A conflict of interest: the evolutionary arms race between mammalian APOBEC3 and lentiviral Vif

Apolipoprotein B mRNA editing enzyme catalytic polypeptide-like 3 (APOBEC3) proteins are mammalian-specific cellular deaminases and have a robust ability to restrain lentivirus replication. To antagonize APOBEC3-mediated antiviral action, lentiviruses have acquired viral infectivity factor (Vif) as an accessory gene. Mammalian APOBEC3 proteins inhibit lentiviral replication by enzymatically inserting G-to-A hypermutations in the viral genome, whereas lentiviral Vif proteins degrade host APOBEC3 via the ubiquitin/proteasome-dependent pathway. Recent investigations provide evidence that lentiviral vif genes evolved to combat mammalian APOBEC3 proteins. In corollary, mammalian APOBEC3 genes are under Darwinian selective pressure to escape from antagonism by Vif. Based on these observations, it is widely accepted that lentiviral Vif and mammalian APOBEC3 have co-evolved and this concept is called an “evolutionary arms race.” This review provides a comprehensive summary of current knowledge with respect to the evolutionary dynamics occurring at this pivotal host-virus interface.

[1]  F. Gao,et al.  Human infection by genetically diverse SIVSM-related HIV-2 in West Africa , 1992, Nature.

[2]  J. Chermann,et al.  Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). , 1983, Science.

[3]  N. Krogan,et al.  Lineage-Specific Viral Hijacking of Non-canonical E3 Ubiquitin Ligase Cofactors in the Evolution of Vif Anti-APOBEC3 Activity. , 2015, Cell reports.

[4]  R. Mamoun,et al.  North American and French caprine arthritis-encephalitis viruses emerge from ovine maedi-visna viruses. , 1997, Virology.

[5]  D. M. Junqueira,et al.  Analysis of single-nucleotide polymorphisms in the APOBEC3H gene of domestic cats (Felis catus) and their association with the susceptibility to feline immunodeficiency virus and feline leukemia virus infections. , 2014, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[6]  K. Cichutek,et al.  Restriction of Equine Infectious Anemia Virus by Equine APOBEC3 Cytidine Deaminases , 2009, Journal of Virology.

[7]  M. Peeters,et al.  Cross-species transmission of simian retroviruses: how and why they could lead to the emergence of new diseases in the human population , 2012, AIDS.

[8]  M. Emerman,et al.  Antiretroelement activity of APOBEC3H was lost twice in recent human evolution. , 2008, Cell host & microbe.

[9]  S. O’Brien,et al.  Functions, structure, and read-through alternative splicing of feline APOBEC3 genes , 2008, Genome Biology.

[10]  Steven Wolinsky,et al.  Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960 , 2008, Nature.

[11]  T. Caro,et al.  Worldwide prevalence of lentivirus infection in wild feline species: epidemiologic and phylogenetic aspects , 1992, Journal of virology.

[12]  H. Varmus,et al.  Characterization of the nucleic acid product of the visna virus RNA dependent DNA polymerase. , 1974, Virology.

[13]  Kazuyuki Aihara,et al.  APOBEC3D and APOBEC3F Potently Promote HIV-1 Diversification and Evolution in Humanized Mouse Model , 2014, PLoS pathogens.

[14]  J. Pecon-Slattery,et al.  Evolution of Puma Lentivirus in Bobcats (Lynx rufus) and Mountain Lions (Puma concolor) in North America , 2014, Journal of Virology.

[15]  Reuben S. Harris,et al.  Retroviral restriction by APOBEC proteins , 2004, Nature Reviews Immunology.

[16]  E. Holmes,et al.  Endogenous Lentiviruses in the Ferret Genome , 2012, Journal of Virology.

[17]  L. Montagnier,et al.  Molecular cloning and polymorphism of the human immune deficiency virus type 2 , 1986, Nature.

[18]  J. Casey,et al.  Comparative replication kinetics of two cytopathic feline lentiviruses ex vivo. , 2005, Virology.

[19]  M. Desport,et al.  Jembrana disease virus: host responses, viral dynamics and disease control. , 2010, Current HIV research.

[20]  G E Wilcox,et al.  Jembrana disease. , 2022, Australian veterinary journal.

[21]  Elisabeth S. Vrba,et al.  The Fossil Record and Evolution of Bovidae: State of the Field , 2009 .

[22]  Bruce T Lahn,et al.  Positive selection on the human genome. , 2004, Human molecular genetics.

[23]  J. Darlix,et al.  APOBEC3A Is a Specific Inhibitor of the Early Phases of HIV-1 Infection in Myeloid Cells , 2011, PLoS pathogens.

[24]  M. Neuberger,et al.  DNA deamination in immunity: AID in the context of its APOBEC relatives. , 2007, Advances in immunology.

[25]  Y. Koyanagi,et al.  Small ruminant lentiviral Vif proteins commonly utilize cyclophilin A, an evolutionarily and structurally conserved protein, to degrade ovine and caprine APOBEC3 proteins , 2016, Microbiology and immunology.

[26]  M. Worobey,et al.  Endogenous lentiviral elements in the weasel family (Mustelidae). , 2012, Molecular biology and evolution.

[27]  V. Pathak,et al.  Identification of Two Distinct Human Immunodeficiency Virus Type 1 Vif Determinants Critical for Interactions with Human APOBEC3G and APOBEC3F , 2007, Journal of Virology.

[28]  M. Emerman,et al.  Ancient Adaptive Evolution of the Primate Antiviral DNA-Editing Enzyme APOBEC3G , 2004, PLoS biology.

[29]  M. Emerman,et al.  Convergence and Divergence in the Evolution of the APOBEC3G-Vif Interaction Reveal Ancient Origins of Simian Immunodeficiency Viruses , 2013, PLoS pathogens.

[30]  M. Stanhope,et al.  Molecules consolidate the placental mammal tree. , 2004, Trends in ecology & evolution.

[31]  J Leibowitch,et al.  Isolation of human T-cell leukemia virus in acquired immune deficiency syndrome (AIDS). , 1983, Science.

[32]  A. Kondrashov.  Deleterious mutations and the evolution of sexual reproduction , 1988, Nature.

[33]  S. O’Brien,et al.  Seroprevalence and Genomic Divergence of Circulating Strains of Feline Immunodeficiency Virus among Felidae and Hyaenidae Species , 2005, Journal of Virology.

[34]  J. Dudley,et al.  APOBECs and virus restriction. , 2015, Virology.

[35]  M. Peretz,et al.  Productive Replication of vif-Chimeric HIV-1 in Feline Cells , 2010, Journal of Virology.

[36]  John S. Albin,et al.  Interactions of host APOBEC3 restriction factors with HIV-1 in vivo: implications for therapeutics , 2010, Expert Reviews in Molecular Medicine.

[37]  D. S. Adams,et al.  A pathogenetic study of the early connective tissue lesions of viral caprine arthritis-encephalitis. , 1980, The American journal of pathology.

[38]  Michael Emerman,et al.  Evolutionary conflicts between viruses and restriction factors shape immunity , 2012, Nature Reviews Immunology.

[39]  W. Sugiura,et al.  The APOBEC3C crystal structure and the interface for HIV-1 Vif binding , 2012, Nature Structural &Molecular Biology.

[40]  A. Hassanin,et al.  Molecular phylogeny of the tribe Bovini (Bovidae, Bovinae) and the taxonomic status of the Kouprey, Bos sauveli Urbain 1937. , 2004, Molecular phylogenetics and evolution.

[41]  F. Kirchhoff.  Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. , 2010, Cell host & microbe.

[42]  P. Bieniasz,et al.  Generation of Simian-Tropic HIV-1 by Restriction Factor Evasion , 2006, Science.

[43]  H. Ode,et al.  Structural Features of Antiviral APOBEC3 Proteins are Linked to Their Functional Activities , 2011, Front. Microbio..

[44]  F. Gao,et al.  Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes , 1999, Nature.

[45]  M. Emerman,et al.  The host restriction factor APOBEC3G and retroviral Vif protein coevolve due to ongoing genetic conflict. , 2012, Cell host & microbe.

[46]  C. Feschotte,et al.  Parallel Germline Infiltration of a Lentivirus in Two Malagasy Lemurs , 2009, PLoS genetics.

[47]  A. Koito,et al.  Intrinsic restriction activity by AID/APOBEC family of enzymes against the mobility of retroelements , 2011, Mobile genetic elements.

[48]  Alteration of Immune Responses of Rabbits Infected with Bovine Immunodeficiency‐Like Virus , 1994, Microbiology and immunology.

[49]  Mamoru Ito,et al.  Remarkable Lethal G-to-A Mutations in vif-Proficient HIV-1 Provirus by Individual APOBEC3 Proteins in Humanized Mice , 2010, Journal of Virology.

[50]  Y. Koyanagi,et al.  Species‐specific differences in the ability of feline lentiviral Vif to degrade feline APOBEC3 proteins , 2016, Microbiology and immunology.

[51]  Sue VandeWoude,et al.  Going Wild: Lessons from Naturally Occurring T-Lymphotropic Lentiviruses , 2006, Clinical Microbiology Reviews.

[52]  R. Desrosiers,et al.  Isolation of T-cell tropic HTLV-III-like retrovirus from macaques. , 1985, Science.

[53]  M. Carpenter,et al.  A Naturally Occurring Domestic Cat APOBEC3 Variant Confers Resistance to Feline Immunodeficiency Virus Infection , 2015, Journal of Virology.

[54]  N. Pedersen,et al.  Isolation of a T-lymphotropic virus from domestic cats with an immunodeficiency-like syndrome. , 1987, Science.

[55]  E. Arts,et al.  Tracking a century of global expansion and evolution of HIV to drive understanding and to combat disease. , 2011, The Lancet. Infectious diseases.

[56]  A. Kiefer,et al.  Molecular species identification boosts bat diversity , 2007, Frontiers in Zoology.

[57]  Jianzhi Zhang.  Evolution by gene duplication: an update , 2003 .

[58]  Andrej Sali,et al.  Vif hijacks CBF-β to degrade APOBEC3G and promote HIV-1 infection , 2011, Nature.

[59]  Martine Peeters,et al.  Hybrid Origin of SIV in Chimpanzees , 2003, Science.

[60]  V. Simon,et al.  The Activity Spectrum of Vif from Multiple HIV-1 Subtypes against APOBEC3G, APOBEC3F, and APOBEC3H , 2011, Journal of Virology.

[61]  J. Garcia,et al.  HIV Restriction by APOBEC3 in Humanized Mice , 2013, PLoS pathogens.

[62]  R. LaRue,et al.  Lentiviral Vif Degrades the APOBEC3Z3/APOBEC3H Protein of Its Mammalian Host and Is Capable of Cross-Species Activity , 2010, Journal of Virology.

[63]  D. de Andrés,et al.  Small Ruminant Lentiviruses: Genetic Variability, Tropism and Diagnosis , 2013, Viruses.

[64]  O. Pybus,et al.  Discovery and analysis of the first endogenous lentivirus , 2007, Proceedings of the National Academy of Sciences.

[65]  M. Licursi,et al.  Evidence of bovine immunodeficiency virus (BIV) infection: serological survey in Argentina. , 2008, Research in veterinary science.

[66]  Xianghui Yu,et al.  Identification of a Cullin5-ElonginB-ElonginC E3 Complex in Degradation of Feline Immunodeficiency Virus Vif-Mediated Feline APOBEC3 Proteins , 2011, Journal of Virology.

[67]  D. Serwadda,et al.  The history and challenge of HIV prevention , 2008, The Lancet.

[68]  J. Garcia,et al.  APOBEC3G and APOBEC3F Act in Concert To Extinguish HIV-1 Replication , 2016, Journal of Virology.

[69]  R. LaRue,et al.  Vif Proteins of Human and Simian Immunodeficiency Viruses Require Cellular CBFβ To Degrade APOBEC3 Restriction Factors , 2011, Journal of Virology.

[70]  M. Poss,et al.  Restrictions to cross-species transmission of lentiviral infection gleaned from studies of FIV. , 2010, Veterinary immunology and immunopathology.

[71]  V. Simon,et al.  APOBEC3A, APOBEC3B, and APOBEC3H Haplotype 2 Restrict Human T-Lymphotropic Virus Type 1 , 2012, Journal of Virology.

[72]  Arndt von Haeseler,et al.  C-->U editing of apolipoprotein B mRNA in marsupials: identification and characterisation of APOBEC-1 from the American opossum Monodelphus domestica , 1999, Nucleic Acids Res..

[73]  J. Krebs,et al.  Arms races between and within species , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[74]  S. O’Brien,et al.  Guidelines for Naming Nonprimate APOBEC3 Genes and Proteins , 2008, Journal of Virology.

[75]  Xiaojun Wang,et al.  Analysis of Human APOBEC3H Haplotypes and Anti-Human Immunodeficiency Virus Type 1 Activity , 2011, Journal of Virology.

[76]  A. Koito,et al.  Opossum APOBEC1 is a DNA mutator with retrovirus and retroelement restriction activity , 2017, Scientific Reports.

[77]  M. Emerman,et al.  A Single Nucleotide Polymorphism in Human APOBEC3C Enhances Restriction of Lentiviruses , 2016, PLoS pathogens.

[78]  W. Mcnab,et al.  A serological survey for bovine immunodeficiency-like virus in Ontario dairy cattle and associations between test results, production records and management practices. , 1994, Canadian journal of veterinary research = Revue canadienne de recherche veterinaire.

[79]  H. Varmus,et al.  Demonstration of a DNA provirus in the lytic growth of visna virus. , 1973, Nature: New biology.

[80]  Jean-Yves Nau,et al.  [A new human immunodeficiency virus derived from gorillas]. , 2009, Revue medicale suisse.

[81]  R. Avery,et al.  Proviral organization and sequence analysis of feline immunodeficiency virus isolated from a Pallas' cat. , 1997, Virology.

[82]  R. Shafer,et al.  A transitional endogenous lentivirus from the genome of a basal primate and implications for lentivirus evolution , 2008, Proceedings of the National Academy of Sciences.

[83]  M. Gonda,et al.  Serologic evidence for bovine immunodeficiency virus infection in France. , 1996, Veterinary microbiology.

[84]  Y. Chebloune,et al.  Small Ruminant Lentiviruses (SRLVs) Break the Species Barrier to Acquire New Host Range , 2013, Viruses.

[85]  G. Silvestri,et al.  Nonpathogenic simian immunodeficiency virus infections. , 2012, Cold Spring Harbor perspectives in medicine.

[86]  Y. Koyanagi,et al.  A naturally occurring bovine APOBEC3 confers resistance to bovine lentiviruses: implication for the co-evolution of bovids and their lentiviruses , 2016, Scientific Reports.

[87]  G. Wilcox,et al.  Characteristics of a retrovirus associated with Jembrana disease in Bali cattle. , 1993, The Journal of general virology.

[88]  M. Emerman,et al.  Host gene evolution traces the evolutionary history of ancient primate lentiviruses , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[89]  Marian C. Horzinek,et al.  Bovine immunodeficiency virus: immunochemical characterization and serological survey. , 1991, The Journal of general virology.

[90]  D. S. Adams,et al.  Immune responses of goats persistently infected with caprine arthritis-encephalitis virus , 1980, Infection and immunity.

[91]  M. Carpenter,et al.  The DNA cytosine deaminase APOBEC3H haplotype I likely contributes to breast and lung cancer mutagenesis , 2016, Nature Communications.

[92]  M. Onuma,et al.  Infection and dysfunction of monocytes induced by experimental inoculation of calves with bovine immunodeficiency-like virus. , 1992, Journal of acquired immune deficiency syndromes.

[93]  K. Ohashi,et al.  Phylogenetic relationships of bovine immunodeficiency virus in cattle and buffaloes based on surface envelope gene sequences , 2001, Archives of Virology.

[94]  S. Conticello.  The AID/APOBEC family of nucleic acid mutators , 2008, Genome Biology.

[95]  W. Boyce,et al.  Feline Immunodeficiency Virus Cross-Species Transmission: Implications for Emergence of New Lentiviral Infections , 2016, Journal of Virology.

[96]  M. J. Van Der Maaten,et al.  Isolation of a virus from cattle with persistent lymphocytosis. , 1972, Journal of the National Cancer Institute.

[97]  R. König,et al.  Species-Specific Exclusion of APOBEC3G from HIV-1 Virions by Vif , 2003, Cell.

[98]  Robert J Gifford,et al.  Viral evolution in deep time: lentiviruses and mammals. , 2012, Trends in genetics : TIG.

[99]  B. Sigurdsson,et al.  VISNA, A DEMYELINATING TRANSMISSIBLE DISEASE OF SHEEP , 1957, Journal of neuropathology and experimental neurology.

[100]  Michael Emerman,et al.  The Role of the Antiviral APOBEC3 Gene Family in Protecting Chimpanzees against Lentiviruses from Monkeys , 2015, PLoS pathogens.

[101]  G. Wilcox,et al.  Sequence analysis of Jembrana disease virus strains reveals a genetically stable lentivirus. , 2007, Virus research.

[102]  N. Yuhki,et al.  Vif of Feline Immunodeficiency Virus from Domestic Cats Protects against APOBEC3 Restriction Factors from Many Felids , 2010, Journal of Virology.

[103]  M. Emerman,et al.  Natural Polymorphisms in Human APOBEC3H and HIV-1 Vif Combine in Primary T Lymphocytes to Affect Viral G-to-A Mutation Levels and Infectivity , 2014, PLoS genetics.

[104]  F. Hecht,et al.  HIV-1 Vif adaptation to human APOBEC3H haplotypes. , 2013, Cell host & microbe.

[105]  P. Sharp,et al.  Origins of HIV and the AIDS pandemic. , 2011, Cold Spring Harbor perspectives in medicine.

[106]  Lela Lackey,et al.  Human and Rhesus APOBEC3D, APOBEC3F, APOBEC3G, and APOBEC3H Demonstrate a Conserved Capacity To Restrict Vif-Deficient HIV-1 , 2011, Journal of Virology.

[107]  E. Foni,et al.  Seroprevalence to bovine immunodeficiency virus and lack of association with leukocyte counts in Italian dairy cattle. , 1998, Preventive veterinary medicine.

[108]  C. Boesch,et al.  Origin of the HIV-1 group O epidemic in western lowland gorillas , 2015, Proceedings of the National Academy of Sciences.

[109]  V. Andrésdóttir,et al.  Evolutionarily conserved and non-conserved retrovirus restriction activities of artiodactyl APOBEC3F proteins , 2006, Nucleic acids research.

[110]  Y. Koyanagi,et al.  Feline Immunodeficiency Virus Evolutionarily Acquires Two Proteins, Vif and Protease, Capable of Antagonizing Feline APOBEC3 , 2017, Journal of Virology.

[111]  M. Malim,et al.  Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein , 2002, Nature.

[112]  S. O’Brien,et al.  Evolution of feline immunodeficiency virus in Felidae: implications for human health and wildlife ecology. , 2008, Veterinary immunology and immunopathology.

[113]  P. Autissier,et al.  Evolutionary and Functional Analysis of Old World Primate TRIM5 Reveals the Ancient Emergence of Primate Lentiviruses and Convergent Evolution Targeting a Conserved Capsid Interface , 2015, PLoS pathogens.

[114]  Sean L. Evans,et al.  T-cell differentiation factor CBF-β regulates HIV-1 Vif-mediated evasion of host restriction , 2011, Nature.

[115]  M. Culver,et al.  Genetic and phylogenetic divergence of feline immunodeficiency virus in the puma (Puma concolor) , 1996, Journal of virology.

[116]  V. Simon,et al.  APOBEC3G Polymorphism as a Selective Barrier to Cross-Species Transmission and Emergence of Pathogenic SIV and AIDS in a Primate Host , 2013, PLoS pathogens.

[117]  Timothy P. L. Smith,et al.  The artiodactyl APOBEC3 innate immune repertoire shows evidence for a multi-functional domain organization that existed in the ancestor of placental mammals , 2008, BMC Molecular Biology.

[118]  R. Harris,et al.  Endogenous Origins of HIV-1 G-to-A Hypermutation and Restriction in the Nonpermissive T Cell Line CEM2n , 2012, PLoS pathogens.

[119]  S. Vandewoude,et al.  Accessory Genes Confer a High Replication Rate to Virulent Feline Immunodeficiency Virus , 2013, Journal of Virology.

[120]  Joel O. Wertheim,et al.  Dating the Age of the SIV Lineages That Gave Rise to HIV-1 and HIV-2 , 2009, PLoS Comput. Biol..

[121]  Bronwen L. Aken,et al.  The sheep genome illuminates biology of the rumen and lipid metabolism , 2014, Science.

[122]  K. Ohashi,et al.  Evidence for bovine immunodeficiency virus infection in cattle in Zambia. , 2004, The Japanese journal of veterinary research.