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CD4 Receptor Diversity Represents an Ancient Protection Mechanism Against Primate Lentiviruses

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CD4 Receptor Diversity Represents an Ancient Protection Mechanism Against Primate Lentiviruses CD4 receptor diversity represents an ancient protection mechanism against primate lentiviruses Ronnie M. Russella,b,1, Frederic Bibollet-Ruchea,1, Weimin Liua, Scott Sherrill-Mixa,b, Yingying Lia, Jesse Connella, Dorothy E. Loya,b, Stephanie Trimbolia,b, Andrew G. Smitha, Alexa N. Avittoa, Marcos V. P. Gondima, Lindsey J. Plenderleithc,d, Katherine S. Wetzelb, Ronald G. Collmana,b, Ahidjo Ayoubae, Amandine Estebane, Martine Peeterse, William J. Kohlerf, Richard A. Millerf, Sandrine François-Souquiereg, William M. Switzerh, Vanessa M. Hirschi, Preston A. Marxj,k, Alex K. Piell, Fiona A. Stewartl,m, Alexander V. Georgievn,o, Volker Sommerl, Paco Bertolanip, John A. Hartq, Terese B. Hartq, George M. Shawa,b, Paul M. Sharpc,d, and Beatrice H. Hahna,b,2 aDepartment of Medicine, University of Pennsylvania, Philadelphia, PA 19104; bDepartment of Microbiology, University of Pennsylvania, Philadelphia, PA 19104; cInstitute of Evolutionary Biology, University of Edinburgh, EH9 3FL Edinburgh, United Kingdom; dCentre for Immunity, Infection, and Evolution, University of Edinburgh, EH9 3FL Edinburgh, United Kingdom; eRecherche Translationnelle Appliquée au VIH et aux Maladies Infectieuses, Institut de Recherche pour le Développement, University of Montpellier, INSERM, 34090 Montpellier, France; fDepartment of Pathology, University of Michigan, Ann Arbor, MI 48109; gHepatology and Gastroenterology Unit, University Hospital of Limoges, 87042 Limoges, France; hLaboratory Branch, Division of HIV/AIDS Prevention, Centers for Disease Control and Prevention, Atlanta, GA 30329; iLaboratory of Molecular Microbiology, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892; jDepartment of Tropical Medicine, School of Public Health and Tropical Medicine, Tulane University, New Orleans, LA 70118; kDivision of Microbiology, Tulane National Primate Research Center, Covington, LA 70433; lDepartment of Anthropology, University College London, WC1H 0BW London, United Kingdom; mSchool of Biological and Environmental Sciences, Liverpool John Moores University, L3 3AF Liverpool, United Kingdom; nDepartment of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138; oSchool of Biological Sciences, Bangor University, LL57 2UW Bangor, United Kingdom; pLeverhulme Centre for Human Evolutionary Studies, University of Cambridge, CB2 1QH Cambridge, United Kingdom; and qLukuru Wildlife Research Foundation, Tshuapa-Lomami-Lualaba Project, BP 2012, Kinshasa, Democratic Republic of the Congo Contributed by Beatrice H. Hahn, February 9, 2021 (sent for review December 22, 2020; reviewed by Michael Emerman, David D. Ho, and Leonidas Stamatatos) Infection with human and simian immunodeficiency viruses (HIV/ (2–5). This has enabled the identification of instances when SIVs SIV) requires binding of the viral envelope glycoprotein (Env) to have crossed species barriers, including from apes and monkeys the host protein CD4 on the surface of immune cells. Although to humans (6). Phylogenetic analyses have shown that both MICROBIOLOGY invariant in humans, the Env binding domain of the chimpanzee pandemic and nonpandemic forms of HIV type 1 (HIV-1) CD4 is highly polymorphic, with nine coding variants circulating in resulted from the cross-species transmission of SIVs infecting wild populations. Here, we show that within-species CD4 diversity central chimpanzees (P. troglodytes troglodytes) and western is not unique to chimpanzees but found in many African primate species. Characterizing the outermost (D1) domain of the CD4 pro- lowland gorillas (G. gorilla gorilla), while the various groups of tein in over 500 monkeys and apes, we found polymorphic resi- HIV type 2 (HIV-2) emerged following the transfer of SIVsmm dues in 24 of 29 primate species, with as many as 11 different coding variants identified within a single species. D1 domain Significance amino acid replacements affected SIV Env-mediated cell entry in a single-round infection assay, restricting infection in a strain- and The CD4 protein of primates has undergone rapid diversifica- allele-specific fashion. Several identical CD4 polymorphisms, in- tion, but the reasons for this remain unknown. Here we show cluding the addition of N-linked glycosylation sites, were found that within-species diversity of the HIV/simian immunodefi- in primate species from different genera, providing striking exam- ciency virus (SIV) envelope (Env) binding (D1) domain is com- ples of parallel evolution. Moreover, seven different guenons (Cer- mon among African primate species, and that these copithecus spp.) shared multiple distinct D1 domain variants, polymorphisms can inhibit SIV Env-mediated cell entry. Amino pointing to long-term trans-specific polymorphism. These data in- acid replacements in the D1 domain changed putative Env dicate that the HIV/SIV Env binding region of the primate CD4 contact residues as well as potential N-linked glycosylation protein is highly variable, both within and between species, and sites in many species, with evidence for parallel evolution and suggest that this diversity has been maintained by balancing se- trans-specific polymorphism. These data suggest that the pri- lection for millions of years, at least in part to confer protection mate CD4 receptor is under long-term balancing selection and against primate lentiviruses. Although long-term SIV-infected spe- that this diversification has been the result of a coevolutionary cies have evolved specific mechanisms to avoid disease progres- arms race between primate lentiviruses and their hosts. sion, primate lentiviruses are intrinsically pathogenic and have left their mark on the host genome. Author contributions: R.M.R., F.B.-R., G.M.S., P.M.S., and B.H.H. designed research; R.M.R., F.B.-R., W.L., Y.L., A.G.S., A.N.A., M.V.P.G., K.S.W., R.G.C., A.A., A.E., and M.P. performed research; K.S.W., R.G.C., M.P., W.J.K., R.A.M., S.F.-S., W.M.S., V.M.H., P.A.M., A.K.P., F.A.S., CD4 | primate lentiviruses | parallel evolution | trans-specific A.V.G., V.S., P.B., J.A.H., and T.B.H. contributed new reagents/analytic tools; R.M.R., polymorphism | balancing selection F.B.-R., S.S.-M., J.C., D.E.L., S.T., L.J.P., and P.M.S. analyzed data; and R.M.R., F.B.-R., P.M.S., and B.H.H. wrote the paper. imian immunodeficiency viruses (SIVs) comprise a large Reviewers: M.E., Fred Hutchinson Cancer Research Center; D.D.H., Columbia University; Sgroup of lentiviruses that infect over 45 African primate and L.S., Fred Hutchinson Cancer Research Center. species, including numerous guenons (Cercopithecus spp.), Afri- The authors declare no competing interest. can green monkeys (Chlorocebus spp.), mandrills and drills This open access article is distributed under Creative Commons Attribution-NonCommercial- NoDerivatives License 4.0 (CC BY-NC-ND). (Mandrillus spp.), mangabeys (Cercocebus spp.), colobus mon- See online for related content such as Commentaries. keys (Colobus spp., Piliocolobus spp.), as well as chimpanzees 1R.M.R. and F.B.-R. contributed equally to this work. (Pan troglodytes) and western gorillas (Gorilla gorilla) (1). Al- 2To whom correspondence may be addressed. Email: [email protected]. though the prevalence rates and geographic distribution of these This article contains supporting information online at https://www.pnas.org/lookup/suppl/ infections vary widely, most SIVs are host-specific (i.e., their doi:10.1073/pnas.2025914118/-/DCSupplemental. genomes form species-specific clusters in phylogenetic trees) Published March 26, 2021. PNAS 2021 Vol. 118 No. 13 e2025914118 https://doi.org/10.1073/pnas.2025914118 | 1of12 Downloaded by guest on September 28, 2021 strains naturally infecting sooty mangabeys (Cercocebus atys) replication (44–48). While the time required to evolve these (6–9). adaptations is unknown, such protective mechanisms are absent SIVs have also jumped between nonhuman primate species, from hosts that acquire new SIV infections. generating new SIV lineages. Cross-species transmission and Unlike restriction factors, which prevent or limit viral repli- recombination between ancestors of viruses today infecting cation, CD4 is a dependency factor (i.e., a host protein that is greater spot-nosed (Cercopithecus nictitans), mustached (Cerco- required for successful infection). Since there are many examples pithecus cephus) and mona (Cercopithecus mona) monkeys of host receptors coevolving with pathogens (49–51), it has been (SIVgsn/SIVmus/SIVmon), and SIVrcm infecting red-capped assumed that pressures exerted by pathogenic SIVs are respon- mangabeys (Cercocebus torquatus) gave rise to SIVcpz in chim- sible for the rapid diversification of primate CD4 (52–54). panzees (10), and onward transmission of this virus to western However, direct evidence for this hypothesis has been lacking. lowland gorillas generated SIVgor (11). Additional cross-species Examining the functional consequences of CD4 diversity in transmissions and recombination events have generated mosaic chimpanzees, we recently found that naturally occurring amino SIV lineages in green monkeys (Chlorocebus sabaeus) and acid replacements in the D1 domain were able to inhibit SIVcpz mandrills (Mandrillus sphinx) (12, 13). Finally, repeated intro- infection, both in vitro and in vivo (55). Protective mechanisms ductions of diverse SIVs into the same primate species have included charged residues at the CD4–Env interface and steric resulted in cocirculating lineages, such as SIVkcol1 and SIVk- hindrance between CD4- and Env-encoded glycans, which were
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