From ancestral infectious retroviruses to bona fide cellular genes: Role of the captured syncytins in placentation

Dupressoír, Anne; Lavialle, Christian; Heidmann, Thiérry

doi:10.1016/j.placenta.2012.05.005

Cited by 295 publications

(255 citation statements)

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“…R. Soc. B 370: 20140070 and different syncytins are found in different clades [59,60]. Syncytins 1 and 2, which promote syncytiotrophoblast formation in human placenta, are present in other platyrrhine and catarrhine primates, but could not be detected in the brown lemur (Eulemur fulvus).…”

Section: Discussionmentioning

confidence: 99%

The role of invasive trophoblast in implantation and placentation of primates

Carter

Enders

Pijnenborg

2015

Phil. Trans. R. Soc. B

130

112

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We here review the evolution of invasive placentation in primates towards the deep penetration of the endometrium and its arteries in hominoids. The strepsirrhine primates (lemurs and lorises) have non-invasive, epitheliochorial placentation, although this is thought to be derived from a more invasive type. In haplorhine primates, there is differentiation of trophoblast at the blastocyst stage into syncytial and cellular trophoblast. Implantation involves syncytiotrophoblast that first removes the uterine epithelium then consolidates at the basal lamina before continuing into the stroma. In later stages of pregnancy, especially in Old World monkeys and apes, cytotrophoblast plays a greater role in the invasive process. Columns of trophoblast cells advance to the base of the implantation site where they spread out to form a cytotrophoblastic shell. In addition, cytotrophoblasts advance into the lumen of the spiral arteries. They are responsible for remodelling these vessels to form wide, low-resistance conduits. In human and great apes, there is additional invasion of the endometrium and its vessels by trophoblasts originating from the base of the anchoring villi. Deep trophoblast invasion that extends remodelling of the spiral arteries to segments in the inner myometrium evolved in the common ancestor of gorilla, chimp and human.

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Section: Discussionmentioning

confidence: 99%

The role of invasive trophoblast in implantation and placentation of primates

Carter

Enders

Pijnenborg

2015

Phil. Trans. R. Soc. B

130

112

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“…While the bulk of transposable element insertions suffer the ignominy of mutational abrasion, some copies have been protected against mutation, suggesting that host genomes have domesticated these insertions for their own purpose. There are some spectacular examples in which protein-coding genes domesticated from transposon insertions have been usurped for host roles, from mediating the genomic rearrangements required for antibody diversification (Agrawal et al, 1998;Hiom et al, 1998), to placental reproduction (Dupressoir et al, 2012), to centromere function (Smit and Riggs, 1996;Tudor et al, 1992) and genome defense (Benit et al, 1997;Best et al, 1996;McLaughlin et al, 2014;Yan et al, 2009). In addition to domestication for their protein-coding function, networks of transposable element insertions distributed across the genome have been domesticated to orchestrate transcriptional programs.…”

Section: The Scourge Of Transposable Elementsmentioning

confidence: 99%

Genetic conflicts: the usual suspects and beyond

McLaughlin

Malik

2017

Journal of Experimental Biology

132

127

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Selfishness is pervasive and manifests at all scales of biology, from societies, to individuals, to genetic elements within a genome. The relentless struggle to seek evolutionary advantages drives perpetual cycles of adaptation and counter-adaptation, commonly referred to as Red Queen interactions. In this review, we explore insights gleaned from molecular and genetic studies of such genetic conflicts, both extrinsic (between genomes) and intrinsic (within genomes or cells). We argue that many different characteristics of selfish genetic elements can be distilled into two types of advantages: an overreplication advantage (e.g. mobile genetic elements in genomes) and a transmission distortion advantage (e.g. meiotic drivers in populations). These two general categories may help classify disparate types of selfish genetic elements.

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“…Some ERVs are domesticated by their hosts and eventually gain physiological functions, such as placentation or viral resistance, in exchange for the loss of their ancestral, viral properties (21)(22)(23)(24)(25)(26)(27)(28)(29). For example, the Friend virus susceptibility4 (Fv4) gene, which is an endogenous defective provirus that resembles the ecotropic murine leukemia virus (MLV), encodes a restriction factor against ecotropic MLVs (30)(31)(32).…”

Section: Domestic Cats Are Colonized With Various Exogenous Retrovirumentioning

confidence: 99%

Ancestral Mutations Acquired in Refrex-1, a Restriction Factor against Feline Retroviruses, during its Cooption and Domestication

Ito

Baba

Kawasaki

et al. 2016

J Virol

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Endogenous retroviruses (ERVs) are remnants of ancestral retroviral infections of germ cells. Retroviral endogenization is an adaptation process for the host genome, and ERVs are gradually attenuated or inactivated by mutation. However, some ERVs that have been "domesticated" by their hosts eventually gain physiological functions, such as placentation or viral resistance. We previously reported the discovery of Refrex-1, a soluble antiretroviral factor in domestic cats that specifically inhibits infection by feline leukemia virus subgroup D (FeLV-D), a chimeric virus of FeLV, and a feline ERV, ERV-DC. Refrex-1 is a truncated envelope protein (Env) encoded by both ERV-DC7 and ERV-DC16 proviral loci. Here, we reconstituted ancestral and functional Env from ERV-DC7 and ERV-DC16 envelope genes (env) by inducing reverse mutations. Unexpectedly, ERV-DC7 and ERV-DC16 full-length Env (ERV-DC7 fl and ERV-DC16 fl), reconstructed by removing stop codons, did not produce infectious viral particles. ERV-DC7 fl and ERV-DC16 fl were highly expressed in cells but were not cleaved into surface subunits (SU) and transmembrane subunits, nor were they incorporated into virions. G407R/N427I-A429T and Y431D substitutions within the SU Cterminal domain of ERV-DC7 fl and ERV-DC16 fl, respectively, caused these dysfunctions. The residues glycine 407 and tyrosine 431 are relatively conserved among infectious gammaretroviruses, and their substitution causes the same dysfunctions as the tested retroviruses. Our results reveal that specific mutations within the SU C-terminal domain suppressed Env cleavage and incorporation into virions and indicate that these mutations contributed to the domestication of Refrex-1 through multistep events that occurred in the postintegration period. IMPORTANCEDomestic cats are colonized with various exogenous retroviruses (exRVs), such as feline leukemia virus (FeLV), and their genomes contain numerous ERVs, some of which are replication-competent proviruses. The feline hosts, exRVs, and ERVs have complicated genetic interactions and provide an interesting field model for triangular relationships: recombination between FeLV and ERV-DC, which is a feline ERV, generated FeLV-D, a chimeric virus, and FeLV-D is restricted by Refrex-1, an antiretroviral factor corresponding to truncated Env of ERV-DC7 and ERV-DC16. Here, we reconstructed ancestral, functional Env from ERV-DC7 and ERV-DC16 env by inducing reverse mutations to elucidate how Refrex-1 was generated from its ancestor. Our results reveal that they were repeatedly inactivated by mutations preventing Env maturation. Our results provide insights into how ERVs were "domesticated" by their hosts and identify the mutations that mediated these evolutions. Notably, experiments that restore inactivated ERVs might uncover previously unrecognized features or properties of retroviruses. E ndogenous retroviruses (ERVs) are present in all vertebrate genomes and are thought to be the remnants of ancestral germ line infections by exogenous retroviruses (exRVs)...

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From ancestral infectious retroviruses to bona fide cellular genes: Role of the captured syncytins in placentation

Cited by 295 publications

References 46 publications

The role of invasive trophoblast in implantation and placentation of primates

The role of invasive trophoblast in implantation and placentation of primates

Genetic conflicts: the usual suspects and beyond

Ancestral Mutations Acquired in Refrex-1, a Restriction Factor against Feline Retroviruses, during its Cooption and Domestication

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