Is there a role for endogenous retroviruses to mediate long-term adaptive phenotypic response upon environmental inputs?

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1609, 2013, Pages

  Sharif, Jafar ^a   Shinkai, Yoichi ^b   Koseki, Haruhiko ^a  

^a Institute of Physical and Chemical Research   (Japan)

^b RIKEN   (Japan)

Author keywords

Adaptive response; DNA methylation; Environmental cues; Intracisternal A particles; Retrotransposons

Indexed keywords

ADAPTATION; BIOLOGICAL DEVELOPMENT; DNA; EMBRYONIC DEVELOPMENT; ENVIRONMENTAL CUE; ENVIRONMENTAL EFFECT; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; GENOME; GENOMICS; METHYLATION; PHENOTYPE; PHENOTYPIC PLASTICITY; PROTEIN; RNA; RODENT; VIRUS;

HISTONE;

ADAPTATION; ANIMAL; DNA METHYLATION; EMBRYO DEVELOPMENT; ENDOGENOUS RETROVIRUS; ENVIRONMENT; FEMALE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; GENOME; METABOLISM; MOUSE; ONCOGENE; PHENOTYPE; PLACENTA; PREGNANCY; PRENATAL DEVELOPMENT; REVIEW;

ADAPTATION, BIOLOGICAL; ANIMALS; DNA METHYLATION; EMBRYONIC DEVELOPMENT; ENDOGENOUS RETROVIRUSES; ENVIRONMENT; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INTRACISTERNAL A-PARTICLE; GENOME; HISTONES; MICE; PHENOTYPE; PLACENTA; PREGNANCY; TRANSCRIPTION, GENETIC;

EID: 84876558534     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0340     Document Type: Review

References (82)

1. Lander ES. et al. 2001 Initial sequencing and analysis of the human genome. Nature 409, 860-921. (doi:10.1038/35057062)
2. McClintock B. 1950 The origin and behavior of mutable loci in maize. Proc. Natl Acad. Sci. USA 36, 344-355. (doi:10.1073/pnas.36.6.344)
3. Wicker T. et al. 2007 A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8, 973-982. (doi:10.1038/nrg2165)
4. Martin SL. 2006 The ORF1 protein encoded by LINE-1: structure and function during L1 retrotransposition. J. Biomed. Biotechnol. 2006, 45621. (doi:10.1155/JBB/2006/45621)
5. Stocking C, Kozak CA. 2008 Murine endogenous retroviruses. Cell Mol. Life Sci. 65, 3383-3398. (doi:10.1007/s00018-008-8497-0)
6. Ryan PF. 2004 Human endogenous retroviruses in health and disease: a symbiotic perspective. J. R. Soc. Med. 97, 560-565. (doi:10.1258/jrsm.98. 3.134-a)
7. Zhang Y, Maksakova IA, Gagnier L, van de Lagemaat LN, Mager DL. 2008 Genome-wide assessments reveal extremely high levels of polymorphism of two active families of mouse endogenous retroviral elements. PLoS Genet. 4, e1000007. (doi:10.1371/journal.pgen)
8. Maksakova IA, Mager DL, Reiss D. 2008 Keeping active endogenous retroviral-like elements in check: the epigenetic perspective. Cell Mol. Life Sci. 65, 3329-3347. (doi:10.1007/s00018-008-8494-3)
9. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. 1999 Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet. 23, 314-318. (doi:10.1038/15490)
10. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KV, Whitelaw E. 2003 Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc. Natl Acad. Sci. USA 100, 2538-2543. (doi:10.1073/pnas.0436776100)
11. Wolff GL, Kodell RL, Moore SR, Cooney CA. 1998 Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J. 12, 949-957.
12. Cropley JE, Suter CM, Beckman KB, Martin DI. 2006 Germ-line epigenetic modification of the murine A vy allele by nutritional supplementation. Proc. Natl Acad. Sci. USA 103, 17 308-17 312. (doi:10.1073/pnas.0607090103)
13. Waterland RA, Dolinoy DC, Lin JR, Smith CA, Shi X, Tahiliani KG. 2006 Maternal methyl supplements increase offspring DNA methylation at axin fused. Genesis 44, 401-406. (doi:10.1002/dvg.20230)
14. Ostertag EM, Kazazian Jr HH. 2001 Biology of mammalian L1 retrotransposons. Annu. Rev. Genet. 35, 501-538. (doi:10.1146/annurev.genet.35. 102401.091032)
15. Kuff EL, Lueders KK. 1988 The intracisternal A-particle gene family: structure and functional aspects. Adv. Cancer Res. 51, 183-276. (doi:10. 1016/S0065-230X(08)60223-7)
16. Dewannieux M, Dupressoir A, Harper F, Pierron G, Heidmann T. 2004 Identification of autonomous IAP LTR retrotransposons mobile in mammalian cells. Nat. Genet. 36, 534-539. (doi:10.1038/ng1353)
17. Qin C et al. 2010 Intracisternal A particle genes: distribution in the mouse genome, active subtypes, and potential roles as species-specific mediators of susceptibility to cancer. Mol. Carcinog. 49, 54-67. (doi:10.1002/mc.20576)
18. Rawn SM, Cross JC. 2008 The evolution, regulation, and function of placenta-specific genes. Annu. Rev. Cell Dev. Biol. 24, 159-181. (doi:10.1146/annurev. cellbio.24.110707.175418)
19. Johnson LJ, Tricker PJ. 2010 Epigenomic plasticity within populations: its evolutionary significance and potential. Heredity (Edinb.) 105, 113-121. (doi:10. 1038/hdy.2010.25)
20. Chang-Yeh A, Mold DE, Huang RC. 1991 Identification of a novel murine IAP-promoted placenta-expressed gene. Nucleic Acids Res. 19, 3667-3672. (doi:10.1093/nar/19.13.3667)
21. Saitou N, Nei M. 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425. (doi:10.1093/molbev/msl072)
22. Feenstra A, Fewell J, Lueders K, Kuff E. 1986 In vitro methylation inhibits the promotor activity of a cloned intracisternal A-particle LTR. Nucleic Acids Res. 14, 4343-4352. (doi:10.1093/nar/14.10.4343)
23. Lasneret J, Canivet M, Hojman-Montes de Oca F, Tobaly J, Emanoil-Ravicovitch R, Peries J. 1983 Activation of intracisternal A particles by 5-azacytidine in mouse Ki-BALB cell line. Virology 128, 485-489. (doi:10.1016/0042-6822(83)90275-1)
24. Walsh CP, Chaillet JR, Bestor TH. 1998 Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 20, 116-117. (doi:10.1038/2413)
25. Hata K, Kusumi M, Yokomine T, Li E, Sasaki H. 2006 Meiotic and epigenetic aberrations in Dnmt3Ldeficient male germ cells. Mol. Reprod. Dev. 73, 116-122. (doi:10.1002/mrd.20387)
26. Sharif J et al. 2007 The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450, 908-912. (doi:10. 1038/nature06397)
27. Zhao X et al. 2003 Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function. Proc. Natl Acad. Sci. USA 100, 6777-6782. (doi:10.1073/pnas.1131928100)
28. Yoshimura T, Toyoda S, Kuramochi-Miyagawa S, Miyazaki T, Miyazaki S, Tashiro F, Yamato E, Nakano T, Miyazaki J. 2009 Gtsf1/Cue110, a gene encoding a protein with two copies of a CHHC Zn-finger motif, is involved in spermatogenesis and retrotransposon suppression in murine testes. Dev. Biol. 335, 216-227. (doi:10.1016/j.ydbio. 2009.09.003)
29. Kuramochi-Miyagawa S et al. 2008 DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 22, 908-917. (doi:10.1101/gad.1640708)
30. Watanabe T et al. 2011 MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline. Dev. Cell 20, 364-375. (doi:10.1016/j.devcel.2011.01.005)
31. Oey HM, Youngson NA, Whitelaw E. 2011 The characterisation of piRNA-related 19mers in the mouse. BMC Genom. 12, 315. (doi:10.1186/1471-2164-12-315)
32. Dupressoir A, Heidmann T. 1996 Germ line-specific expression of intracisternal A-particle retrotransposons in transgenic mice. Mol. Cell Biol. 16, 4495-4503.
33. Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, Kimura H, Tachibana M, Lorincz MC, Shinkai Y. 2010 Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464, 927-931. (doi:10.1038/nature08858)
34. Dong KB et al. 2008 DNA methylation in ES cells requires the lysine methyltransferase G9a but not its catalytic activity. EMBO J. 27, 2691-2701. (doi:10. 1038/emboj.2008.193)
35. Rowe HM et al. 2010 KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463, 237-240. (doi:10.1038/nature08674)
36. Reik W, Dean W, Walter J. 2001 Epigenetic reprogramming in mammalian development. Science 293, 1089-1093. (doi:10.1126/science.1063443)
37. Leung DC, Lorincz MC. 2012 Silencing of endogenous retroviruses: when and why do histone marks predominate? Trends Biochem. Sci. 37, 127-133. (doi:10.1016/j.tibs.2011.11.006)
38. Hemberger M. 2010 Genetic-epigenetic intersection in trophoblast differentiation: implications for extraembryonic tissue function. Epigenetics 5, 24-29. (doi:10.4161/epi.5.1.10589)
39. Farthing CR, Ficz G, Ng RK, Chan CF, Andrews S, Dean W, Hemberger M, Reik W. 2008 Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes. PLoS Genet. 4, e1000116. (doi:10.1371/journal.pgen.1000116)
40. Djaffar I, Dianoux L, Leibovich S, Kaplan L, Emanoil-Ravier R, Peries J. 1990 Detection of IAP related transcripts in normal and transformed rat cells. Biochem. Biophys. Res. Commun. 169, 222-231. (doi:10.1016/0006-291X(90)91457-4)
41. Ball M, McLellan A, Collins B, Coadwell J, Stewart F, Moore T. 2004 An abundant placental transcript containing an IAP-LTR is allelic to mouse pregnancy-specific glycoprotein 23 (Psg23): cloning and genetic analysis. Gene 325, 103-113. (doi:10.1016/j.gene.2003.10.001)
42. Macaulay EC, Weeks RJ, Andrews S, Morison IM. 2011 Hypomethylation of functional retrotransposon-derived genes in the human placenta. Mamm. Genome 22, 722-735. (doi:10. 1007/s00335-011-9355-1)
43. Bièche I et al. 2003 Placenta-specific INSL4 expression is mediated by a human endogenous retrovirus element. Biol. Reprod. 68, 1422-1429. (doi:10.1095/biolreprod.102.010322)
44. Landry JR, Mager DL. 2003 Functional analysis of the endogenous retroviral promoter of the human endothelin B receptor gene. J. Virol. 77, 7459-7466. (doi:10.1128/JVI.77.13.7459-7466.2003)
45. Schulte AM, Lai S, Kurtz A, Czubayko F, Riegel AT, Wellstein A. 1996 Human trophoblast and choriocarcinoma expression of the growth factor pleiotrophin attributable to germ-line insertion of an endogenous retrovirus. Proc. Natl Acad. Sci. USA 93, 14 759-14 764. (doi:10.1073/pnas.93.25. 14759)
46. Landry JR, Rouhi A, Medstrand P, Mager DL. 2002 The Opitz syndrome gene Mid1 is transcribed from a human endogenous retroviral promoter. Mol. Biol. Evol. 19, 1934-1942. (doi:10.1093/oxfordjournals. molbev.a004017)
47. Nelson PN, Hooley P, Roden D, Davari Ejtehadi H, Rylance P, Warren P, Martin J, Murray PG. 2004 Human endogenous retroviruses: transposable elements with potential? Clin. Exp. Immunol. 138, 1-9. (doi:10.1111/j.1365-2249.2004.02592.x)
48. Emera D, Casola C, Lynch VJ, Wildman DE, Agnew D, Wagner GP. 2012 Convergent evolution of endometrial prolactin expression in primates, mice, and elephants through the independent recruitment of transposable elements. Mol. Biol. Evol. 29, 239-247. (doi:10.1093/molbev/msr189)
49. Cornelis G, Heidmann O, Bernard-Stoecklin S, Reynaud K, Véron G, Mulot B, Dupressoir A, Heidmann T. 2012 Ancestral capture of syncytin-Car1, a fusogenic endogenous retroviral envelope gene involved in placentation and conserved in Carnivora. Proc. Natl Acad. Sci. USA 109, E432-E441. (doi:10.1073/pnas.1115346109)
50. Dolinoy DC. 2008 The agouti mouse model: an epigenetic biosensor for nutritional and environmental alterations on the fetal epigenome. Nutr. Rev. 66(Suppl. 1), S7-S11. (doi:10.1111/j. 1753-4887.2008.00056.x)
51. Dolinoy DC, Huang D, Jirtle RL. 2007 Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc. Natl Acad. Sci. USA 104, 13 056-13 061. (doi:10.1073/pnas.0703739104)
52. Gluckman PD, Hanson MA, Pinal C. 2005 The developmental origins of adult disease. Matern. Child Nutr. 1, 130-141. (doi:10.1111/j.1740-8709. 2005.00020.x)
53. Wells JC. 2011 The thrifty phenotype: an adaptation in growth or metabolism? Am. J. Hum. Biol. 23, 65-75. (doi:10.1002/ajhb.21100)
54. Scherneck S et al. 2009 Positional cloning of zinc finger domain transcription factor Zfp69, a candidate gene for obesity-associated diabetes contributed by mouse locus Nidd/SJL. PLoS Genet. 5, e1000541. (doi:10.1371/journal.pgen.1000541)
55. Kouyama R et al. 2005 Attenuation of diet-induced weight gain and adiposity through increased energy expenditure in mice lacking angiotensin II type 1a receptor. Endocrinology 146, 3481-3489. (doi:10. 1210/en.2005-0003)
56. Nikpay M, Seda O, Tremblay J, Petrovich M, Gaudet D, Kotchen TA, Cowley Jr AW, Hamet P. 2012 Genetic mapping of habitual substance use, obesity-related traits, responses to mental and physical stress, and heart rate and blood pressure measurements reveals shared genes that are overrepresented in the neural synapse. Hypertens. Res. 35, 585-591. (doi:10.1038/hr.2011.233)
57. Song YB, An YR, Kim SJ, Park HW, Jung JW, Kyung JS, Hwang SY, Kim YS. 2012 Lipid metabolic effect of Korean red ginseng extract in mice fed on a high-fat diet. J. Sci. Food Agric. 92, 388-396. (doi:10.1002/jsfa.4589)
58. Masson O, Chavey C, Dray C, Meulle A, Daviaud D, Quilliot D, Muller C, Valet P, Liaudet-Coopman E. 2009 LRP1 receptor controls adipogenesis and is up-regulated in human and mouse obese adipose tissue. PLoS ONE 4, e7422. (doi:10.1371/journal. pone.0007422)
59. Allen DL, Greybeck BJ, Hanson AM, Cleary AS, Lindsay SF. 2010 Skeletal muscle expression of bone morphogenetic protein-1 and tolloid-like-1 extracellular proteases in different fiber types and in response to unloading, food deprivation and differentiation. J. Physiol. Sci. 60, 343-352. (doi:10. 1007/s12576-010-0110-2)
60. Mehedint MG, Craciunescu CN, Zeisel SH. 2010 Maternal dietary choline deficiency alters angiogenesis in fetal mouse hippocampus. Proc. Natl Acad. Sci. USA 107, 12 834-12 839. (doi:10.1073/pnas.0914328107)
61. Chen JH, Tarry-Adkins JL, Matharu K, Yeo GS, Ozanne SE. 2010 Maternal protein restriction affects gene expression profiles in the kidney at weaning with implications for the regulation of renal function and lifespan. Clin. Sci. (Lond.) 119, 373-384. (doi:10.1042/CS20100230)
62. Chalkiadaki A, Guarente L. 2012 Sirtuins mediate mammalian metabolic responses to nutrient availability. Nat. Rev. Endocrinol. 8, 287-296. (doi:10.1038/nrendo.2011.225)
63. Morris-Rosendahl DJ et al. 2010 New RAB3GAP1 mutations in patients with Warburg Micro Syndrome from different ethnic backgrounds and a possible founder effect in the Danish. Eur. J. Hum. Genet. 18, 1100-1106. (doi:10.1038/ejhg.2010.79)
64. van Daalen E et al. 2011 Social responsiveness scale-aided analysis of the clinical impact of copy number variations in autism. Neurogenetics 12, 315-323. (doi:10.1007/s10048-011-0297-2)
65. Brown AM, Gordon D, Lee H, Caudy M, Hardy J, Haroutunian V, Blass JP. 2004 Association of the dihydrolipoamide dehydrogenase gene with Alzheimer's disease in an Ashkenazi Jewish population. Am. J. Med. Genet. B Neuropsychiatr. Genet. 131B, 60-66. (doi:10.1002/ajmg.b.30008)
66. MacLaren EJ, Charlesworth P, Coba MP, Grant SG. 2011 Knockdown of mental disorder susceptibility genes disrupts neuronal network physiology in vitro. Mol. Cell Neurosci. 47, 93-99. (doi:10.1016/j. mcn.2010.12.014)
67. Elia J et al. 2011 Genome-wide copy number variation study associates metabotropic glutamate receptor gene networks with attention deficit hyperactivity disorder. Nat. Genet. 44, 78-84. (doi:10.1038/ng.1013)
68. Ayuso P et al. 2011 A polymorphism located at an ATG transcription start site of the heme oxygenase-2 gene is associated with classical Parkinson's disease. Pharmacogenet. Genom. 21, 565-571. (doi:10.1097/FPC.0b013e328348f729)
69. Gregersen N et al. 2012 A genome-wide study of panic disorder suggests the amiloride-sensitive cation channel 1 as a candidate gene. Eur. J. Hum. Genet. 20, 84-90. (doi:10.1038/ejhg.2011.148)
70. Peñagarikano O, Geschwind DH. 2012 What does CNTNAP2 reveal about autism spectrum disorder? Trends Mol. Med. 18, 156-163. (doi:10.1016/j. molmed.2012.01.003)
71. Al Badr W et al. 2011 Exome capture and massively parallel sequencing identifies a novel HPSE2 mutation in a Saudi Arabian child with Ochoa (urofacial) syndrome. J. Pediatr. Urol. 7, 569-573. (doi:10.1016/j.jpurol.2011.02.034)
72. Kantojärvi K, Kotala I, Rehnström K, Ylisaukko-Oja T, Vanhala R, von Wendt TN, von Wendt L, Järvelä I. 2011 Fine mapping of Xq11.1-q21.33 and mutation screening of RPS6KA6, ZNF711, ACSL4, DLG3, and IL1RAPL2 for autism spectrum disorders (ASD). Autism Res. 4, 228-233. (doi:10.1002/aur.187)
73. Swaminathan S, Shen L, Kim S, Inlow M, West JD, Faber KM, Foroud T, Mayeux R, Saykin AJ. 2012 Analysis of copy number variation in Alzheimer's disease: the NIA-LOAD/NCRAD Family Study. Curr. Alzheimer Res. 9, 801-814. (doi:10.2174/156720512802455331)
74. Kushima I et al. 2012 Resequencing and association analysis of the KALRN and EPHB1 genes and their contribution to schizophrenia susceptibility. Schizophr Bull. 38, 552-560. (doi:10.1093/schbul/sbq118)
75. Yoritaka A, Shimo Y, Shimo Y, Inoue Y, Yoshino H, Hattori N. 2011 Nonmotor symptoms in patients with PARK2 mutations. Parkinsons Dis. 2011, 473640. (doi:10.4061/2011/473640)
76. Wan XH, Li SJ, Cheng P, Zhang Q, Yang XC, Zhong GZ, Hu WL, Jin L, Wang XF. 2011 NINJ2 polymorphism is associated with ischemic stroke in Chinese Han population. J. Neurol. Sci. 308, 67-71. (doi:10.1016/j.jns.2011.06.011)
77. Raychaudhuri S, Korn JM, McCarroll SA, International Schizophrenia Consortium, Altshuler D, Sklar P, Purcell S, Daly MJ. 2010 Accurately assessing the risk of schizophrenia conferred by rare copy-number variation affecting genes with brain function. PLoS Genet. 6, e1001097. (doi:10. 1371/journal.pgen.1001097)
78. Wildman DE, Chen C, Erez O, Grossman LI, Goodman M, Romero R. 2006 Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc. Natl Acad. Sci. USA 103, 3203-3208. (doi:10.1073/pnas.0511344103)
79. Watson ED, Cross JC. 2005 Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 20, 180-193. (doi:10.1152/physiol.00001.2005)
80. Sharif J, Endo TA, Toyoda T, Koseki H. 2010 Divergence of CpG island promoters: a consequence or cause of evolution? Dev. Growth Differ. 52, 545-554. (doi:10.1111/j.1440-169X. 2010.01193.x)
81. Knox K, Baker JC. 2008 Genomic evolution of the placenta using co-option and duplication and divergence. Genome Res. 18, 695-705. (doi:10. 1101/gr.071407.107)
82. Lynch VJ, Brayer K, Gellersen B, Wagner GP. 2009 HoxA-11 and FOXO1A cooperate to regulate decidual prolactin expression: towards inferring the core transcriptional regulators of decidual genes. PLoS ONE 4, e6845. (doi:10.1371/journal.pone.0006845)