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From Viruses to Genes: Syncytins

Abstract

The content of 5–90 million years old retroviruses and even older retrotransposons of animal genomes and the wide variety of modern retroviruses infecting the same range of species suggest that these elements can be assimilated to shuttle across evolution. A snapshot taken a few decades ago showed us the capture of cellular proto-oncogenes by infectious elements, representing the dark side of the communication between the worlds of viruses and animals. Another snapshot we took more recently shows multiple captures by animal genomes of envelope genes originating from infectious retroviruses, illustrating a phenomenon of convergent evolution. This could be seen as the bright side of these relations as those envelopes were shown to be involved in the earlier steps of human development, i.e. fusion of placental syncytiotrophoblastic layer, therefore they were dubbed Syncytins. Sequencing of more and more animal genomes allowed comparative genomic analyses that revealed how these envelopes have been domesticated in human, mouse, goat, rabbit, etc. More generally, we illustrate in this chapter how close are the viral and animal genome worlds and, focusing mainly on the hominoid ERVWE1 locus encoding Synctin-1, how the different proviruses encoding Syncytins have been domesticated to achieve placental functions. Influence of the chromosomal integration context, the epigenetic control and the splicing strategy upon transcription, and protein maturation processes as well will be discussed in order to illustrate what makes these nowadays genes different from their ancestral infectious counterpart. The price to pay for this beneficial invasion will be illustrated by the possible implications of Syncytin-1 in a wide range of diseases. Last, the apparent stringency of placental regulation will await to be challenged as regard to the evidence of expression in other physiological fusogenic contexts such as myoblasts and osteoclasts.

Keywords

  • Retrovirus
  • Endogenous retrovirus
  • Syncytins
  • Domestication

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Abbreviations

ALV:

Avian leukosis virus

BaEV:

Baboon endogenous virus

BLV:

Bovine leukemia virus

cyt:

Cytoplasmic tail

en:

Endogenous

EnCa:

Endometrial carcinoma

Env:

Envelope

ER:

Endoplasmic reticulum

ERV:

Endogenous retrovirus

Exo:

Exogenous

FcEV:

Felis catus endogenous retrovirus

FP:

Fusion peptide

GCM:

Glial cell missing

GPI:

Glycosylphosphatidylinositol

h:

Human

HELLP:

Hemolysis, elevated liver enzymes and low platelets

HERV:

Human endogenous retrovirus

HFV:

Human foamy virus

HIV:

Human immunodeficiency virus

HTLV:

Human T-cell leukemia virus

JSRV:

Jaagsiekte sheep retrovirus

KoRV:

Koala retrovirus

LTR:

Long terminal repeat

m:

Mouse

MALR:

Mammalian apparent LTR-retrotransposon

MAO:

Morpholino antisense oligonucleotide

MLV:

Murine leukemia virus

MMTV:

Mouse mammary tumor virus

MPMV:

Mason-Pfizer monkey virus

MS:

Multiple sclerosis

MSRV:

Multiple sclerosis associated retrovirus

NO:

Nitric oxide

OASIS:

Old astrocytes specifically induced substance

ORF:

Open reading frame

PBMC:

Peripheral blood mononuclear cell

PBS:

Primer binding site

PCR:

Polymerase chain reaction

PcRV:

Papio cynocephalus retrovirus

PE:

Preeclampsia

RBD:

Receptor-binding domain

RD114:

A feline endogenous retrovirus

RT:

Reverse transcriptase

SERV:

Simian endogenous retrovirus

SIV:

Simian immunodeficiency virus

SNV:

Spleen Necrosis virus

SP:

Signal peptide

SRV:

Simian retrovirus

SU:

Surface unit

TM:

Transmembrane unit

tm:

Transmembrane domain

URE:

Upstream regulatory element

WDS:

Walleye dermal sarcoma

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Acknowledgements

We thank Danièle Evain-Brion, Thierry Heidmann, Thomas E. Spencer, and François-Loïc Cosset for providing pictures and photographs. We are grateful to Laurent Duret for his support in bioinformatics, and we want to pay a tribute to Jean de La Fontaine for the contribution that his fable on the domestication ‘The Wolf and the Dog’ brought to our scientific reflection.

Dedicate On behalf of past and present members of the Mallet’s group, we would like to dedicate this chapter to the memory of our colleague and friend Olivier Bouton who substantially contributed to the human and scientific adventure that was the MSRV/HERV-W/ERVWE1 discovery.

Funding

Advanced Diagnostics for New Therapeutic Approaches (ADNA), a program dedicated to personalized Medicine, coordinated by Mérieux Alliance and supported by the French public agency, OSEO. PP and FM are employees of bioMérieux SA. PAB was supported by a grant from the Ministère français du Travail, de l’Emploi et de la Santé.

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Pérot, P., Bolze, PA., Mallet, F. (2012). From Viruses to Genes: Syncytins. In: Witzany, G. (eds) Viruses: Essential Agents of Life. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4899-6_17

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