolates in the continent since only few studies have been published. Although there are no doubts about the presence of FIV in South America, prevalence data obtained using different techniques cannot be compared amongst countries or studies (Table 1). Knowing the prevalence and variability of FIV is important for designing and testing vaccines under field conditions [27,77]. Also, identification of circulating subtypes is essential to develop strategies for molecular diagnosis, since the genetic diversity of this virus is high [44,54] which may lead to false negative diagnoses if inappropriate primers are used. In South America, only subtype B and E viruses have been found. It is important to remember that subtype B viruses are distributed worldwide and that the subtype E viruses have been more consistently identified only in Argentina (Figure 1).
Preliminary studies suggested that FIV infection is widespread in the domestic cat population of Brazil [9,12,40,52,61,64]. A published review indicated that subtype E was the only prevalent in Brazil . Nevertheless, all studies indentified B as the only subtype circulating in FIV positive animals in Brazil, [12,32,40,62]. Here an analysis was conducted with 473 bp of sequence encoding 157 amino acids comprising the V3-V4 region of the envelope glycoprotein from different subtypes, including those reported previously from South America (Figure 2). In this study we used this region of env in order to permit us to include more samples from South America. For this phylogenetic tree, the GenBank accession numbers, names, country and subtype for the FIV env sequences included were: M25381.1, Petaluma, United States, A; L00608.1, Dixon, United States, A; M59418.1, TM2, Japan, B; M36968.1, PPR, United States, A; X69496.1, UK8, England, A; X69494, UK2, Scotland, A; X57001, SwissZ2, Switzerland, A; AY621093, FC1, United States (Florida), B; U02392.1, CABCpady02C, Canada, C; D84498, LP20, Argentina, E; D84496, LP3, Argentina, E; D84500, LP24, Argentina, E; D37813.1, Sendai 1, Japan, A; D37816, Aomori 1, Japan, B; D37814.1, Sendai 2, Japan, B; D37812, Yokohama, Japan, B; D37815.1, Fukuoka, Japan, D; D37817.1, Aomori 2, Japan, B; D37811.1, Shizuoka, Japan, D; AY139094.1, TX125, United States (Texas), F; AY139096.1, TX200, United States (Texas), F; AY139097.1, TXMK, United States (Texas), F; EF153977.1, TKP88, New Zealand, U; EF153979.1, TKP22, New Zealand, U; EU375619, RJ35, Brazil, B; EU375617, RJ24, Brazil, B; EU375616, RJ23, Brazil, B; B; EU375597.1, strain RJ04, Brazil, B; EU375604.1, strain RJ11, Brazil, B; EU375606.1, strain RJ13, Brazil, B; EU375608.1, strain RJ15, Brazil, B; DQ248885.1, strain 1044MG, Brazil, B; DQ177159.2, strain 945MG, Brazil, B; DQ641681.1, strain 459MG, Brazil, B; DQ865447.1, strain 301MG, Brazil, B; DQ865449.1, strain 832MG, Brazil, B; DQ865454.1, strain 1160MG, Brazil, B.
It is important to state that all phylogenetic studies carried out in Brazil were performed in the same area, namely the south-east, and that Brazil is a huge country (Figure 1). More widespread surveys of Brazilian isolates are required to determine whether a single subtype of FIV predominates in Brazil. In Brazilian domestic cats, FIV infected cats have been observed over a prolonged period. During this time, few clinical signs were observed, although the virus was replicating and inducing changes in the immune system, leading to a progressive decline in immune function and the development later of overt clinical signs [51, 78, Hagiwara and Teixeira, unpublished data]. Previously, Brazilian studies established relationships between FIV infection and Toxoplasma gondii and Mycoplasma haemofelis [37,39]. Otherwise, no association with disease has been recorded in cases of Brazilian FIV infection. It has been suggested that clade B viruses may be more ancient and relatively host adapted and thus may be less virulent [2,50,63].
Preliminary seroepidemiological studies carried out on clinical cases suggested that FIV infection is widespread in the domestic cat population of Argentina . The genetic diversity of FIV isolates from Argentine domestic cats has been well characterized [47,75]. FIV isolates were isolated from peripheral blood mononuclear cells of four domestic cats. Phylogenetic analysis revealed that one isolate clustered with subtype B and the others formed subtype E , prototype sequence for this group (Figure 2).
In the north of the continent a single study was performed in 52 domestic cats on Isabela Island, Galapagos, Ecuador’s coast. It was demonstrated using serological methods that none of the tested animals was infected with FIV .
3. Nondomestic Felid Species
Viruses related to domestic cat FIV occur also in nondomestic felids, indeed FIV strains have been present in the nondomestic cat population for longer than domestic cats . Carpenter et al. (1996) comment that members of at least eighteen of the 37 species in the family Felidae carry an FIV-related virus, as has been shown by the presence in their sera of antibodies which react with FIV antigens. A further twelve species were reported in another study that employed a three-antigen Western blot screening (cat, puma and lion FIV antigens) and a multigene PCR amplification of FIV genes . In South America, 12 native species of Felidae’s family are found: Leopardus braccatus; Leopardus colocolo; Leopardus geoffroyi; Leopardus guingna; Leopardus jacobita; Leopardus pajeros; Leopardus pardalis; Leopardus tigrinus; Leoparuds wiedii; Puma concolor; Puma yagouaroundi; Panthera onca . Lentiviruses in eight of these species have been detected in South America [6,10,19,20,33,55,66].
Data regarding FIV infections in South American wild felids are sparse and studies have concentrated primarily on Brazil. The presence of antibodies against FIV in puma, detected by Western blotting, was found in Argentina (5 in 22, 23%), Bolivia (5 in 5, 100%), Brazil (2 in 13, 15%), Peru (1 in 5, 20%) and Venezuela (4 in 8, 50%) . Further studies have reported antibodies recognizing FIV and the puma lentivirus (PLV in Brazilian free-ranging puma) [6,19]. Troyer et al. (2005) concluded that most of the South American felids maintain a low level of FIV infection throughout their population. Within wild populations, the seroprevalence in South American felids varies from 5 to 28%. Unfortunately, the authors did not describe the regions of the continent where the samples originated. FIV pol genes from a Peruvian and a Brazilian zoo puma have been sequenced, the former being classified as subtype B and the latter as a distinct group, neither A nor B . Additionally, FIV provirus has been reported in Brazilian jaguars (Panthera onca), pumas, jaguarondis (Puma yagouaroundi), oncelots (Leopardus pardalis), margays (Leopardus wiedii), pampas cat (Leopardus colocolo), geoffroy’s cat (Leopardus geoffroyi) and little spotted cats (Leopardus tigrinus) [20,33,55]. The finding of these FIV infected species highlights the need for additional monitoring. Although the implications of these infections for wild felid conservation are difficult to assess, it is generally accepted that monitoring these infections is an important component for the management of endangered populations .
It is important to emphasize that FIV strains infecting 9 species of the Felidae have been at least partially sequenced and molecularly characterized [3,10,11,25,34,38,42,43,66]. Genetic analysis indicates that different felid species are infected by different strains of FIV [8,11]. Analysis of pol gene sequence of FIV from lions (Panthera leo), pumas (Puma concolor) and domestic cats indicated that each species has a specific strain of FIV and that the strains are related but distinct [7,43]. Also, strains from African lions (subtype B and E) differ in their abilities to replicate in feline cell lines , their sensitivity to receptor antagonists , and their requirement for ectopic expression of CD134, the primary cellular receptor, for productive infection .
It remains to be demonstrated that FIV-related viruses cause severe disease in species other than the domestic cat [6,38]. The apparent absence of clinical signs in pumas and lions may reflect a longer period of coevolution between virus and host in these species, whereas in the domestic cat, the virus and host have not yet had time to reach a similar state of nonpathogenic coexistence [6,7,57]. However, it is by no means certain that FIV does not cause disease in non-domestic cats. Not long ago, reports have shown immune depletion associated with FIV infection in lions and pumas [56,57] and another recent study reported evidence of immune suppression in the Pallas’ cat (Otocolobus manul), including histopatological changes . In addition, interspecies transmission (although is rare) may occur [22,67]. For example, a leopard cat (Felis bengalensis) was found to be infected with a domestic cat virus  and FIV infecting one puma was more characteristic of domestic cat FIV rather than puma FIV .
The prevalence of FIV infection is South America has not been well evaluated and regional variations remain largely unexplored in domestic and wild cats. Considering that FIV has been detected in domestic cats in South America and that wild and domestic cats have overlapping territories in the communities and buffer zone, there is the potential for domestic felids to transmit this virus to naive wild felids in zoologic as well as free-range settings. The isolation and molecular characterization of these pathogens, both in domestic and a variety of wild felines, would be helpful and may provide important baseline data to develop effective programs aimed at infectious disease prevention. We believe that the feline population should be continually monitored for FIV infection and that clinical correlates to FIV infection should be further investigated. As recently proposed , researchers could consider early surveillance programs across defined populations and detailed, cohort studies of naturally infected animals to provide further insights. Such studies would provide an opportunity to track retrospectively the pattern and consequences of an ongoing epizootic. There are technical reasons that hinder such studies, there is an urgent need for increased capacity in South American laboratories in order to conduct FIV screening and the apparent absence of FIV infection in some countries of the continent may merely reflect an absence of investigations. In addition, it is not easy to study FIV in wild cats as it is difficult to obtain samples from wild populations and only when these difficulties are overcome will it be possible to analyze and characterize FIV strains from the continent.
This work was supported from grants 07 04180-2 of the FAPESP (the São Paulo State research funding foundation), 480330-2007-7 of the CNPq (Brazil’s National Research Council) and Public Heath Service grant AI049765 to M.J.H from the National Institute of Allergy and Infectious Diseases.
We would like to thank Sandra Skrabanek for her time and valuable assistance on the map. Thanks are also due to all members of Projeto José de Melo for their delightful cooperation and support.
Conflict of Interest
The authors declare no conflict of interest.
- Ackley, C.D.; Yamamoto, J.K.; Levy, N.; Pedersen, N.C.; Cooper, M.D. Immunologic abnormalities in pathogen-free cats experimentally infected with feline immunodeficiency virus. J. Virol. 1990, 64, 5652–5655. [Google Scholar]
- Bachmann, M.H.; Mathiason-Dubard, C.; Learn, G.H.; Rodrigo, A.G.; Sodora, D.L.; Mazzetti, P.; Hoover, E.A.; Mullins, J.I. Genetic diversity of feline immunodeficiency virus: dual infection, recombination, and distinct evolutionary rates among envelope sequence clades. J. Virol. 1997, 71, 4241–4253. [Google Scholar]
- Barr, M.C.; Zou, L.; Long, F.; Hoose, W.A.; Avery, R.J. Proviral organization and sequence analysis of feline immunodeficiency virus isolated from a Pallas' cat. Virology 1997, 228, 84–91. [Google Scholar]
- Beatty, J.A.; Lawrence, C.E.; Callanan, J.J.; Grant, C.K.; Gault, E.A.; Neil, J.C.; Jarrett, O. Feline immunodeficiency virus (FIV)-associated lymphoma: a potential role for immune dysfunction in tumourigenesis. Vet. Immunol. Immunop. 1998, 65, 309–322. [Google Scholar]
- Bendinelli, M.; Pistello, M.; Lombardi, S.; Poli, A.; Garzelli, C.; Matteucci, D.; Ceccherini-Nelli, L.; Malvaldi, G.; Tozzini, F. Feline immunodeficiency virus: an interesting model for AIDS studies and an important cat pathogen. Clin. Microbiol. Rev. 1995, 8, 87–112. [Google Scholar]
- Brown, E.W.; Miththapala, S.; O'Brien, S.J. Prevalence of exposure to feline immunodeficiency virus in exotic felid species. J. Zoo Wildlife Med. 1993, 24, 357–364. [Google Scholar]
- Brown, E.W.; Yuhki, N.; Packer, C.; O'Brien, S.J. A lion lentivirus related to feline immunodeficiency virus: epidemiologic and phylogenetic aspects. J. Virol. 1994, I, 5953–5968. [Google Scholar]
- Brown, M.A.; Munkhtsog, B.; Troyer, J.L.; Ross, S.; Sellers, R.; Fine, A.E.; Swanson, W.F.; Roelke, M.E.; O'Brien, S.J. Feline immunodeficiency virus (FIV) in wild Pallas' cats. Vet. Immunol. Immunop. 2010, 134, 90–95. [Google Scholar]
- Caldas, A.P.F.; Leal, E.S.; Silva, E.F.A.; Ravazzolo, A. Detection of feline immunodeficiency provirus in domestic cats by polymerase chain reaction. Pesquisa Vet. Brasil. 2000, 20, 20–25. [Google Scholar]
- Carpenter, M.A.; Brown, E.W.; Culver, M.; Johnson, W.E.; Pecon-Slattery, J.; Brousset, D.; O'Brien, S.J. Genetic and phylogenetic divergence of feline immunodeficiency virus in the puma (Puma concolor). J. Virol. 1996, 70, 6682–6693. [Google Scholar]
- Carpenter, M.A.; O'Brien, S.J. Coadaptation and immunodeficiency virus: lessons from the Felidae. Curr. Opin. Gen. Dev. 1995, 5, 739–745. [Google Scholar]
- Caxito, F.A.; Coelho, F.M.; Oliveira, M.E.; Resende, M. Feline immunodeficiency virus subtype B in domestic cats in Minas Gerais, Brazil. Vet. Res. Comm. 2006, 30, 953–956. [Google Scholar]
- Daszak, P.; Cunningham, A.A.; Hyatt, A.D. Emerging infectious diseases of wildlife--threats to biodiversity and human health. Science 2000, 287, 443–449. [Google Scholar]
- de Monte, M.; Nonnenmacher, H.; Brignon, N.; Ullmann, M.; Martin, J.P. A multivariate statistical analysis to follow the course of disease after infection of cats with different strains of the feline immunodeficiency virus (FIV). J. Virol. Methods 2002, 103, 157–170. [Google Scholar]
- Dean, G.A.; Reubel, G.H.; Moore, P.F.; Pedersen, N.C. Proviral burden and infection kinetics of feline immunodeficiency virus in lymphocyte subsets of blood and lymph node. J. Virol. 1996, 70, 5165–5169. [Google Scholar]
- Elder, J.H.; Lin, Y.C.; Fink, E.; Grant, C.K. Feline immunodeficiency virus (FIV) as a model for study of lentivirus infections: parallels with HIV. Curr. HIV Res. 2010, 8, 73–80. [Google Scholar]
- English, R.V.; Johnson, C.M.; Gebhard, D.H.; Tompkins, M.B. In vivo lymphocyte tropism of feline immunodeficiency virus. J. Virol. 1993, 67, 5175–5186. [Google Scholar]
- Filoni, C.; Adania, C.H.; Durigon, E.L.; Catão-Dias, J.L. Serosurvey for feline leukemia virus and lentiviruses in captive small neotropic felids in São Paulo state, Brazil. J. Zoo Wildlife Med. 2003, 34, 65–68. [Google Scholar]
- Filoni, C.; Catão-Dias, J.L.; Bay, G.; Durigon, E.L.; Jorge, R.S.; Lutz, H.; Hofmann-Lehmann, R. First evidence of feline herpesvirus, calicivirus, parvovirus, and Ehrlichia exposure in Brazilian free-ranging felids. J. Zoo Wildlife Med. 2006, 42, 470–477. [Google Scholar]
- Filoni, C.; Catão-Dias, J.L.; Cattori, V.; Willi, B.; Meli, M.L.; Ramiro Corrêa, S.H.; Cristina Marques, M.; Harumi Adania, C.; Ramos Silva, J.C.; Vianna Marvulo, M.F.; Ferreira Neto, J.S.; Luiz Durigon, E.; de Carvalho, V.M.; Dall'acqua Coutinho, S.; Lutz, H.; Hofmann-Lehmann, R. Surveillance using serological and molecular methods for the detection of infectious agents in captive Brazilian neotropic and exotic felids. J. Vet. Diagn. Invest. 2012, 24, 166–173. [Google Scholar]
- Fiorello, C.V.; Noss, A.J.; Deem, S.L.; Maffei, L.; Dubovi, E.J. Serosurvey of small carnivores in the Bolivian Chaco. J. Wildlife Dis. 2007, 43, 551–557. [Google Scholar]
- Franklin, S.P.; Troyer, J.L.; Terwee, J.A.; Lyren, L.M.; Boyce, W.M.; Riley, S.P.; Roelke, M.E.; Crooks, K.R.; Vandewoude, S. Frequent transmission of immunodeficiency viruses among bobcats and pumas. J. Virol. 2007, 81, 10961–10969. [Google Scholar]
- Hagiwara, M.K.; Reche Junior, A.; Dagli, M.L.Z. Feline immunodeficiency virus infection in cats from Sao Paulo, Brazil. Braz. J. Vet. Res. Anim. Sci. 1993, 30, 217–220. [Google Scholar]
- Hayward, J.J.; Taylor, J.; Rodrigo, A.G. Phylogenetic analysis of feline immunodeficiency virus in feral and companion domestic cats of New Zealand. J. Virol. 2007, 81, 2999–3004. [Google Scholar]
- Hofmann-Lehmann, R.; Fehr, D.; Grob, M.; Elgizoli, M.; Packer, C.; Martenson, J.S.; O'Brien, S.J.; Lutz, H. Prevalence of antibodies to feline parvovirus, calicivirus, herpesvirus, coronavirus, and immunodeficiency virus and of feline leukemia virus antigen and the interrelationship of these viral infections in free-ranging lions in east Africa. Clin. Diagn. Lab. Immun. 1996, 3, 554–562. [Google Scholar]
- 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. Feline immunodeficiency. ABCD guidelines on prevention and management. 2009, 11, 575–584. [Google Scholar]
- Hosie, M.J.; Beatty, J.A. Vaccine protection against feline immunodeficiency virus: setting the challenge. Aust. Vet. J. 2007, 85, 5–12. [Google Scholar]
- Hosie, M.J.; Robertson, C.; Jarrett, O. Prevalence of feline leukaemia virus and antibodies to feline immunodeficiency virus in cats in the United Kingdom. Vet. Rec. 1989, 125, 293–297. [Google Scholar]
- Joshi, A.; Garg, H.; Tompkins, M.B.; Tompkins, W.A. Preferential feline immunodeficiency virus (FIV) infection of CD4+ CD25+ T-regulatory cells correlates both with surface expression of CXCR4 and activation of FIV long terminal repeat binding cellular transcriptional factors. J. Virol. 2005, 79, 4965–4976. [Google Scholar]
- Kakinuma, S.; Motokawa, K.; Hohdatsu, T.; Yamamoto, J.K.; Koyama, H.; Hashimoto, H. Nucleotide sequence of feline immunodeficiency virus: classification of Japanese isolates into two subtypes which are distinct from non-Japanese subtypes. J. Virol. 1995, 69, 3639–3646. [Google Scholar]
- Lara, V.M.; Taniwaki, S.A.; Araujo Junior, J.P. Occurrence of feline immunodeficiency virus infection in cats. Cienc. Rural 2008, 38, 2245–2249. [Google Scholar]
- Lara, V.M.; TaniwakiII, S.A.; Araújo, J.P., Jr. Phylogenetic characterization of feline immunodeficiency virus (FIV) isolates from the state of São Paulo. Pesquisa Vet. Brasil. 2007, 27, 467–470. [Google Scholar]
- Leal, E.S.; Ravazzolo, A.P. Detecção do vírus da imunodeficiência felina (FIV) em felídeos selvagens pertencentes à região neotropical, através da técnica de reação em cadeia da polimerase (PCR). Hora Vet. 1998, 101, 57–60. [Google Scholar]
- Leutenegger, C.M.; Hofmann-Lehmann, R.; Riols, C.; Liberek, M.; Worel, G.; Lups, P.; Fehr, D.; Hartmann, M.; Weilenmann, P.; Lutz, H. Viral infections in free-living populations of the European wildcat. J. Wildl. Dis. 1999, 35, 678–686. [Google Scholar]
- Levy, J.; Crawford, C.; Hartmann, K.; Hofmann-Lehmann, R.; Little, S.; Sundahl, E.; Thayer, V. 2008 American Association of Feline Practitioners' feline retrovirus management guidelines. J. Fel. Med.Surg. 2008b, 10, 300–316. [Google Scholar]
- Levy, J.K.; Crawford, P.C.; Lappin, M.R.; Dubovi, E.J.; Levy, M.G.; Alleman, R.; Tucker, S.J.; Clifford, E.L. Infectious diseases of dogs and cats on Isabela Island, Galapagos. J. Vet. Intern. Med. 2008b, 22, 60–65. [Google Scholar]
- Lucas, S.R.R.; Hagiwara, M.K.; Reche, A.R., Jr.; Germano, P.M.L. Ocorrencia de anticorpos antitoxoplasma em gatos infectados naturalmente pelo virus da imunodeficiencia dos felinos. Braz. J. Vet. Res. Anim. Sci. 1998, 35, 41–45. [Google Scholar]
- Lutz, H.; Isenbügel, E.; Lehmann, R.; Sabapara, R.H.; Wolfensberger, C. Retrovirus infections in non-domestic felids: serological studies and attempts to isolate a lentivirus. Vet. Immunol. Immunop. 1992, 35, 215–224. [Google Scholar]
- Macieira, D.B.; de Menezes, RdeC.; Damico, C.B.; Almosny, N.R.; McLane, H.L.; Daggy, J.K.; Messick, J.B. Prevalence and risk factors for hemoplasmas in domestic cats naturally infected with feline immunodeficiency virus and/or feline leukemia virus in Rio de Janeiro-Brazil. J. Fel. Med. Surg. 2008, 10, 120–129. [Google Scholar] [CrossRef]
- Martins, A.N.; Medeiros, S.O.; Simonetti, J.P.; Schatzmayr, H.G.; Tanuri, A.; Brindeiro, R.M. Phylogenetic and genetic analysis of feline immunodeficiency virus gag, pol, and env genes from domestic cats undergoing nucleoside reverse transcriptase inhibitor treatment or treatment-naive cats in Rio de Janeiro, Brazil. J. Virol. 2008, 82, 7863–7874. [Google Scholar]
- McEwan, W.A.; McMonagle, E.L.; Logan, N.; Serra, R.C.; Kat, P.; Vandewoude, S.; Hosie, M.J.; Willett, B.J. Genetically divergent strains of feline immunodeficiency virus from the domestic cat (Felis catus) and the African lion (Panthera leo) share usage of CD134 and CXCR4 as entry receptors. J. Virol. 2008, 82, 10953–10958. [Google Scholar]
- Nishimura, Y.; Goto, Y.; Yoneda, K.; Endo, Y.; Mizuno, T.; Hamachi, M.; Maruyama, H.; Kinoshita, H.; Koga, S.; Komori, M.; Fushuku, S.; Ushinohama, K.; Akuzawa, M.; Watari, T.; Hasegawa, A.; Tsujimoto, H. Interspecies transmission of feline immunodeficiency virus from the domestic cat to the Tsushima cat (Felis bengalensis euptilura) in the wild. J. Virol. 1999, 73, 7916–7921. [Google Scholar]
- Olmsted, R.A.; Langley, R.; Roelke, M.E.; Goeken, R.M.; Adger-Johnson, D.; Goff, J.P.; Albert, J.P.; Packer, C.; Laurenson, M.K.; Caro, T.M. Worldwide prevalence of lentivirus infection in wild feline species: epidemiologic and phylogenetic aspects. J. Virol. 1992, 66, 6008–6018. [Google Scholar]
- Pancino, G.; Camoin, L.; Sonigo, P. Structural analysis of the principal immunodominant domain of the feline immunodeficiency virus transmembrane glycoprotein. J. Virol. 1995, 69, 2110–2118. [Google Scholar]
- Pecon-Slattery, J.; Troyer, J.L.; Johnson, W.E.; O'Brien, S.J. Evolution of feline immunodeficiency virus in Felidae: implications for human health and wildlife ecology. Vet. Immunol. Immunop. 2008, 123, 32–44. [Google Scholar]
- Pecoraro, M.R.; Tomonaga, K.; Miyazawa, T.; Kawaguchi, Y.; Sugita, S.; Tohya, Y.; Kai, C.; Etcheverrigaray, M.E.; Mikami, T. Genetic diversity of Argentine isolates of feline immunodeficiency virus. J. Gen. Virol. 1996a, 77, 2031–2035. [Google Scholar]
- Pecoraro, M.R.; Tomonaga, K.; Miyazawa, T.; Kawaguchi, Y.; Sugita, S.; Tohya, Y.; Kai, C.; Etcheverrigaray, M.E.; Mikami, T. Genetic diversity of Argentine isolates of feline immunodeficiency virus. J. Gen. Virol. 1996b, 77, 2031–2035. [Google Scholar]
- Pedersen, N.C.; Ho, E.W.; Brown, M.L.; Yamamoto, J.K. Isolation of a T-lymphotropic virus from domestic cats with an immunodeficiency-like syndrome. Science 1987, 235, 790–793. [Google Scholar]
- Pedersen, N.C.; Leutenegger, C.M.; Woo, J.; Higgins, J. Virulence differences between two field isolates of feline immunodeficiency virus (FIV-APetaluma and FIV-CPGammar) in young adult specific pathogen free cats. Vet. Immunol. Immunop. 2001, 79, 53–67. [Google Scholar]
- Pistello, M.; Cammarota, G.; Nicoletti, E.; Matteucci, D.; Curcio, M.; Del Mauro, D.; Bendinelli, M. Analysis of the genetic diversity and phylogenetic relationship of Italian isolates of feline immunodeficiency virus indicates a high prevalence and heterogeneity of subtype B. J. Gen. Virol. 1997, 78, 2247–2257. [Google Scholar]
- Reche, A.; Daniel, A.G.; Lazaro Strauss, T.C.; Taborda, C.P.; Vieira Marques, S.A.; Haipek, K.; Oliveira, L.J.; Monteiro, J.M.; Kfoury, J.R. Cutaneous mycoflora and CD4:CD8 ratio of cats infected with feline immunodeficiency virus. J. Fel. Med. Surg. 2010, 12, 355–358. [Google Scholar]
- Reche, A., Jr.; Hagiwara, M.K.; Lucas, S.R.R. Clinical study of acquired immunodeficiency syndrome in domestic cats in São Paulo. Braz. J. Vet. Res. Anim. Sci. 1997, 34, 152–155. [Google Scholar]
- Reggeti, F.; Ackerley, C.; Bienzle, D. CD134 and CXCR4 expression corresponds to feline immunodeficiency virus infection of lymphocytes, macrophages and dendritic cells. J. Gen. Virol. 2008, 89, 277–287. [Google Scholar]
- Reggeti, F.; Bienzle, D. Feline immunodeficiency virus subtypes A, B and C and intersubtype recombinants in Ontario, Canada. J. Gen. Virol. 2004, 85, 1843–1852. [Google Scholar] [CrossRef]
- Rivetti, A.V., Jr.; Caxito, F.A.; Resende, M.; Lobato, Z.I.P. Avaliação sorológica para Toxoplasma gondii pela imunofluorescência indireta e detecção do vírus da imunodeficiência felina pela nested PCR em felinos selvagens. Arq. Bras. Med. Vet. Zoo. 2008, 60, 1281–1283. [Google Scholar] [CrossRef]
- Roelke, M.E.; Brown, M.A.; Troyer, J.L.; Winterbach, H.; Winterbach, C.; Hemson, G.; Smith, D.; Johnson, R.C.; Pecon-Slattery, J.; Roca, A.L.; Alexander, K.A.; Klein, L.; Martelli, P.; Krishnasamy, K.; O'Brien, S.J. Pathological manifestations of feline immunodeficiency virus (FIV) infection in wild African lions. Virology 2009, 390, 1–12. [Google Scholar]
- Roelke, M.E.; Pecon-Slattery, J.; Taylor, S.; Citino, S.; Brown, E.; Packer, C.; Vandewoude, S.; O'Brien, S.J. T-lymphocyte profiles in FIV-infected wild lions and pumas reveal CD4 depletion. J. Wildl. Dis. 2006, 42, 234–248. [Google Scholar]
- Shimojima, M.; Miyazawa, T.; Ikeda, Y.; McMonagle, E.L.; Haining, H.; Akashi, H.; Takeuchi, Y.; Hosie, M.J.; Willett, B.J. Use of CD134 as a primary receptor by the feline immunodeficiency virus. Science 2004, 303, 1192–1195. [Google Scholar]
- Smirnova, N.; Troyer, J.L.; Schissler, J.; Terwee, J.; Poss, M.; VandeWoude, S. Feline lentiviruses demonstrate differences in receptor repertoire and envelope structural elements. Virology 2005, 342, 60–76. [Google Scholar]
- Sodora, D.L.; Shpaer, E.G.; Kitchell, B.E.; Dow, S.W.; Hoover, E.A.; Mullins, J.I. 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. 1994, 68, 2230–2238. [Google Scholar]
- Souza, H.J.M.; Teixeira, C.H.R.; Graça, R.F.S. Epidemiological study of feline leukaemia virus and feline immunodeficiency virus infections in domestic cats in the city of Rio de Janeiro. Clín. Vet. 2002, 36, 14–21. [Google Scholar]
- Teixeira, B.M.; Logan, N.; Cruz, J.C.; Reis, J.K.; Brandão, P.E.; Richtzenhain, L.J.; Hagiwara, M.K.; Willett, B.J.; Hosie, M.J. Genetic diversity of Brazilian isolates of feline immunodeficiency virus. Arch. Virology 2010, 155, 379–384. [Google Scholar]
- Teixeira, B.M.; Logan, N.; Samman, A.; Miyashiro, S.I.; Brandão, P.E.; Willett, B.J.; Hosie, M.J.; Hagiwara, M.K. Isolation and partial characterization of Brazilian samples of feline immunodeficiency virus. Vir. Res. 2011, 160, 59–65. [Google Scholar]
- Teixeira, B.M.; Rajão, D.S.; Haddad, J.P.A.; Leite, R.C.; Reis, J.K.P. Occurrence of feline immunodeficiency virus and feline leukemia virus in Sheltered domestic cats of Belo Horizonte. Arq. Bras. Med. Vet. Zoo. 2007, 59, 939–942. [Google Scholar]
- Tohya, Y.; Castellano, M.C.; Norimine, J.; Etcheverrigaray, M.E. Anticuerpos contra el virus da la inmunodeficiencia felina: Primeira comprobacion en Argentina. Rev. Med. Vet. 1994, 75, 242–246. [Google Scholar]
- Troyer, J.L.; Pecon-Slattery, J.; Roelke, M.E.; Johnson, W.; VandeWoude, S.; Vazquez-Salat, N.; Brown, M.; Frank, L.; Woodroffe, R.; Winterbach, C.; Winterbach, H.; Hemson, G.; Bush, M.; Alexander, K.A.; Revilla, E.; O'Brien, S.J. Seroprevalence and genomic divergence of circulating strains of feline immunodeficiency virus among Felidae and Hyaenidae species. J. Virol. 2005, 79, 8282–8294. [Google Scholar]
- Troyer, J.L.; Vandewoude, S.; Pecon-Slattery, J.; McIntosh, C.; Franklin, S.; Antunes, A.; Johnson, W.; O'Brien, S.J. FIV cross-species transmission: an evolutionary prospective. Vet. Immun. Immunop. 2008, 123, 159–166. [Google Scholar]
- Weaver, E.A. A detailed phylogenetic analysis of FIV in the United States. PLoS One 2010, 5, e12004. [Google Scholar]
- Weaver, E.A.; Collisson, E.W.; Slater, M.; Zhu, G. Phylogenetic analyses of Texas isolates indicate an evolving subtype of the clade B feline immunodeficiency viruses. J. Virol. 2004, 78, 2158–2163. [Google Scholar]
- White, J.; Stickney, A.; Norris, J.M. Feline immunodeficiency virus: disease association versus causation in domestic and nondomestic felids. Vet. Clin. North Am. Small Anim. Pract. 2011, 41, 1197–1208. [Google Scholar]
- Willett, B.J.; Hosie, M.J. Chemokine receptors and co-stimulatory molecules: unravelling feline immunodeficiency virus infection. Vet. Immun. Immunop. 2008, 123, 56–64. [Google Scholar]
- Willett, B.J.; McMonagle, E.L.; Bonci, F.; Pistello, M.; Hosie, M.J. Mapping the domains of CD134 as a functional receptor for feline immunodeficiency virus. J. Virol. 2006a, 80, 7744–7747. [Google Scholar]
- Willett, B.J.; McMonagle, E.L.; Ridha, S.; Hosie, M.J. Differential utilization of CD134 as a functional receptor by diverse strains of feline immunodeficiency virus. J. Virol. 2006b, 80, 3386–3394. [Google Scholar]
- Wozencraft, W.C. Order Carnivora. In Mammal species of the world: a taxonomic and geographic reference, 3nd; Wilson, D.E., Reeder, D.M., Eds.; Johns Hopkins University Press: Baltimore, USA, 2005; Volume 1, pp. 532–628. [Google Scholar]
- Yamada, H.; Miyazawa, T.; Tomonaga, K.; Kawaguchi, Y.; Maeda, K.; Castellano, M.C.; Kai, C.; Tohya, Y.; Mikami, T. Phylogenetic analysis of the long terminal repeat of feline immunodeficiency viruses from Japan, Argentina and Australia. Arch. Virology 1995, 140, 41–52. [Google Scholar]
- Yamamoto, J.K.; Hansen, H.; Ho, E.W.; Morishita, T.Y.; Okuda, T.; Sawa, T.R.; Nakamura, R.M.; Pedersen, N.C. 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. 1989, 194, 213–220. [Google Scholar]
- Yamamoto, J.K.; Pu, R.; Sato, E.; Hohdatsu, T. Feline immunodeficiency virus pathogenesis and development of a dual-subtype feline-immunodeficiency-virus vaccine. AIDS 2007, 21, 547–563. [Google Scholar]
- Zanuto, M.S.; Froes, T.R.; Teixeira, A.L.; Hagiwara, M.K. Caracteristicas clinicas da fase aguda da infeccao experimental de felinos pelo virus da imunodeficiencia felina. Pesq. Vet. Brasil. 2011, 31, 255–260. [Google Scholar]
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