General Physics and Astronomy; General Biochemistry, Genetics and Molecular Biology; General Chemistry; Multidisciplinary
Abstract :
[en] Five to ten percent of mammalian genomes is occupied by multiple clades of endogenous retroviruses (ERVs), that may count thousands of members. New ERV clades arise by retroviral infection of the germline followed by expansion by reinfection and/or retrotransposition. ERV mobilization is a source of deleterious variation, driving the emergence of ERV silencing mechanisms, leaving "DNA fossils". Here we show that the ERVK[2-1-LTR] clade is still active in the bovine and a source of disease-causing alleles. We develop a method to measure the rate of ERVK[2-1-LTR] mobilization, finding an average of 1 per ~150 sperm cells, with >10-fold difference between animals. We perform a genome-wide association study and identify eight loci affecting ERVK[2-1-LTR] mobilization. We provide evidence that polymorphic ERVK[2-1-LTR] elements in four of these loci cause the association. We generate a catalogue of full length ERVK[2-1-LTR] elements, and show that it comprises 15% of C-type autonomous elements, and 85% of D-type non-autonomous elements lacking functional genes. We show that >25% of the variance of mobilization rate is determined by the number of C-type elements, yet that de novo insertions are dominated by D-type elements. We propose that D-type elements act as parasite-of-parasite gene drives that may contribute to the observed demise of ERV elements.
Swedlund, Benjamin ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA) ; Keck School of Medicine, University of Southern California, Los Angeles, USA
Dupont, Sébastien ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA)
Harland, Chad ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA) > GIGA-R : Génomique animale ; Livestock Improvement Corporation, Hamilton, New Zealand
Costa Monteiro Moreira, Gabriel ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA)
Durkin, Keith ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Artesi, Maria ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Génétique humaine
Mullaart, Eric ; CRV, Arnhem, The Netherlands
Sartelet, Arnaud ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Médecine vétérinaire comparée
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
A.B. Osmanski et al. Insights into mammalian TE diversity via the curation of 248 mammalian genome assemblies Science 2023 380 eabn1430 1:CAS:528:DC%2BB3sXovFehtrw%3D 37104570
M. Dewannieux T. Heidmann Endogenous retroviruses: Acquisition, amplification and taming of genome invaders Curr. Opin. Virol. 2013 3 646 656 1:CAS:528:DC%2BC3sXhtlyisLbN 24004725
Mager, D. L. & Stoye, J. P. Mammalian endogenous retroviruses. In Mobile DNA III 1079–1100 (2015).
W.E. Johnson Origins and evolutionary consequences of ancient endogenous retroviruses Nat. Rev. Microbiol. 2019 17 355 370 1:CAS:528:DC%2BC1MXosF2ku7k%3D 30962577
E.S. Chiu S. Vandewoude Endogenous Retroviruses Drive Resistance and Promotion of Exogenous Retroviral Homologs Annu. Rev. Anim. Biosci. 2021 9 225 248 1:CAS:528:DC%2BB3cXisFSns7vK 33290087
D. Blanco-Melo R.J. Gifford P.D. Bieniasz Co-option of an endogenous retrovirus envelope for host defense in hominid ancestors Elife 2017 6 1 19
K. Lindblad-Toh et al. A high-resolution map of human evolutionary constraint using 29 mammals Nature 2011 478 476 482 1:CAS:528:DC%2BC3MXhtlSktbnM 21993624 3207357
J. Feusier et al. Pedigree-based estimation of human mobile element retrotransposition rates Genome Res. 2019 29 1567 1577 1:CAS:528:DC%2BC1MXisVags7zE 31575651 6771411
Y. Zhang I.A. Maksakova L. Gagnier L.N. Van De Lagemaat D.L. Mager Genome-wide assessments reveal extremely high levels of polymorphism of two active families of mouse endogenous retroviral elements PLoS Genet. 2008 4 e1000007 18454193 2265474
J.L. Elmer A.C. Ferguson-Smith Strain-specific epigenetic regulation of endogenous retroviruses: The role of Trans-acting modifiers Viruses 2020 12 1 21
S. Kipp et al. A new Holstein Haplotype affecting calf survival Interbull Bull. 2015 49 49 53
D. Becker et al. Allele-biased expression of the bovine APOB gene associated with the cholesterol deficiency defect suggests cis-regulatory enhancer effects of the LTR retrotransposon insertion Sci. Rep. 2022 12 1 14
F. Menzi et al. A transposable element insertion in APOB causes cholesterol deficiency in Holstein cattle Anim. Genet. 2016 47 253 257 1:CAS:528:DC%2BC28XktVOit7o%3D 26763170 4849205
E. Schütz et al. Correction: The Holstein Friesian Lethal Haplotype 5 (HH5) results from a complete deletion of TBF1M and Cholesterol Deficiency (CDH) from an ERV-(LTR) insertion into the coding region of APOB PLoS One 2016 11 1 15
W. Bao K.K. Kojima O. Kohany Repbase Update, a database of repetitive elements in eukaryotic genomes Mob. DNA 2015 6 26045719 4455052
D. Rosenkranz piRNA cluster database: A web resource for piRNA producing loci Nucleic Acids Res. 2016 44 D223 D230 1:CAS:528:DC%2BC2sXhtV2gu7vI 26582915
N. Zamudio D. Bourc’His Transposable elements in the mammalian germline: A comfortable niche or a deadly trap Heredity (Edinb.). 2010 105 92 104 1:CAS:528:DC%2BC3cXnsVOrtLk%3D 20442734
M. Artesi et al. PCIP-seq: simultaneous sequencing of integrated viral genomes and their insertion sites with long reads Genome Biol. 2021 22 1 24
P.D.W. Kirk M. Huvet A. Melamed G.N. Maertens C.R.M. Bangham Retroviruses integrate into a shared, non-palindromic DNA motif Nat. Microbiol. 2016 2 16212 1:CAS:528:DC%2BC2sXkvFyrtbc%3D 27841853 7613964
G.A. Van der Auwera et al. From FastQ Data to High-Confidence Variant Calls: The Genome Analysis Toolkit Best Practices Pipeline Curr. Protoc. Bioinforma. 2013 43 11.10.1 11.10.33
J. Ito R.J. Gifford K. Sato Retroviruses drive the rapid evolution of mammalian APOBEC3 genes Proc. Natl Acad. Sci. USA. 2020 117 610 618 2020PNAS.117.610I 1:CAS:528:DC%2BB3cXmtFOluw%3D%3D 31843890
H.G. Drost D.H. Sanchez A. Eyre-Walker Becoming a Selfish Clan: Recombination Associated to Reverse-Transcription in LTR Retrotransposons Genome Biol. Evol. 2019 11 3382 3392 1:CAS:528:DC%2BB3cXhvFels7zI 31755923 6894440
A.S. Van Laere W. Coppieters M. Georges Characterization of the bovine pseudoautosomal boundary: Documenting the evolutionary history of mammalian sex chromosomes Genome Res. 2008 18 1884 1895 18981267 2593575
A.D. Greenwood Y. Ishida S.P. O’Brien A.L. Roca M.V. Eiden Transmission, Evolution, and Endogenization: Lessons Learned from Recent Retroviral Invasions Microbiol. Mol. Biol. Rev. 2017 82 e00044 17 29237726 5813887
G. Bologna C. Yvon S. Duvaud A.L. Veuthey N-terminal myristoylation predictions by ensembles of neural networks Proteomics 2004 4 1626 1632 1:CAS:528:DC%2BD2cXkvFGitLs%3D 15174132
D. Ribet et al. An infectious progenitor for the murine IAP retrotransposon: Emergence of an intracellular genetic parasite from an ancient retrovirus Genome Res. 2008 18 597 609 1:CAS:528:DC%2BD1cXks1alsLg%3D 18256233 2279247
H. Cullen A.J. Schorn Endogenous Retroviruses Walk a Fine Line between Priming and Silencing Viruses 2020 12 792 1:CAS:528:DC%2BB3cXhslCgur7P 32718022 7472051
N. Bannert R. Kurth The evolutionary dynamics of human endogenous retroviral families Annu. Rev. Genomics Hum. Genet. 2006 7 149 173 1:CAS:528:DC%2BD28Xht1WgsrzF 16722807
M. Saitou H. Miyauchi Gametogenesis from Pluripotent Stem Cells Cell Stem Cell 2016 18 721 735 1:CAS:528:DC%2BC28XotF2rurs%3D 27257761
Harland, C. et al. Frequency of mosaicism points towards mutation-prone early cleavage cell divisions in cattle. bioRxiv 79863. https://doi.org/10.1101/079863 (2017).
A. Katzourakis A. Rambaut O.G. Pybus The evolutionary dynamics of endogenous retroviruses Trends Microbiol. 2005 13 463 468 1:CAS:528:DC%2BD2MXhtVWnsLrL 16109487
A. Onafuwa-Nuga A. Telesnitsky The Remarkable Frequency of Human Immunodeficiency Virus Type 1 Genetic Recombination Microbiol. Mol. Biol. Rev. 2009 73 451 480 1:CAS:528:DC%2BD1MXht1Ohu77J 19721086 2738136
D.L. Mager J.D. Freeman D. Novel Mouse Type Endogenous Proviruses and ETn Elements Share Long Terminal Repeat and Internal Sequences J. Virol. 2000 74 7221 7229 1:CAS:528:DC%2BD3cXlt1Gku7o%3D 10906176 112243
D. Ribet M. Dewannieux T. Heidmann An active murine transposon family pair: Retrotransposition of ‘master’ MusD copies and ETn trans-mobilization Genome Res. 2004 14 2261 2267 1:CAS:528:DC%2BD2cXpvVCitbY%3D 15479948 525684
E.S. Saito V.W. Keng J. Takeda K. Horie Translation from nonautonomous type IAP retrotransposon is a critical determinant of transposition activity: Implication for retrotransposon-mediated genome evolution Genome Res. 2008 18 859 868 1:CAS:528:DC%2BD1cXnsVygsLk%3D 18456863 2413153
M. Dewannieux A. Dupressoir F. Harper G. Pierron T. Heidmann Identification of autonomous IAP LTR retrotransposons mobile in mammalian cells Nat. Genet. 2004 36 534 539 1:CAS:528:DC%2BD2cXjsFSntL4%3D 15107856
U. Löber et al. Degradation and remobilization of endogenous retroviruses by recombination during the earliest stages of a germ-line invasion Proc. Natl Acad. Sci. 2018 115 8609 8614 2018PNAS.115.8609L 30082403 6112702
Tarlinton, R. E. et al. Differential and defective transcription of koala retrovirus indicates the complexity of host and virus evolution. J. Gen. Virol. 103, (2022).
J. Costas Evolutionary Dynamics of the Human Endogenous Retrovirus Family HERV-K Inferred from Full-Length Proviral Genomes J. Mol. Evol. 2001 53 237 243 2001JMolE.53.237C 1:CAS:528:DC%2BD3MXnt1Ghs7g%3D 11523010
S. Das et al. Next-generation genotype imputation service and methods Nat. Genet. 2016 48 1284 1287 1:CAS:528:DC%2BC28XhsVWksL%2FK 27571263 5157836
H. Li R. Durbin Fast and accurate short read alignment with Burrows-Wheeler transform Bioinformatics 2009 25 1754 1760 1:CAS:528:DC%2BD1MXot1Cjtbo%3D 19451168 2705234
X. Zhou M. Stephens Genome-wide efficient mixed-model analysis for association studies Nat. Genet. 2012 44 821 824 1:CAS:528:DC%2BC38Xos12gur0%3D 22706312 3386377
J.L. Gualdrón Duarte et al. Sequenced-based GWAS for linear classification traits in Belgian Blue beef cattle reveals new coding variants in genes regulating body size in mammals Genet. Sel. Evol. 2023 55 83 38017417 10683324
P. Danecek et al. Twelve years of SAMtools and BCFtools Gigascience 2021 10 1 4 1:CAS:528:DC%2BB3MXhsVaksLnM
H. Thorvaldsdóttir J.T. Robinson J.P. Mesirov Integrative Genomics Viewer (IGV): High-performance genomics data visualization and exploration Brief. Bioinform. 2013 14 178 192 22517427
L.S. Mamsen M.C. Lutterodt E.W. Andersen A.G. Byskov C.Y. Andersen Germ cell numbers in human embryonic and fetal gonads during the first two trimesters of pregnancy: Analysis of six published studies Hum. Reprod. 2011 26 2140 2145 21593044
Tang, L. GWAS reveals determinants of mobilization rate and dynamics of an active endogenous retrovirus of cattle. https://doi.org/10.5281/zenodo.10630335 (2024).
H. Li et al. The Sequence Alignment/Map format and SAMtools Bioinformatics 2009 25 2078 2079 19505943 2723002
L. Grobet et al. A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle Nat. Genet. 1997 17 71 74 1:CAS:528:DyaK2sXlvVGhtr8%3D 9288100
Similar publications
Sorry the service is unavailable at the moment. Please try again later.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.