Browse > Article
http://dx.doi.org/10.14348/molcells.2017.0141

Identification and Expression Analyses of Equine Endogenous Retroviruses in Horses  

Gim, Jeong-An (Department of Biological Sciences, College of Natural Sciences, Pusan National University)
Kim, Heui-Soo (Department of Biological Sciences, College of Natural Sciences, Pusan National University)
Abstract
Endogenous retroviruses (ERVs) have been integrated into vertebrate genomes and have momentously affected host organisms. Horses (Equus caballus) have been domesticated and selected for elite racing ability over centuries. ERVs played an important role in the evolutionary diversification of the horse genome. In the present study, we identified six equine ERV families (EqERVs-E1, I1, M2, P1, S1, and Y4), their full-length viral open reading frames (ORFs), and elucidated their phylogenetic relationships. The divergence time of EqERV families assuming an evolutionary rate of 0.2%/Myr indicated that EqERV-S3 (75.4 million years ago; mya) on chromosome 10 is an old EqERV family and EqERV-P5 (1.2 Mya) on chromosome 12 is a young member. During the evolutionary diversification of horses, the EqERV-I family diverged 1.7 Mya to 38.7 Mya. Reverse transcription quantitative real-time PCR (RT-qPCR) amplification of EqERV pol genes showed greater expression in the cerebellum of the Jeju horse than the Thoroughbred horse. These results could contribute further dynamic studies for horse genome in relation to EqERV gene function.
Keywords
EqERV; Jeju horse; pol gene; quantitative real-time RT-PCR; thoroughbred horse;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
연도 인용수 순위
1 Kang, Y.J., Jo, J.O., Ock, M.S., Chang, H.K., Baek, K.W., Lee, J.R., Choi, Y.H., Kim, W.J., Leem, S.H., Kim, H.S., et al. (2014). Human ERV3-1 env protein expression in various human tissues and tumours. J. Clin. Pathol. 67, 86-90.   DOI
2 Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111-120.   DOI
3 Kremer, D., Schichel, T., Förster, M., Tzekova, N., Bernard, C., Valk, P., Horssen, J., Hartung, H.P., Perron, H., and Kury, P. (2013). Human endogenous retrovirus type W envelope protein inhibits oligodendroglial precursor cell differentiation. Ann. Neurol. 74, 721- 732.   DOI
4 Lau, A.N., Peng, L., Goto, H., Chemnick, L., Ryder, O.A., and Makova, K.D. (2009). Horse domestication and conservation genetics of Przewalski's horse inferred from sex chromosomal and autosomal sequences. Mol. Biol. Evol. 26, 199-208.   DOI
5 Lebedev, Y.B., Belonovitch, O.S., Zybrova, N.V., Khil, P.P., Kurdyukov, S.G., Vinogradova, T.V., Hunsmann, G., and Sverdlov, E.D. (2000). Differences in HERV-K LTR insertions in orthologous loci of humans and great apes. Gene 247, 265-277.   DOI
6 Lee, A., Nolan, A., Watson, J., and Tristem, M. (2013). Identification of an ancient endogenous retrovirus, predating the divergence of the placental mammals. Phil. Trans. R. Soc. B 368, 20120503.   DOI
7 Macfadden, B.J. (2005). Evolution. Fossil horses--evidence for evolution. Science 307, 1728-1730.   DOI
8 Malassine, A., Handschuh, K., Tsatsaris, V., Gerbaud, P., Cheynet, V., Oriol, G., Mallet, F., and Evain-Brion, D. (2005). Expression of HERVW Env glycoprotein (syncytin) in the extravillous trophoblast of first trimester human placenta. Placenta 26, 556-562.   DOI
9 Malfavon-Borja, R., and Feschotte, C. (2015). Fighting fire with fire: endogenous retrovirus envelopes as restriction factors. J. Virol. 89, 4047-4050.   DOI
10 Ahn, K., Bae, J.-H., Nam, K.-H., Lee, C.-E., Park, K.-D., Lee, H.-K., Cho, B.-W., and Kim, H.-S. (2011a). Identification of reference genes for normalization of gene expression in thoroughbred and Jeju native horse (Jeju pony) tissues. Genes Genom. 33, 245-250.   DOI
11 Ahn, K., Han, K., and Kim, H.S. (2011b). Quantitative analysis of the HERV pol gene in human tissues. Genes Genom. 33, 439-443.   DOI
12 Park, K.D., Park, J., Ko, J., Kim, B.C., Kim, H.S., Ahn, K., Do, K.T., Choi, H., Kim, H.M., Song, S., et al. (2012). Whole transcriptome analyses of six thoroughbred horses before and after exercise using RNA-Seq. BMC Genomics 13, 473.   DOI
13 Martins, H., and Villesen, P. (2011). Improved integration time estimation of endogenous retroviruses with phylogenetic data. PLoS One 6, e14745.   DOI
14 Milne, I., Stephen, G., Bayer, M., Cock, P.J., Pritchard, L., Cardle, L., Shaw, P.D., and Marshall, D. (2013). Using Tablet for visual exploration of second-generation sequencing data. Brief. Bioniform. 14, 193-202.   DOI
15 Mortelmans, K., Wang‐Johanning, F., and Johanning, G.L. (2016). The role of human endogenous retroviruses in brain development and function. Apmis 124, 105-115.   DOI
16 Oakenfull, E.A., Lim, H.N., and Ryder, O.A. (2000). A survey of equid mitochondrial DNA: Implications for the evolution, genetic diversity and conservation of Equus. Conserv. Genet. 1, 341-355.   DOI
17 Orlando, L., Ginolhac, A., Zhang, G., Froese, D., Albrechtsen, A., Stiller, M., Schubert, M., Cappellini, E., Petersen, B., Moltke, I., et al. (2013). Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 499, 74-78.   DOI
18 Perron, H., Mekaoui, L., Bernard, C., Veas, F., Stefas, I., and Leboyer, M. (2008). Endogenous retrovirus type W GAG and envelope protein antigenemia in serum of schizophrenic patients. Biol. Psychiatry 64, 1019-1023.   DOI
19 Perron, H., Germi, R., Bernard, C., Garcia-Montojo, M., Deluen, C., Farinelli, L., Faucard, R., Veas, F., Stefas, I., and Fabriek, B.O. (2012). Human endogenous retrovirus type W envelope expression in blood and brain cells provides new insights into multiple sclerosis disease. Mult. Scler. J. 18, 1721-1736.   DOI
20 Ahn, K., and Kim, H.S. (2009). Structural and quantitative expression analyses of HERV gene family in human tissues. Mol. Cells 28, 99- 103.   DOI
21 Brown, K., Moreton, J., Malla, S., Aboobaker, A.A., Emes, R.D., and Tarlinton, R.E. (2012). Characterisation of retroviruses in the horse genome and their transcriptional activity via transcriptome sequencing. Virology 433, 55-63.   DOI
22 Anderssen, S., Sjottem, E., Svineng, G., and Johansen, T. (1997). Comparative analyses of LTRs of the ERV-H family of primate-specific retrovirus-like elements isolated from marmoset, African green monkey, and man. Virology 234, 14-30.   DOI
23 Blikstad, V., Benachenhou, F., Sperber, G.O., and Blomberg, J. (2008). Evolution of human endogenous retroviral sequences: a conceptual account. Cell. Mol. Life Sci. 65, 3348-3365.   DOI
24 Bower, M.A., McGivney, B.A., Campana, M.G., Gu, J., Andersson, L.S., Barrett, E., Davis, C.R., Mikko, S., Stock, F., Voronkova, V., et al. (2012). The genetic origin and history of speed in the Thoroughbred racehorse. Nat. Commun. 3, 643.   DOI
25 Cho, G.J. (2007). Genetic relationship and characteristics using microsatellite. J. Life Sci. 17, 699-705.   DOI
26 Dunn, C.A., Romanish, M.T., Gutierrez, L.E., van de Lagemaat, L.N., and Mager, D.L. (2006). Transcription of two human genes from a bidirectional endogenous retrovirus promoter. Gene 366, 335-342.   DOI
27 Esnault, C., Heidmann, O., Delebecque, F., Dewannieux, M., Ribet, D., Hance, A.J., Heidmann, T., and Schwartz, O. (2005). APOBEC3G cytidine deaminase inhibits retrotransposition of endogenous retroviruses. Nature 433, 430-433.   DOI
28 Frank, O., Giehl, M., Zheng, C., Hehlmann, R., Leib-Mosch, C., and Seifarth, W. (2005). Human endogenous retrovirus expression profiles in samples from brains of patients with schizophrenia and bipolar disorders. J. Virol. 79, 10890-10901.   DOI
29 Ruprecht, K., Mayer, J., Sauter, M., Roemer, K., and Mueller-Lantzsch, N. (2008). Endogenous retroviruses and cancer. Cell. Mol. Life Sci. 65, 3366-3382.   DOI
30 Reis, B.S., Jungbluth, A.A., Frosina, D., Holz, M., Ritter, E., Nakayama, E., Ishida, T., Obata, Y., Carver, B., Scher, H., et al. (2013). Prostate cancer progression correlates with increased humoral immune response to a human endogenous retrovirus GAG protein. Clin. Cancer Res. 19, 6112-6125.   DOI
31 Shin, J.A., Yang, Y.H., Kim, H.S., Yun, Y.M., and Lee, K.K. (2002). Genetic polymorphism of the serum proteins of horses in Jeju. J. Vet. Sci. 3, 255-263.
32 Sperber, G., Lovgren, A., Eriksson, N.E., Benachenhou, F., and Blomberg, J. (2009). RetroTector online, a rational tool for analysis of retroviral elements in small and medium size vertebrate genomic sequences. BMC Bioinformatics 10 Suppl 6, S4.
33 Tristem, M. (2000). Identification and characterization of novel human endogenous retrovirus families by phylogenetic screening of the human genome mapping project database. J. Virol. 74, 3715- 3730.   DOI
34 van der Kuyl, A.C. (2011). Characterization of a full-length endogenous beta-retrovirus, EqERV-beta1, in the genome of the horse (Equus caballus). Viruses 3, 620-628.   DOI
35 Yi, J.M., and Kim, H.S. (2006). Molecular evolution of the HERV-E family in primates. Arch. Virol. 151, 1107-1116.   DOI
36 Yi, J.M., Kim, T.H., Huh, J.W., Park, K.S., Jang, S.B., Kim, H.M., and Kim, H.S. (2004). Human endogenous retroviral elements belonging to the HERV-S family from human tissues, cancer cells, and primates: expression, structure, phylogeny and evolution. Gene 342, 283-292.   DOI
37 Gim, J.-A., Han, K., and Kim, H.-S. (2015). Identification and expression analysis of human endogenous retrovirus Y (HERV-Y) in various human tissues. Arch. Virol. 160, 2161-2168.   DOI
38 Yi, J.M., Schuebel, K., and Kim, H.S. (2007). Molecular genetic analyses of human endogenous retroviral elements belonging to the HERV-P family in primates, human tissues, and cancer cells. Genomics 89, 1-9.   DOI
39 Garcia-Etxebarria, K., and Jugo, B.M. (2012). Detection and characterization of endogenous retroviruses in the horse genome by in silico analysis. Virology 434, 59-67.   DOI
40 Gifford, R., and Tristem, M. (2003). The evolution, distribution and diversity of endogenous retroviruses. Virus Genes 26, 291-315.   DOI
41 Gu, J., Orr, N., Park, S.D., Katz, L.M., Sulimova, G., MacHugh, D.E., and Hill, E.W. (2009). A genome scan for positive selection in thoroughbred horses. PLoS One 4, e5767.   DOI
42 Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT; in Nucleic Acids Symp. Ser. Vol. 41, pp. 95-98.
43 Hill, E.W., Gu, J., Eivers, S.S., Fonseca, R.G., McGivney, B.A., Govindarajan, P., Orr, N., Katz, L.M., and MacHugh, D.E. (2010). A sequence polymorphism in MSTN predicts sprinting ability and racing stamina in thoroughbred horses. PLoS One 5, e8645.   DOI
44 Hughes, J.F., and Coffin, J.M. (2001). Evidence for genomic rearrangements mediated by human endogenous retroviruses during primate evolution. Nat. Genet. 29, 487-489.   DOI
45 Jern, P., and Coffin, J.M. (2008). Effects of retroviruses on host genome function. Annu. Rev. Genet. 42, 709-732.   DOI
46 Johnson, M., Zaretskaya, I., Raytselis, Y., Merezhuk, Y., McGinnis, S., and Madden, T.L. (2008). NCBI BLAST: a better web interface. Nucleic Acids Res. 36, W5-W9.   DOI
47 Johnson, W.E., and Coffin, J.M. (1999). Constructing primate phylogenies from ancient retrovirus sequences. Proc. Natl. Acad. Sci. USA 96, 10254-10260.   DOI