Convergent and divergent evolution of genomic imprinting in the marsupial Monodelphis domestica

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Das, Radhika ^a   Anderson, Nathan ^b   Koran, MaryEllen I ^a   Weidman, Jennifer R ^a   Mikkelsen, Tarjei S ^b   Kamal, Michael ^b   Murphy, Susan K ^a   Linblad Toh, Kerstin ^b,c   Greally, John M ^d   Jirtle, Randy L ^e  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c UPPSALA UNIVERSITY   (Sweden)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Eutherians; Genomic imprinting; Marsupials

Indexed keywords

SEROTONIN RECEPTOR; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CONVERGENT EVOLUTION; COPG2 GENE; CPG ISLAND; DIVERGENT EVOLUTION; DNA METHYLATION; EPIGENETICS; EVOLUTION; GENE; GENE EXPRESSION; GENE FUNCTION; GENE LOCUS; GENOME IMPRINTING; HISTONE MODIFICATION; HTR2A GENE; IMPACT GENE; L3MBTL GENE; MARSUPIAL; MONODELPHIS DOMESTICA; MOUSE; NONHUMAN; OPOSSUM; PLACENTAL MAMMALS; PLAGL1 GENE; PROMOTER REGION;

ALLELES; ANIMALS; BIOLOGICAL EVOLUTION; CPG ISLANDS; DNA METHYLATION; GENOME; GENOMIC IMPRINTING; HISTONES; HUMANS; INTRONS; MICE; MONODELPHIS; PROMOTER REGIONS, GENETIC;

DIDELPHIDAE; EUTHERIA; METATHERIA; MONODELPHIS DOMESTICA; THERIA;

EID: 84864952442     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-394     Document Type: Article

References (43)

1. Morison IM, Ramsay JP, Spencer HG. A census of mammalian imprinting. Trends Genet 2005, 21(8):457-465. 10.1016/j.tig.2005.06.008, 15990197.
2. Barton SC, Surani MA, Norris ML. Role of paternal and maternal genomes in mouse development. Nature 1984, 311(5984):374-376. 10.1038/311374a0, 6482961.
3. McGrath J, Solter D. Nucleocytoplasmic interactions in the mouse embryo. J Embryol Exp Morphol 1986, 97(Suppl):277-289.
4. Surani MA, Barton SC, Norris ML. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 1984, 308(5959):548-550. 10.1038/308548a0, 6709062.
5. Killian JK, Buckley TR, Stewart N, Munday BL, Jirtle RL. Marsupials and Eutherians reunited: genetic evidence for the Theria hypothesis of mammalian evolution. Mamm Genome 2001, 12(7):513-517. 10.1007/s003350020026, 11420613.
6. Killian JK, Nolan CM, Wylie AA, Li T, Vu TH, Hoffman AR, Jirtle RL. Divergent evolution in M6P/IGF2R imprinting from the Jurassic to the Quaternary. Hum Mol Genet 2001, 10(17):1721-1728. 10.1093/hmg/10.17.1721, 11532981.
7. Suzuki S, Ono R, Narita T, Pask AJ, Shaw G, Wang C, Kohda T, Alsop AE, Marshall Graves JA, Kohara Y, et al. Retrotransposon silencing by DNA methylation can drive mammalian genomic imprinting. PLoS Genet 2007, 3(4):e55. 10.1371/journal.pgen.0030055, 1851980, 17432937.
8. Suzuki S, Renfree MB, Pask AJ, Shaw G, Kobayashi S, Kohda T, Kaneko-Ishino T, Ishino F. Genomic imprinting of IGF2, p57(KIP2) and PEG1/MEST in a marsupial, the tammar wallaby. Mech Dev 2005, 122(2):213-222. 10.1016/j.mod.2004.10.003, 15652708.
9. Weidman JR, Maloney KA, Jirtle RL. Comparative phylogenetic analysis reveals multiple non-imprinted isoforms of opossum Dlk1. Mamm Genome 2006, 17(2):157-167. 10.1007/s00335-005-0116-x, 16465595.
10. Weidman JR, Murphy SK, Nolan CM, Dietrich FS, Jirtle RL. Phylogenetic footprint analysis of IGF2 in extant mammals. Genome Res 2004, 14(9):1726-1732. 10.1101/gr.2774804, 515318, 15342558.
11. Ager E, Suzuki S, Pask A, Shaw G, Ishino F, Renfree MB. Insulin is imprinted in the placenta of the marsupial, Macropus eugenii. Dev Biol 2007, 309(2):317-328. 10.1016/j.ydbio.2007.07.025, 17706631.
12. Edwards CA, Mungall AJ, Matthews L, Ryder E, Gray DJ, Pask AJ, Shaw G, Graves JA, Rogers J, Dunham I, et al. The evolution of the DLK1-DIO3 imprinted domain in mammals. PLoS Biol 2008, 6(6):e135. 10.1371/journal.pbio.0060135, 2408620, 18532878.
13. Killian JK, Nolan CM, Stewart N, Munday BL, Andersen NA, Nicol S, Jirtle RL. Monotreme IGF2 expression and ancestral origin of genomic imprinting. J Exp Zool 2001, 291(2):205-212. 10.1002/jez.1070, 11479919.
14. Haig D. Genomic imprinting and kinship: how good is the evidence?. Annu Rev Genet 2004, 38:553-585. 10.1146/annurev.genet.37.110801.142741, 15568986.
15. Moore T, Haig D. Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet 1991, 7(2):45-49. 10.1016/0168-9525(91)90230-N, 2035190.
16. Hoffman AR, Vu TH, Hu J. Mechanisms of genomic imprinting. Growth Horm IGF Res 2000, 10(Suppl A):S18-S19.
17. Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet 2001, 2(1):21-32.
18. Lawton BR, Carone BR, Obergfell CJ, Ferreri GC, Gondolphi CM, Vandeberg JL, Imumorin I, O'Neill RJ, O'Neill MJ. Genomic imprinting of IGF2 in marsupials is methylation dependent. BMC Genomics 2008, 9:205. 10.1186/1471-2164-9-205, 2386826, 18454865.
19. Smrzka OW, Fae I, Stoger R, Kurzbauer R, Fischer GF, Henn T, Weith A, Barlow DP. Conservation of a maternal-specific methylation signal at the human IGF2R locus. Hum Mol Genet 1995, 4(10):1945-1952. 10.1093/hmg/4.10.1945, 8595419.
20. Grandjean V, O'Neill L, Sado T, Turner B, Ferguson-Smith A. Relationship between DNA methylation, histone H4 acetylation and gene expression in the mouse imprinted Igf2-H19 domain. FEBS Lett 2001, 488(3):165-169. 10.1016/S0014-5793(00)02349-8, 11163765.
21. Vu TH, Li T, Hoffman AR. Promoter-restricted histone code, not the differentially methylated DNA regions or antisense transcripts, marks the imprinting status of IGF2R in human and mouse. Hum Mol Genet 2004, 13(19):2233-2245. 10.1093/hmg/ddh244, 15294879.
22. Yang Y, Li T, Vu TH, Ulaner GA, Hu JF, Hoffman AR. The histone code regulating expression of the imprinted mouse Igf2r gene. Endocrinology 2003, 144(12):5658-5670. 10.1210/en.2003-0798, 12975326.
23. Reik W, Lewis A. Co-evolution of X-chromosome inactivation and imprinting in mammals. Nat Rev Genet 2005, 6(5):403-410. 10.1038/nrg1602, 15818385.
24. Yokomine T, Hata K, Tsudzuki M, Sasaki H. Evolution of the vertebrate DNMT3 gene family: a possible link between existence of DNMT3L and genomic imprinting. Cytogenet Genome Res 2006, 113(1-4):75-80.
25. Ding F, Patel C, Ratnam S, McCarrey JR, Chaillet JR. Conservation of Dnmt1o cytosine methyltransferase in the marsupial Monodelphis domestica. Genesis 2003, 36(4):209-213. 10.1002/gene.10215, 12929092.
26. Kaslow DC, Migeon BR. DNA methylation stabilizes X chromosome inactivation in eutherians but not in marsupials: evidence for multistep maintenance of mammalian X dosage compensation. Proc Natl Acad Sci U S A 1987, 84(17):6210-6214. 10.1073/pnas.84.17.6210, 299040, 3476942.
27. Loebel DA, Johnston PG. Methylation analysis of a marsupial X-linked CpG island by bisulfite genomic sequencing. Genome Res 1996, 6(2):114-123. 10.1101/gr.6.2.114, 8919690.
28. Lee JT. Molecular links between X-inactivation and autosomal imprinting: X-inactivation as a driving force for the evolution of imprinting?. Curr Biol 2003, 13(6):R242-R254. 10.1016/S0960-9822(03)00162-3, 12646153.
29. Dolinoy D, Huang D, Jirtle R. Maternal nutrient supplementation counteracts bisphenol-A induced hypomethylation in early development. Proc Natl Acad Sci USA 2007, 104(32):13056-13061. 10.1073/pnas.0703739104, 1941790, 17670942.
30. Kobayashi S, Kohda T, Miyoshi N, Kuroiwa Y, Aisaka K, Tsutsumi O, Kaneko-Ishino T, Ishino F. Human PEG1/MEST, an imprinted gene on chromosome 7. Hum Mol Genet 1997, 6(5):781-786. 10.1093/hmg/6.5.781, 9158153.
31. Blagitko N, Schulz U, Schinzel AA, Ropers HH, Kalscheuer VM. gamma2-COP, a novel imprinted gene on chromosome 7q32, defines a new imprinting cluster in the human genome. Hum Mol Genet 1999, 8(13):2387-2396. 10.1093/hmg/8.13.2387, 10556286.
32. De Luca V, Likhodi O, Kennedy JL, Wong AH. Parent-of-origin effect and genomic imprinting of the HTR2A receptor gene T102C polymorphism in psychosis. Psychiatry Res 2007, 151(3):243-248. 10.1016/j.psychres.2006.11.010, 17407792.
33. Li J, Bench AJ, Vassiliou GS, Fourouclas N, Ferguson-Smith AC, Green AR. Imprinting of the human L3MBTL gene, a polycomb family member located in a region of chromosome 20 deleted in human myeloid malignancies. Proc Natl Acad Sci U S A 2004, 101(19):7341-7346. 10.1073/pnas.0308195101, 409920, 15123827.
34. Okamura K, Hagiwara-Takeuchi Y, Li T, Vu TH, Hirai M, Hattori M, Sakaki Y, Hoffman AR, Ito T. Comparative genome analysis of the mouse imprinted gene impact and its nonimprinted human homolog IMPACT: toward the structural basis for species-specific imprinting. Genome Res 2000, 10(12):1878-1889. 10.1101/gr.139200, 11116084.
35. Okamura K, Ito T. Lessons from comparative analysis of species-specific imprinted genes. Cytogenet Genome Res 2006, 113(1-4):159-164.
36. Valleley EM, Cordery SF, Bonthron DT. Tissue-specific imprinting of the ZAC/PLAGL1 tumour suppressor gene results from variable utilization of monoallelic and biallelic promoters. Hum Mol Genet 2007, 16(8):972-981. 10.1093/hmg/ddm041, 17341487.
37. Weidman JR, Dolinoy DC, Maloney KA, Cheng JF, Jirtle RL. Imprinting of opossum Igf2r in the absence of differential methylation and air. Epigenetics 2006, 1(1):49-54. 10.4161/epi.1.1.2592, 17998818.
38. Khatib H. The COPG2, DCN, and SDHD genes are biallelically expressed in cattle. Mamm Genome 2005, 16(7):545-552. 10.1007/s00335-005-0029-8, 16151700.
39. Rapkins RW, Hore T, Smithwick M, Ager E, Pask AJ, Renfree MB, Kohn M, Hameister H, Nicholls RD, Deakin JE, et al. Recent assembly of an imprinted domain from non-imprinted components. PLoS Genet 2006, 2(10):e182. 10.1371/journal.pgen.0020182, 1626109, 17069464.
40. Edwards CA, Rens W, Clarke O, Mungall AJ, Hore T, Graves JA, Dunham I, Ferguson-Smith AC, Ferguson-Smith MA. The evolution of imprinting: chromosomal mapping of orthologues of mammalian imprinted domains in monotreme and marsupial mammals. BMC Evol Biol 2007, 7:157. 10.1186/1471-2148-7-157, 2042987, 17822525.
41. Hore TA, Rapkins RW, Graves JA. Construction and evolution of imprinted loci in mammals. Trends Genet 2007, 23(9):440-448. 10.1016/j.tig.2007.07.003, 17683825.
42. Smits G, Mungall AJ, Griffiths-Jones S, Smith P, Beury D, Matthews L, Rogers J, Pask AJ, Shaw G, VandeBerg JL, et al. Conservation of the H19 noncoding RNA and H19-IGF2 imprinting mechanism in therians. Nat Genet 2008, 40(8):971-976. 10.1038/ng.168, 18587395.
43. Suzuki S, Shaw G, Kaneko-Ishino T, Ishino F, Renfree MB. Characterisation of marsupial PHLDA2 reveals eutherian specific acquisition of imprinting. BMC Evol Biol 2011, 11:244. 10.1186/1471-2148-11-244, 3170258, 21854573.