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Identification and Characterization of Novel Human Endogenous Retrovirus Families by Phylogenetic Screening of the Human Genome Mapping Project Database
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Human endogenous retroviruses (HERVs) were first identified almost 20 years ago, and since then numerous families have been described. It has, however, been difficult to obtain a good estimate of both the total number of independently derived families and their relationship to each other as well as to other members of the family Retroviridae . In this study, I used sequence data derived from over 150 novel HERVs, obtained from the Human Genome Mapping Project database, and a variety of recently identified nonhuman retroviruses to classify the HERVs into 22 independently acquired families. Of these, 17 families were loosely assigned to the class I HERVs, 3 to the class II HERVs and 2 to the class III HERVs. Many of these families have been identified previously, but six are described here for the first time and another four, for which only partial sequence information was previously available, were further characterized. Members of each of the 10 families are defective, and calculation of their integration dates suggested that most of them are likely to have been present within the human lineage since it diverged from the Old World monkeys more than 25 million years ago.
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“In the case of endogenous retroviruses (embedded in the genome of their host), dates of origin can be estimated without a calibration date by comparing the two long terminal repeats (LTRs) that flank the viral genome - a method that has helped uncover the history of viral DNA in the human genome 60,61 .”
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BackgroundA Human Genome Structural Variation Sequencing Resource Reveals Insights into Mutational Mechanisms
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Mammalian Endogenous Retroviruses
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BackgroundERVmap analysis reveals genome-wide transcription of human endogenous retroviruses
Tokuyama, M., Kong, Y., Song, E., Jayewickreme, T., Kang, I., & Iwasaki, A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1814589115 · Cited by 202
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Nelson, P. N., Carnegie, P., Martin, J., Ejtehadi, H. D., Hooley, P., Roden, D., Rowland-Jones, S., Warren, P., Astley, J., & Murray, P. G. (2003) · Molecular Pathology · doi:10.1136/mp.56.1.11 · Cited by 210
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Villesen, P., Aagaard, L., Wiuf, C., & Pedersen, F. (2004) · Retrovirology · doi:10.1186/1742-4690-1-32 · Cited by 37
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MethodInfluentialEndogenous viruses: Connecting recent and ancient viral evolution
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“However, it is inconsistent for many other ERV groups that have alternative PBSes [18] e.g. HERV-H/F [17], ERV3 [16], and ERV9/HERV-W [19].”
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Wang‐Johanning, F., Frost, A. R., Johanning, G. L., Khazaeli, M. B., LoBuglio, A. F., Shaw, D. R., & Strong, T. V. (2001) · PubMed · Cited by 174
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“In a similar study, it has been reported that most human endogenous retroviruses (HERVs) inserted into the human genome long before humans diverged from the Old World monkeys, more than 25 million years ago (Tristem 2000).”
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Self-citationHuman RNA “Rumor” Viruses: the Search for Novel Human Retroviruses in Chronic Disease
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Long terminal repeat retrotransposons of Oryza sativa
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BackgroundRate of Recombinational Deletion among Human Endogenous Retroviruses
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“HERVs are divided into a relatively small number of lineages (or families), each of which is considered to represent the proliferation of an initial independent infection of the ancestor of the human genome up to 70 million years ago (mya) (36).”
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Magiorkinis, G., Gifford, R. J., Katzourakis, A., Ranter, J. D., & Belshaw, R. D. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200913109 · Cited by 137
“These loci form phylogenetically distinct lineages traditionally called “families” (4) (unrelated to the general use of this term in taxonomy), each of which is the result of the expansion of a founder infection of the organism’s germline that can have occurred more than ∼100 million years ago (5).”
BackgroundEndogenous retroviruses and the human germline
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Evolutionary Genomics of Chromoviruses in Eukaryotes
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Endogenous Retroviruses in the Genomics Era
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Activation of human endogenous retroviruses and its physiological consequences
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BackgroundKAP1 regulates endogenous retroviruses in adult human cells and contributes to innate immune control
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The Opitz Syndrome Gene Mid1 Is Transcribed from a Human Endogenous Retroviral Promoter
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“…RefSeq database (RRID: SCR_003496) (Pruitt et al., 2014), and ERV sequences were based either on consensus sequences of previously published ERV sequence data (Bénit et al., 2001; Sverdlov, 2005; Tristem, 2000; Villesen et al., 2004), or previously inferred consensus sequences (Jern et al., 2005).”
MethodImplication of Human Endogenous Retroviruses in the Development of Autoimmune Diseases
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“The analysis of human gene loci, plus information from the human genome project have also helped to detect HERV sequences [19, 20].”
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“The fulllength structure is present in approximately 35–50 copies per human haploid genome.(3) The nucleotide sequence of HERV-E 4-1 reveals a 449 base pair (bp) 3 LTR and a 495-bp 5 LTR, and the genomic DNA is organized into gag, pol, and env genes interspersed between the 2 LTRs.”
BackgroundYohn, C. T., Jiang, Z., McGrath, S. D., Hayden, K. E., Khaitovich, P., Johnson, M. E., Eichler, M. Y., McPherson, J. D., Zhao, S., Pääbo, S., et al. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030110 · Cited by 104
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Multiple sclerosis–associated retrovirus (MSRV) in Sardinian MS patients
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“Thirty-five patients with OND were diagnosed as having infectious and postinfectious encephalomyelitis (4), immune-mediated peripheral neuropathy (3), epilepsy (5), neurosis (4), ischemic stroke (3), compressive radiculomyelopathy (3), migraine (3), trigeminal neuralgia (2), myasthenia gravis (2), CNS vasculitis (1),…”
BackgroundHuman endogenous retroviruses and cancer
María, G.-C., Paola, I., Niki, K., Mariacarmela, S., Julià, B., & Rafael, R. (2016) · Cancer Biology & Medicine · doi:10.20892/j.issn.2095-3941.2016.0080 · Cited by 100
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Molecular functions of human endogenous retroviruses in health and disease
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“HERV-K/HML-2 (ERVK) is the sole group of HERVs known to contain human specific members, totally *140 such elements found in previous works [1, 21, 24, 38, 47, 81–86], that contributed *330 kb of the human DNA [87].”
Intrinsic immunity against retrotransposons by APOBEC cytidine deaminases
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“…although none of the HERVs are replication-competent due to their accumulation of mutations (deletions, termination, and frame shifts), more than 20 independent HERV families, which include proviruses that belong to beta-, gamma-, and spuma-retrovirus families, have been identified (Tristem, 2000).”
BackgroundThe evolutionary dynamics of endogenous retroviruses
Katzourakis, A., Rambaut, A., & Pybus, O. G. (2005) · Trends in Microbiology · doi:10.1016/j.tim.2005.08.004 · Cited by 92
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Allelic Variation of HERV-K(HML-2) Endogenous Retroviral Elements in Human Populations
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“Several distinct human ERV families (HERVs) have been identified, which show different genomic integration patterns (Urnovitz and Murphy 1996) and range in copy number from 1 to 1000 (Tristem 2000).”
BackgroundCharacterization of the Intragenomic Spread of the Human Endogenous Retrovirus Family HERV-W
Costas, J. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004108 · Cited by 89
Evolution and Distribution of Class II-Related Endogenous Retroviruses
Gifford, R. J., Kabát, P., Martin, J. L., Lynch, C., & Tristem, M. (2005) · Journal of Virology · doi:10.1128/jvi.79.10.6478-6486.2005 · Cited by 88
“This is in contrast to previous reports, which have generally placed the lentiviruses toward the base of the class II virus phylogeny, as paraphyletic sister taxa to the exogenous deltaretroviruses (5, 11, 16, 18, 33, 37).”
BackgroundResultInfluentialSelf-citationStrissel, P. L., Ruebner, M., Thiel, F. C., Wachter, D. L., Ekici, A. B., Wolf, F., Thieme, F., Ruprecht, K., Beckmann, M. W., & Strick, R. (2012) · Oncotarget · doi:10.18632/oncotarget.679 · Cited by 88
“To date 31 distinct groups and over 100 different ERV families have been found integrated throughout the human chromosomes and represent different copy numbers [13, 14].”
Lukic, S., Nicolas, J.-C., & Levine, A. J. (2013) · Cell Death and Differentiation · doi:10.1038/cdd.2013.150 · Cited by 89
“previous studies.(15,16) In addition, by comparing the binding affinities of tandems of homologous zinc-fingers across the”
BackgroundEndogenous retroviruses and animal reproduction
Prudhomme, S., Bonnaud, B., & Mallet, F. (2005) · Cytogenetic and Genome Research · doi:10.1159/000084967 · Cited by 85
“Twenty six families are characterized in terms of phylogeny (Tristem, 2000; Benit et al., 2001) but fewer are studied in detail.”
BackgroundDigital expression profiles of human endogenous retroviral families in normal and cancerous tissues.
Stauffer, Y., Theiler, G., Sperisen, P., Lebedev, Y. B., & Jongeneel, C. V. (2004) · PubMed · Cited by 85
Variable Transcriptional Activity of Endogenous Retroviruses in Human Breast Cancer
Frank, O., Verbeke, C. S., Schwarz, N., Mayer, J. M., Fabarius, A. C., Hehlmann, R., Leib‐Mösch, C., & Seifarth, W. (2007) · Journal of Virology · doi:10.1128/jvi.02115-07 · Cited by 86
“Moreover, the presence of endogenous MMTV-related sequences in the human genome (1, 4, 36, 37, 46, 47) and their ubiquitous transcriptional activities in normal human tissues, including mammary gland tissue (31, 33, 42, 54), has complicated a systematic investigation.”
BackgroundChen, J., Foroozesh, M. K., & Qin, Z. (2019) · Oncogenesis · doi:10.1038/s41389-018-0114-y · Cited by 79
Ishida, T., Obata, Y., Ohara, N., Matsushita, H., Sato, S., Uenaka, A., Saika, T., Miyamura, T., Chayama, K., Nakamura, Y., et al. (2008) · PubMed Central · Cited by 77
Endogenous Retroviruses: With Us and against Us
Meyer, T. J., Rosenkrantz, J. L., Carbone, L., & Chavez, S. L. (2017) · Frontiers in Chemistry · doi:10.3389/fchem.2017.00023 · Cited by 81
“Given that some ERV families have expanded substantially in the number of genomic integrations in animals (Tristem, 2000; Bénit et al., 2001), it has been hypothesized that widespread reactivation of ERVs during the waves of global reprogramming within germ cell and pre-implantation development are…”
BackgroundAre human endogenous retroviruses pathogenic? An approach to testing the hypothesis
Young, G. R., Stoye, J. P., & Kassiotis, G. (2013) · BioEssays · doi:10.1002/bies.201300049 · Cited by 78
“Around 30 such groups have been described based on a phylogenetic analysis of pol sequences; they vary in copy number from one to a few thousand [10], specific proviruses showing unique flanking sequences depending on their integration site.”
BackgroundDevelopmental expression of HERV-R (ERV3) and HERV-K in human tissue.
Andersson, A., Venables, P., Tonjes, R., Scherer, J., Eriksson, L., & Larsson, E. (2002) · Virology · doi:10.1006/viro.2002.1428 · Cited by 89
“About 5% of the human genome, like DNA of other species, contains retroviral and related sequences (Prak and Kazazian, 2000; Tristem, 2000).”
BackgroundEmergence of vertebrate retroviruses and envelope capture
Kim, F. J., Battini, J., Manel, N., & Sitbon, M. (2003) · Virology · doi:10.1016/j.virol.2003.09.026 · Cited by 77
Human endogenous retroviruses and cancer prevention: evidence and prospects
Cegolon, L., Salata, C., Weiderpass, E., Vineis, P., Palù, G., & Mastrangelo, G. (2013) · BMC Cancer · doi:10.1186/1471-2407-13-4 · Cited by 77
“HERVs are classified in more than 22 different families [15,41-44] depending on their sequence identity and partly on the similarity of their primer binding sites to host tRNAs [15,44,45].”
BackgroundPushing the endogenous envelope
Henzy, J. E., & Johnson, W. E. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0506 · Cited by 83
“Phylogenetic trees combining RT sequences from both endogenous and exogenous retroviruses suggest that all known retroviruses can be grouped into three broad classes [4, 15] : class I consists of gammaretroviruses, epsilonretroviruses and the ERVs that cluster along with them.”
BackgroundMaking a virtue of necessity: the pleiotropic role of human endogenous retroviruses in cancer
Kassiotis, G., & Stoye, J. P. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0277 · Cited by 78
Association of Endogenous Retroviruses and Long Terminal Repeats with Human Disorders
Katoh, I., & Kurata, S. (2013) · Frontiers in Oncology · doi:10.3389/fonc.2013.00234 · Cited by 77
Weis, S., Llenos, I. C., Sabunciyan, S., Dulay, J. R., Isler, L., Yolken, R. H., & Perron, H. (2007) · Journal of Neural Transmission · doi:10.1007/s00702-006-0599-y · Cited by 76
Human endogenous retroviruses in the primate lineage and their influence on host genomes
Mayer, J. M., & Meese, E. U. (2005) · Cytogenetic and Genome Research · doi:10.1159/000084977 · Cited by 72
“Often, HERV families are designated according to the tRNA formerly used to prime reverse transcription of retroviral RNA by binding to the primer binding site (PBS), with the tRNA’s corresponding amino acid single letter code appended to HERV.”
BackgroundInfluentialLavie, L., Medstrand, P., Schempp, W., Meese, E. U., & Mayer, J. M. (2004) · Journal of Virology · doi:10.1128/jvi.78.16.8788-8798.2004 · Cited by 72
“…of the human genome sequence, Tristem suggested that the HERV-K(HML-5) primer binding site region is more similar to iso-leucine than to lysine (43) We analyzed the HERV-K(HML-5) consensus primer binding site region in regard to the similarity to reported human tRNA sequences (22) (http:…”
Mager, D. L., & Medstrand, P. (2005) · Encyclopedia of Life Sciences · doi:10.1038/npg.els.0005062 · Cited by 73
Sicat, J., Sutkowski, N., & Huber, B. T. (2005) · PubMed · Cited by 72
Microbiome, holobiont and the net of life
Salvucci, E. (2014) · Critical Reviews in Microbiology · doi:10.3109/1040841x.2014.962478 · Cited by 75
“Virus gene rearrangements participate and underlie the process of generation of new structures, metabolic ways and gene regulation that result in evolutionary changes (Casjens, 2003; Feschotte & Gilbert, 2012; Johnson, 2008; Johnson & Coffin, 1999; Tristem, 2000).”
BackgroundTissue specificity of enhancer and promoter activities of a HERV-K(HML-2) LTR
Ruda, V. M., Акопов, С. Б., Trubetskoy, D. O., Manuylov, N. L., Vetchinova, A. S., Zavalova, L. L., Николаев, Л. Г., & Sverdlov, E. D. (2004) · Virus Research · doi:10.1016/j.virusres.2004.02.036 · Cited by 72
Tokuyama, M., Gunn, B. M., Venkataraman, A., Kong, Y., Kang, I., Rakib, T., Townsend, M. J., Costenbader, K. H., Alter, G., & Iwasaki, A. (2021) · The Journal of Experimental Medicine · doi:10.1084/jem.20191766 · Cited by 73
“A minority of ERVs represented by a few thousand copies have a relatively intact proviral structure, composed of some or all of the original open reading frames (Tristem, 2000; Subramanian et al., 2011; Schmitt et al., 2013a, 2013b; Vargiu et al., 2016).”
BackgroundEndogenous retroviral pathogenesis in lupus
Perl, A., Fernandez, D., Telarico, T., & Phillips, P. E. (2010) · Current Opinion in Rheumatology · doi:10.1097/bor.0b013e32833c6297 · Cited by 75
Magiorkinis, G., Belshaw, R. D., & Katzourakis, A. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0504 · Cited by 69
“These families generally represent a single invasion followed by a copy-number expansion within the host’s genome [8].”
Definition and variation of human endogenous retrovirus H
Jern, P., Sperber, G., & Blomberg, J. (2004) · Virology · doi:10.1016/j.virol.2004.06.023 · Cited by 66
Nexø, B. A., Christensen, T., Frederiksen, J., Møller-Larsen, A., Oturai, A. B., Villesen, P., Hansen, B., Nissen, K. K., Laska, M. J., Petersen, T. S., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016652 · Cited by 83
“genes have shown that HERV-Fc is closely related to HERV-H, more distantly related to HERV-W and only remotely related to HERV-K”
Background
Metadata
- Authors
- Tristem, M.
- Affiliations
- Imperial College London (GB)
- Corresponding author
- Tristem, Michael
- ORCID
- Tristem, Michael
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 2000-04-15
- Volume
- 74
- Issue
- 8
- Pages
- 3715-3730
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC111881
- OpenAlex
- W2082918825
- Cited by
- 330
- References
- 64
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 9 · 2023: 7 · 2022: 5 · 2021: 12 · 2020: 6 · 2019: 11 · 2018: 8 · 2017: 13 · 2016: 11 · 2015: 15 · 2014: 12 · 2013: 18 · 2012: 16
- FWCI
- 34.65
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Virology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Royal Society
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Health Sciences › Medicine › Infectious Diseases › Infectious Diseases and Mycology
- Keywords
- human endogenous retroviruses, phylogenetic analysis, human evolution, Old World monkeys, retroviral evolution
- MeSH terms
- Amino Acid Sequence, Animals, Base Sequence, Chromosome Mapping, Humans, Molecular Sequence Data, Terminology as Topic, Phylogeny, Human Genome Project, Databases, Factual, Sequence Alignment, Sequence Analysis, DNA, Endogenous Retroviruses
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