DOI QR코드

DOI QR Code

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)
  • Received : 2017.07.24
  • Accepted : 2017.08.24
  • Published : 2017.10.31

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.

Acknowledgement

Supported by : ministry of Education

References

  1. 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. https://doi.org/10.1007/s13258-010-0114-6
  2. Ahn, K., Han, K., and Kim, H.S. (2011b). Quantitative analysis of the HERV pol gene in human tissues. Genes Genom. 33, 439-443. https://doi.org/10.1007/s13258-011-0005-5
  3. Ahn, K., and Kim, H.S. (2009). Structural and quantitative expression analyses of HERV gene family in human tissues. Mol. Cells 28, 99- 103. https://doi.org/10.1007/s10059-009-0107-y
  4. 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. https://doi.org/10.1006/viro.1997.8590
  5. 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. https://doi.org/10.1007/s00018-008-8495-2
  6. 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. https://doi.org/10.1038/ncomms1644
  7. 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. https://doi.org/10.1016/j.virol.2012.07.010
  8. Cho, G.J. (2007). Genetic relationship and characteristics using microsatellite. J. Life Sci. 17, 699-705. https://doi.org/10.5352/JLS.2007.17.5.699
  9. 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. https://doi.org/10.1016/j.gene.2005.09.003
  10. 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. https://doi.org/10.1038/nature03238
  11. 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. https://doi.org/10.1128/JVI.79.17.10890-10901.2005
  12. 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. https://doi.org/10.1016/j.virol.2012.08.047
  13. Gifford, R., and Tristem, M. (2003). The evolution, distribution and diversity of endogenous retroviruses. Virus Genes 26, 291-315. https://doi.org/10.1023/A:1024455415443
  14. 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. https://doi.org/10.1007/s00705-015-2486-z
  15. 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. https://doi.org/10.1371/journal.pone.0005767
  16. 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.
  17. 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. https://doi.org/10.1371/journal.pone.0008645
  18. 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. https://doi.org/10.1038/ng775
  19. Jern, P., and Coffin, J.M. (2008). Effects of retroviruses on host genome function. Annu. Rev. Genet. 42, 709-732. https://doi.org/10.1146/annurev.genet.42.110807.091501
  20. 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. https://doi.org/10.1093/nar/gkn201
  21. Johnson, W.E., and Coffin, J.M. (1999). Constructing primate phylogenies from ancient retrovirus sequences. Proc. Natl. Acad. Sci. USA 96, 10254-10260. https://doi.org/10.1073/pnas.96.18.10254
  22. 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. https://doi.org/10.1136/jclinpath-2013-201841
  23. 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. https://doi.org/10.1007/BF01731581
  24. 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. https://doi.org/10.1002/ana.23970
  25. 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. https://doi.org/10.1093/molbev/msn239
  26. 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. https://doi.org/10.1016/S0378-1119(00)00062-7
  27. 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. https://doi.org/10.1098/rstb.2012.0503
  28. Macfadden, B.J. (2005). Evolution. Fossil horses--evidence for evolution. Science 307, 1728-1730. https://doi.org/10.1126/science.1105458
  29. 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. https://doi.org/10.1016/j.placenta.2004.09.002
  30. Malfavon-Borja, R., and Feschotte, C. (2015). Fighting fire with fire: endogenous retrovirus envelopes as restriction factors. J. Virol. 89, 4047-4050. https://doi.org/10.1128/JVI.03653-14
  31. Martins, H., and Villesen, P. (2011). Improved integration time estimation of endogenous retroviruses with phylogenetic data. PLoS One 6, e14745. https://doi.org/10.1371/journal.pone.0014745
  32. 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. https://doi.org/10.1093/bib/bbs012
  33. 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. https://doi.org/10.1111/apm.12495
  34. 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. https://doi.org/10.1023/A:1011559200897
  35. 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. https://doi.org/10.1038/nature12323
  36. 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. https://doi.org/10.1186/1471-2164-13-473
  37. 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. https://doi.org/10.1016/j.biopsych.2008.06.028
  38. 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. https://doi.org/10.1177/1352458512441381
  39. 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. https://doi.org/10.1158/1078-0432.CCR-12-3580
  40. Ruprecht, K., Mayer, J., Sauter, M., Roemer, K., and Mueller-Lantzsch, N. (2008). Endogenous retroviruses and cancer. Cell. Mol. Life Sci. 65, 3366-3382. https://doi.org/10.1007/s00018-008-8496-1
  41. 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.
  42. 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.
  43. 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. https://doi.org/10.1128/JVI.74.8.3715-3730.2000
  44. 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. https://doi.org/10.3390/v3060620
  45. Yi, J.M., and Kim, H.S. (2006). Molecular evolution of the HERV-E family in primates. Arch. Virol. 151, 1107-1116. https://doi.org/10.1007/s00705-005-0701-z
  46. 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. https://doi.org/10.1016/j.gene.2004.08.007
  47. 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. https://doi.org/10.1016/j.ygeno.2006.08.010