- Open Access
A conflict of interest: the evolutionary arms race between mammalian APOBEC3 and lentiviral Vif
© The Author(s) 2017
- Received: 3 March 2017
- Accepted: 27 April 2017
- Published: 8 May 2017
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.
- Evolutionary arms race
Classification of lentiviruses
Characteristics of APOBEC3 genes
Apolipoprotein B mRNA editing enzyme catalytic polypeptide-like 3 (APOBEC3; A3) proteins are cellular cytidine deaminases and are specifically found in mammals but not in other vertebrates [3, 4]. The A3 proteins of mammals, particularly those of primates, are considered to be cell-intrinsic immune factors that combat viruses, including lentiviruses and retrotransposons. To limit the replication of lentiviruses, the A3 proteins expressed in virus-producing cells are packaged into virions released from the cell. Then, A3 proteins are brought into neighboring cells and halt viral replication via enzymatic hypermutation of the viral genome and by blocking reverse transcription directly (for more detail, see references [5, 6]. As a result, lentiviral virions produced in the presence of A3 proteins are dramatically less infectious.
Based on the sequence homology of zinc-coordinating (Z) catalytic domains, mammalian A3 proteins are classified into three subsets: Z1, Z2 or Z3. Each A3 protein is composed of single or double Z domains . For instance, human A3A, A3C and A3H encode single Z1, Z2 and Z3 domain proteins, respectively, whereas human A3B, A3D, A3F and A3G encode double Z domain proteins (Fig. 2) . Previous molecular phylogenetic studies have indicated that the mammalian A3 genes are evolving under positive selection [9, 10] and the gene duplications themselves likely result from selection pressures imposed by virus infections .
An evolutionary arms race between mammals and lentiviruses
In the field of virology, revealing the co-evolutionary relationship between viruses and their hosts is intriguing and is crucial to understanding how viruses can impact the evolution of their hosts and vice versa. As summarized in Fig. 1, a hallmark of lentivirus ecology is the emergence of new lineages via cross-species transmission (CST) events. Additionally, viral recombination between lentivirus strains occurs frequently. As a result, reconstructing the dynamic relationship between lentiviruses and their hosts is complex.
To gain a better understanding of the evolutionary conflict between lentiviruses and their host species, cell-based virological experiments with a focus on the functional relationship between viral and host proteins have recently been conducted in combination with a molecular phylogenetic approach. This strategy stems from the concept known as the “Red Queen hypothesis ”, which proposes that games of cat-and-mouse occur between viral and host proteins as they engage with one another over time [13–15]. Based on this concept, various experiments have been conducted using mammalian A3 proteins and a lentiviral protein, viral infectivity factor (Vif).
Vif-A3 interplay in terms of the CST events and the evolutionary arms race of lentiviruses and mammals
Throughout lentiviral lineages, the vif gene serves the same functional purpose of degrading antiviral A3 proteins. However, there is only ~25% conservation of its genetic sequence . Despite the significant divergence of this genetic sequence, all lentiviral Vifs are capable of hijacking the cullin-RING ubiquitin ligase (CRL) complex, which consists of cullin E3 ubiquitin ligase (CUL; CUL2 or CUL5), ring box protein 2 (RBX2) and elongin B/C (ELOB/C) [81, 110, 111]. Although the vif sequence is highly divergent, the S/TLQ motif is highly conserved in all lentiviral Vif proteins, and Vif interacts with the CRL complex in an S/TLQ motif-dependent manner .
In 2012, two groups identified core binding factor subunit β (CBFB) as the co-factor necessary for PLV Vif to degrade host A3 proteins [110, 111]. PLV Vif, CBFB and ELOB/C form a substrate adaptor for CUL5 and RBX2, which allows the Vif interaction with suitable and susceptible A3 proteins . Vif is the adaptor between the A3 proteins and the CRL complex . CBFB is required for PLV Vif to degrade host A3s but is dispensable for other lentiviral Vif proteins [81, 110–112].
A comparative approach combining proteomic, biochemical, structural, and virological techniques conducted by Kane et al.  identified cyclophilin A (CYPA; also known as peptidylprolyl isomerase A) as the co-factor for MVV Vif. The requirement of CYPA is specific for MVV Vif (strain Iceland) , and a subsequent study has recently revealed that CAEV (strains Cork, 1GA, and Roccaverano), in addition to MVV Vif (strain 1514), also bind to CYPA . These observations indicate that the CYPA requirement for host A3 degradation is a common feature of SRLV Vif proteins, although PLV Vif does not appear to need CYPA. Moreover, a combination approach of molecular phylogenetic and structural techniques has suggested that mammalian CBFB and CYPA are evolutionarily and structurally conserved . Therefore, lentiviral Vif may have evolved to utilize evolutionarily and structurally stable proteins to degrade host A3 proteins . In contrast to PLV and SRLV, it is intriguing that BIV Vif activity does not appear to be reliant on any co-factors, and no co-factors have yet been identified for FIV Vif activity . These insights further suggest that each lentiviral Vif has evolved an individual strategy to adapt to each host mammal.
Here, we described the co-evolutionary relationship between mammalian A3 genes and exogenous lentiviruses. However, many intriguing questions remain: when and how was the A3 gene acquired in mammals? When and how did lentiviruses acquire the vif gene? Was vif gene acquired for the purpose of combating host A3s? Or did Vif perform other functions in lentivirus replication that were supplanted? Why is vif gene lacking in EIAV?
Regarding the origin of A3 genes; A3 is known as a component of AID/APOBEC family. AID (activation-induced cytidine deaminase) is a nucleotide mutator contributing to the somatic hypermutation of immunoglobulin genes in B cells, while APOBEC1 edits the mRNA encoding apolipoprotein B that is expressed in small intestine (reviewed in [113, 114]). Since both AID and APOBEC1 are commonly encoded in all mammals as well as birds and reptiles , it is plausible to speculate that these genes can be the origin of A3 genes in mammals. On the other hand, it is known that A3 genes are not present in opossums (Fig. 2) , suggesting that A3 genes were acquired after (in which family/order of mammals?) divergence with Marsupialia. However, it is unclear whether A3 gene acquisition occurred in the common ancestor of Eutheria or Boreoeutheria (see Fig. 2). Moreover, we still do not know how many A3 genes are encoded in the other mammals such as bats and elephants (Fig. 2). Particularly, the mammals belonging to the order Chiroptera (e.g., microbats and megabats) are highly divergent . Therefore, it is plausible to assume that Chiroptera A3 genes exhibit a high level of diversity. This information will be useful for considering the evolutionary scenario of A3 acquisition/duplication, which is likely to depend on the evolutionary relationship between lentiviruses and these hosts. Furthermore, Ikeda et al.  have recently demonstrated that opossum A1 possesses the activity to impair the replication of lentiviruses and retroelements, suggesting that certain marsupial AID/APOBEC family proteins potently exhibit compensatory activity to limit lentiviral replication instead of A3. Nevertheless, it is still intriguing that the duplications of AID and A1 genes have not been found and that the gene duplication of AID/APOBEC family in mammals is specifically occurred in A3 genes.
The driving force and moment of A3 duplication are still both unclear. In contrast to the Z1 and Z2 domains, it is intriguing that the duplication of Z3 domain has not been observed in any mammals (Fig. 2). This is reminiscent of the “Kondrashov hypothesis” (also known as “deterministic mutation hypothesis”), which assumes that the majority of deleterious mutations are of small effect and that each subsequent mutation has an increasingly large effect on host fitness . According to this concept, duplication of the A3Z3 gene may be evolutionarily constrained due to deleterious effects for the host organism. The possibility of host A3Z3 toxicity is further supported by findings related to the A3H (the ortholog to A3Z3 in primates) gene of human and chimpanzee. Human has seven A3H haplotypes, but four are not expressed at the protein level . In contrast, chimpanzee A3H is monomorphic, and this protein is expressed , suggesting that there is a cost to maintain multiple copies of functional A3H. In fact, a recent paper has revealed that human A3H likely contributes to cancer mutagenesis . Therefore, functional A3H has been evolutionarily lost in humans after the divergence from chimpanzees due to its toxicity.
Similar to mammalian A3 genes, the origin of lentiviral vif genes is also unclear. In this regard, endogenous lentiviruses have been detected in the genomes of various mammals, including European rabbits (Oryctolagus cuniculus) , lemurs belonging to two different genera (Microcebus and Cheirogaleus) [121, 122], and ferrets (Mustela putorius furo) [123, 124]. More intriguingly, all endogenous lentiviruses ever detected appear to encode putative vif sequences [121–123]. Considering that all exogenous lentiviruses, with the exception of EIAV in horses, also possess this accessory gene, vif gene is an ancient lentiviral component with crucial importance to maintaining lentivirus infections worldwide.
YN, HA, AS, EY, MM, GJ-F, YK and KS wrote the paper. All authors read and approved the final manuscript.
We would like to thank Robert Gifford (University of Glasgow, United Kingdom), Alex Compton (National Cancer Institute, USA) and Terumasa Ikeda (University of Minnesota, USA) for providing crucial comments, and Mss. Naoko Misawa and Kotubu Misawa for their dedicated support.
The authors declare that they have no competing interests.
This study was supported in part by CREST, JST (to KS); Takeda Science Foundation (to KS); Mochida Memorial Foundation for Medical and Pharmaceutical Research (to KS); Salt Science Research Foundation (to KS); Smoking Research Foundation (to KS); Grants-in-Aid for Scientific Research C 15K07166 (to KS), Scientific Research B (Generative Research Fields) 16KT0111 (to KS), and Scientific Research on Innovative Areas 17H05813 (to KS) and 24115008 (to YK) from JSPS; the Platform Project for Supporting in Drug Discovery and Life Science Research (Platform for Dynamic Approaches to Living System) from AMED (to EY); and the JSPS Core-to-Core program, A. Advanced Research Networks (to YK); and Research on HIV/AIDS 16fk0410203h0002 from AMED (to YK).
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