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FIV Diversity: Fivple Subtype Composition May Influence Disease

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FIV Diversity: Fivple Subtype Composition May Influence Disease Veterinary Immunology and Immunopathology 143 (2011) 338–346 Contents lists available at ScienceDirect Veterinary Immunology and Immunopathology j ournal homepage: www.elsevier.com/locate/vetimm Research paper FIV diversity: FIVPle subtype composition may influence disease outcome in African lions a,∗ a b b,1 Jennifer L. Troyer , Melody E. Roelke , Jillian M. Jespersen , Natalie Baggett , b c,2 c,3 c Valerie Buckley-Beason , Dan MacNulty , Meggan Craft , Craig Packer , b b Jill Pecon-Slattery , Stephen J. O’Brien a Laboratory of Genomic Diversity, SAIC-Frederick, National Cancer Institute, Frederick, MD, United States b Laboratory of Genomic Diversity, National Cancer Institute, Frederick, MD, United States c Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN, United States a r t i c l e i n f o a b s t r a c t Keywords: Feline immunodeficiency virus (FIV) infects domestic cats and at least 20 additional species FIVPle of non-domestic felids throughout the world. Strains specific to domestic cat (FIVFca) pro- Lions duce AIDS-like disease progression, sequelae and pathology providing an informative model CDV for HIV infection in humans. Less is known about the immunological and pathological influ- Babesia ence of FIV in other felid species although multiple distinct strains of FIV circulate in natural populations. As in HIV-1 and HIV-2, multiple diverse cross-species infections may have occurred. In the Serengeti National Park, Tanzania, three divergent subtypes of lion FIV (FIVPle) are endemic, whereby 100% of adult lions are infected with one or more of these strains. Herein, the relative distribution of these subtypes in the population are surveyed and, combined with observed differences in lion mortality due to secondary infections based on FIVPle subtypes, the data suggest that FIVPle subtypes may have different patterns of pathogenicity and transmissibility among wild lion populations. © 2011 Elsevier B.V. All rights reserved. 1. Introduction et al., 1998, 2010; Henriksen et al., 1995; Stump and VandeWoude, 2007). As with HIV and SIV models, there Feline immunodeficiency virus (FIV) is a lentivirus is considerable variation in transmission, course of infec- closely related to HIV and SIV. In domestic cats (Felis catus), tion, and outcome of FIV infections in domestic cats. Some FIV infection results in immune pathology, secondary infec- variation likely results from host genetic restriction factors tions, and death. The parallels between human and feline that influence the viral life cycle, similar to those described AIDS (FAIDS) have been explored for further understand- in humans (Lochelt et al., 2005; Munk et al., 2008, 2007; ing of HIV/AIDS transmission, infection, and pathology Troyer et al., 2008; VandeWoude et al., 2010). However, (Bendinelli et al., 1995; Burkhard and Dean, 2003; Elder differences in pathogenicity have also been demonstrated among genetically distinct subtypes of FIV that circulate in domestic cats (de Monte et al., 2002; Elder et al., 2010; ∗ Corresponding author. Tel.: +1 301 486 7478; fax: +1 301 846 6100. Pedersen et al., 2001; Weaver, 2010). E-mail address: [email protected] (J.L. Troyer). Most experimental viruses representing FIVFca subtypes 1 Current address: Department of Biology, Rider University, are cell-line adapted but nonetheless retain recognized Lawrenceville, NJ, United States. differences in pathogenicity. For example, FIV-CPG derived 2 Current address: Utah State University, Department of Wildland strains generally result in high initial viral loads and a faster Resources, Logan, UT, United States. 3 progression to disease, especially in young cats (de Rozieres Current address: College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK. et al., 2004a,b, 2008). In contrast, cats infected with FIV-A 0165-2427/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.vetimm.2011.06.013 J.L. Troyer et al. / Veterinary Immunology and Immunopathology 143 (2011) 338–346 339 strains often remain asymptomatic for longer periods of outcomes, in part because of the same geographic and envi- time, with lower initial viral loads, though viral growth ronmental co-factors mentioned above. kinetics are similar in adult cats once the acute stage of Several lines of evidence suggest that FIVPle subtypes infection has passed (de Rozieres et al., 2008; Pedersen may be substantially different from each other. Two FIVPle et al., 2001; Sparger et al., 1994). FIV subtype A strains are strains, FIVPle subtype E and FIVPle subtype A, circulate in often neurotrophic and neurotoxic, producing CNS symp- Botswana while three, FIVPle subtypes A, B, and C, occur in toms similar to those seen in HIV-1 infection (Gruol et al., the Serengeti National Park (Antunes et al., 2007; Brown 1998; Henriksen et al., 1995; Johnston et al., 2000; Meeker, et al., 1994; O’Brien et al., 2006; Troyer et al., 2004, 2005). 2007; Phillips et al., 1994, 1996; Power et al., 1998). Strains representing the predominant subtype in each of Species-specific FIV viruses infect other felids and are these populations, FIVPle-B from the Serengeti and FIVPle- distributed throughout the world, yet little is known about E from Botswana, have been fully sequenced revealing their immunological and pathological effects in wild popu- remarkable differences between these subtypes (Pecon- lations (Brown et al., 2010; Carpenter et al., 1996; Franklin Slattery et al., 2008a). While these two strains form a et al., 2008, 2007; Olmsted et al., 1992; Troyer et al., 2005). lion-specific clade when full length viruses are aligned, Long term surveillance of non-domestic felids infected the envelope (env) sequence by itself displays a different with FIV, as well as evidence from free-ranging popula- phylogenetic relationship that suggests an historic recom- tions of pumas (Puma concolor) and lions (Panthera leo), bination event between distantly related viruses, making suggest that these viruses are ancient, host-adapted, and FIVPle-E env seemingly more similar to domestic cat FIV have little to no negative impact on life-history param- than to FIVPle-B. In contrast, FIVPle-B env groups with eters such as longevity (Biek et al., 2006; Carpenter and other non-domestic cat env gene sequences (Carpenter and O’Brien, 1995; Packer et al., 1999). However, a few clin- O’Brien, 1995; Pecon-Slattery et al., 2008a; Smirnova et al., ical studies have revealed that individuals of these same 2005). The env gene is responsible for several aspects of species may demonstrate FIV-associated immune deple- lentiviral pathogenicity; changes in these sequences can tion and, in some cases, AIDS-like complications and death affect receptor binding, antibody affinity, and target cell (Brennan et al., 2006; Brown et al., 2010; Bull et al., 2002, specificity. Therefore, these differences have been hypoth- 2003; Roelke et al., 2006, 2009). Data on life history and esised to influence disease outcomes (Barlough et al., 1993; clinical parameters are rare, and seldom collected in the Burkhard and Dean, 2003; Elder et al., 2010; Patrick et al., same population. 2002; VandeWoude and Apetrei, 2006). At least six genetically distinct strains of lion FIV (FIVPle) The FIVPle subtypes circulating in Serengeti lions are circulate in wild populations of African lions (Panthera more divergent then the FIVPle found in other African lion leo) (Fig. 1; Antunes et al., 2008; O’Brien et al., 2006; populations. Specifically, FIVPle-C pol is as different from Pecon-Slattery et al., 2008b; Troyer et al., 2005). FIVPle sub- the other two Serengeti subtypes as from FIV strains that types demonstrate distinct phylogeographic distributions, infect other felid species (Troyer et al., 2005). Further, suggesting prolonged host association, perhaps predating within-subtype diversity is much higher for FIVPle-B than the Late-Pleistocene expansions of lions (Antunes et al., for the other two subtypes. Phylogenetic reconstruction of 2008). Probably as a result of the highly social nature of the three Serengeti FIVPle subtypes suggest different ances- lions, FIVPle-infected populations have high prevalence of tral evolutionary trajectories and/or selection pressures seropositive individuals, often approaching 100% in adults, (Troyer et al., 2004). For example, FIVPle-B is representa- while other populations remain completely uninfected tive of a widely distributed East African clade found across (Antunes et al., 2008; Brown et al., 1994; Troyer et al., 2005). Tanzania, Uganda, and Kenya. FIVPle-A appears to have This “all or nothing” distribution of FIV in lion population spread from Southern Africa as the most closely related lion makes appropriate comparisons of infected vs. uninfected viruses are found in South Africa and Botswana. Unique to lions a challenge. Differences in FIVPle status may be con- the Serengeti, FIVPle-C is distantly related to other FIVPle founded by important environmental parameters affecting viral subtypes (Antunes et al., 2008; O’Brien et al., 2006) lion health including other infectious agents, prey abun- and exhibits relatively low within strain diversity consis- dance, and water availability. tent with either recent introduction or stronger selective Epidemiological and life history vs. clinical and pressure from the host immune system. This pattern likely immunological studies on FIVPle-infected lions have been arose from three separate introductions of FIVPle to this collected in different populations
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