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A Proviral Puzzle with a Prosimian Twist

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A Proviral Puzzle with a Prosimian Twist COMMENTARY A proviral puzzle with a prosimian twist Welkin E. Johnson1 Department of Microbiology and Molecular Genetics, New England Primate Research Center, Harvard Medical School, Southborough, MA 01772 iruses are obligatory intracellu- ported last year (3). Using an iterative somal DNA. In the event that this pro- lar parasites, and as such they BLAST procedure, Gifford and col- cess occurs in germ-line DNA—either cannot exist in the absence of leagues (1) have now found small se- directly by infection of germ-line tissue a host. It follows that the natu- quence fragments resembling lentiviral or indirectly by infection of embryonic Vral history of the viruses is inseparable Micro- cells destined to differentiate into germ- sequences in the archives of the from that of their animal hosts, and to cebus murinus (gray mouse lemur) ge- line tissue—the newly-integrated provi- reconstruct the evolutionary past of a nome project. Multiple proviral frag- rus constitutes a heritable, insertional virus is to understand much about the ments were uncovered, and together mutation. Proviral sequences in the history of those species it colonizes. Un- with additional sequences recovered by germ line are referred to as endogenous fortunately, viruses do not leave behind PCR, the authors were able to piece retroviruses or ERVs (the term is mis- physical remnants of their presence: together a consensus viral genome. The leading, because it refers strictly to a once a viral species becomes extinct, it reconstructed provirus, which they refer sequence’s retroviral origin and does not vanishes without a trace. At best, the to as pSIVgml (prosimian immunodefi- imply the capacity to express infectious evolutionary history of most viruses can ciency virus of gray mouse lemur), clus- virions). Because an ERV-containing only be inferred indirectly through the ters with modern primate lentiviruses in locus can be inherited by any or all lin- phylogenetic comparison of modern, eages descending from the original host living viruses. There is, however, one species, the distribution of the ERV prominent exception: the Retroviridae. ERVs have been likened among related taxa is an indication of The genomes of all animal species have its relative age. In this regard, ERVs accumulated (over hundreds of millions to fossils, with modern have been likened to fossils, with mod- of years) the proviral remnants of an- ern genomes filling the role of geologi- cient, largely extinct, retroviral species. genomes filling the role cal strata (4). This vast archive of viral ‘‘fossils’’ com- In the beginning, chromosomes bear- prises millions upon millions of ele- of geological strata. ing a newly-formed ERV will be exceed- ments, a tiny fraction of which are com- ingly rare relative to wild-type chromo- ing to light as a consequence of genome somes (i.e., lacking the provirus). An sequencing efforts. From the genome of phylogenetic analyses incorporating rep- upstream battle against the flow of ran- the gray mouse lemur, a diminutive pri- Ͻ resentatives of all known lentiviral taxa. dom genetic drift ensues, and the vast mate ( 100 g) found only on the island In addition, a comparison of structural majority of ERVs are probably lost to of Madagascar, Gifford and colleagues features provides new insight into lenti- antiquity. With time and luck, an ERV (1) have now unearthed a retroviral fos- viral evolution. For example, pSIVgml may be passed on more often than not, sil unambiguously related to the modern contains a dUTPase domain embedded spreading slowly through the gene pool AIDS viruses, as reported in this issue in the Gag-Pol polyprotein. A dUTPase and eventually achieving fixation [if the of PNAS. How it came to be there is an is present in the same location in some ERV happens to confer some benefit on intriguing, and as yet unsolved, evolu- nonprimate lentiviruses, but is not found the organism, it might even get a boost tionary mystery. in HIV/SIV, suggesting that it is an an- along the way from positive selection The Lemur’s Tale cestral feature that was lost in the lin- (5)]. For these reasons, the age of ERV The lentiviruses constitute a genus eage leading to the modern primate len- loci may vastly postdate the initial incur- within the Retroviridae and include the tiviruses. pSIVgml also lacks some of sion of a retrovirus into a new host. De- primate lentiviruses of humans, apes, the accessory genes found among the spite the dismal prospects for any newly- and Old World monkeys, as well as modern primate lentiviruses, such as formed provirus, this outcome has been lentiviruses that have been isolated from Vpr, Vpx, and Vpu, indicating that these consummated many millions of times sheep, goats, cattle, horses, and cats (2). genes are recently derived features of during metazoan evolution, and ERVs The most notorious of the primate lenti- modern HIV/SIV. pSIVgml has an ad- can outnumber actual genes in the ge- viruses are the human immunodefi- ditional ORF in approximately the same nomes of modern species [including ciency viruses (HIV-1 and HIV-2), but location as the nef gene of modern pri- humans (6)]. there are also some 30 or more lenti- mate lentiviruses, although the predicted The retroviral provirus is bracketed viruses indigenous to African primates amino acid sequence does not signifi- by two long terminal repeats (LTRs), (the simian immunodeficiency viruses or cantly resemble any known Nef homo- with the viral genes arrayed in between. SIVs). Endemic SIV infections of Afri- logue. It should prove informative, from The mechanism of reverse transcription can primates are generally nonpatho- an evolutionary perspective, to compare ensures that the 5Ј and 3Ј LTRs are genic, probably reflecting a substantial and contrast cellular functions of resur- identical at the moment of integration. period of virus/host coevolution. Thus rected pSIVgml proteins with their As a component of the nuclear genome, far, lentiviruses have not been detected modern counterparts. in the Asian apes or monkeys, or in any species of New World monkey (primates Genesis Author contributions: W.E.J. wrote the paper. of Central and South America). After a retrovirus enters a cell, the viral The author declares no conflict of interest. Discovery of the first endogenous len- RNA genome is converted into double- See companion article on page 20362. tivirus, in the genome of Oryctolagus stranded DNA and inserted irreversibly 1E-mail: [email protected]. cuniculus, the European rabbit, was re- and at random into the cell’s chromo- © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0811419106 PNAS ͉ December 23, 2008 ͉ vol. 105 ͉ no. 51 ͉ 20051–20052 Downloaded by guest on October 1, 2021 an ERV will accumulate sequence dently estimate the age of pSIVgml ial vector capable of crossing the changes over time, and consequently the based on the distribution of individual Mozambique Channel. Vectored trans- two LTR sequences will diverge in loci among extant species, particularly mission has not been documented for rough proportion to the age of the other mouse lemurs. A thorough assess- any extant retrovirus, making this the ERV. Given a reasonable calibration of ment could give a precise estimate of most speculative scenario. the molecular clock, the genetic distance when pSIVgml-related viruses last Introduction of a lentivirus into a na- between the LTRs of an ERV can be roamed Madagascar, in the process pro- ¨veı host on Madagascar by either the used to estimate its age. If ERVs are viding a lower bound for the most re- second or third scenario raises many molecular fossils, then divergence be- cent common ancestor of the primate interesting questions. What might the tween the LTRs is the counterpart to lentiviruses. As more sequence data ac- result of transmission and colonization radioisotope dating. cumulate from the gray mouse lemur, of the Malagasy primates, long sepa- So how and when did this virus arrive proviruses containing both LTRs may rated from the rest of Africa and the in Madagascar? Endogenization does be identified, which can be used to other primate lineages, have been? not necessarily follow immediately on make additional estimates of insertion From modern examples of cross-species the heels of cross-species transmission, times. ERV sequences are also uniquely transmission, it is clear that such events and analysis of ERV loci can only pro- suited for use as phylogenetic markers, can be overtly pathogenic (witness vide a minimum estimate of when a vi- and accurately estimating the age of the HIV-1 and HIV-2 in humans). It could rus first colonized an ancestral host. Un- SIV-related ERV in lemurs could con- be interesting to ask whether integration fortunately, perhaps because the M. tribute to investigations of the biogeo- times correspond to known extinctions murinus genome project is still a work in graphical history of Madagascar (9). or other major phylogenetic events in progress, a pSIVgml provirus with both lemur history. Is there evidence for LTRs intact was not found. Instead, Gif- The Itinerant Lentivirus cross-species transmissions during the ford et al. (1) used LTR remnants from More than 250 miles of open ocean sep- lemuriform radiation? Do the lemur orthologues of antiretroviral genes such two pSIVgml alleles unambiguously de- arate Madagascar from mainland Africa, as TRIM5, BST2, and APOBEC3 reveal scended from the same original provirus the state of affairs for more than 120 distinct episodes of positive selection? to estimate the age of the insertion. One million years. The progenitor of the Does an exogenous lentivirus, perhaps allele still contained what was clearly a Malagasy primates arrived sometime with the potential for zoonotic trans- 3Ј LTR, whereas the other allele was a later, circa 50–80 MYA (7).
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