The Evolution of Genomic Imprinting – A Marsupial Perspective

  • Timothy A. Hore
  • Marilyn B. Renfree
  • Andrew J. Pask
  • Jennifer A. Marshall Graves


Genomic imprinting is a medically significant epigenetic trait in which genes are expressed from only one of the two alleles, according to their parent of origin. Among vertebrates, imprinted gene expression has been found only in the live-bearing therian mammals – eutherians (placental mammals) and marsupials. Because marsupials are so distantly related to eutherians, comparisons of imprinting between the two mammalian infraclasses are particularly valuable. However, the popular mammalian model organisms (humans, mice and domestic mammals) are all eutherian, so imprinting in marsupials has not received the attention it deserves. Research gathered over some years shows that marsupial orthologues of many imprinted domains in eutherians, such as the well characterised IGF2/H19 and PEG10 domains, comprise fewer imprinted genes. Other eutherian imprinted domains, such as the X-inactivation centre, Callipyge and Prader-Willi/Angleman syndrome domains, are either completely absent in marsupials or are not imprinted. The occurrence of imprinting in marsupials (with some imprinted genes) and eutherians (with many imprinted genes) contrasts with the likely absence of imprinting in egg-laying vertebrates (monotreme mammals, birds and reptiles). The acquisition of imprinting by therian mammals correlates with increased dependence on placentation for early development and coincides with the acquisition of a unique repeat content within the genome and germline expression of BORIS. Analysis of the evolutionary trajectory of these traits offers us insights into how and why genomic imprinting evolved in mammals.


Evolution Genomic imprinting Marsupials Parental conflict Regulators of imprinting 


  1. Ager E, Suzuki S, Pask AJ, et al. (2007) Insulin is imprinted in the placenta of the marsupial, Macropus eugenii. Dev Biol 309:317–328.PubMedCrossRefGoogle Scholar
  2. Ager EI, Pask AJ, Gehring HM, Shaw G, Renfree MB (2008a). Evolution of the CDKN1C-KCNQ1 imprinted domain. BMC Evol Biol 8:163.PubMedCrossRefGoogle Scholar
  3. Ager EI, Pask AJ, Shaw G, Renfree MB (2008b). Expression and protein localisation of IGF2 in the marsupial placenta. BMC Dev Biol 8:17.PubMedCrossRefGoogle Scholar
  4. Angiolini E, Fowden A, Coan P, et al. (2006) Regulation of placental efficiency for nutrient transport by imprinted genes. Placenta 27(Suppl A):S98–S102.PubMedCrossRefGoogle Scholar
  5. Barlow DP (1993) Methylation and imprinting: from host defense to gene regulation? Science 260:309–310.PubMedCrossRefGoogle Scholar
  6. Bartolomei MS, Zemel S, Tilghman SM (1991) Parental imprinting of the mouse H19 gene. Nature 351:153–155.PubMedCrossRefGoogle Scholar
  7. Bell AC, Felsenfeld G (2000) Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405:482–485.PubMedCrossRefGoogle Scholar
  8. Bininda-Emonds OR, Cardillo M, Jones KE, et al. (2007) The delayed rise of present-day mammals. Nature 446:507–512.PubMedCrossRefGoogle Scholar
  9. Bourc’his D, Xu GL, Lin CS, Bollman B, Bestor TH (2001) Dnmt3L and the establishment of maternal genomic imprints. Science 294:2536–2539.PubMedCrossRefGoogle Scholar
  10. Burke LJ, Hollemann T, Pieler T, Renkawitz R (2002) Molecular cloning and expression of the chromatin insulator protein CTCF in Xenopus laevis. Mech Dev 113:95–98.PubMedCrossRefGoogle Scholar
  11. Cai X, Cullen BR (2007) The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA 13:313–316.PubMedCrossRefGoogle Scholar
  12. Cavaille J, Seitz H, Paulsen M, Ferguson-Smith AC, Bachellerie JP (2002) Identification of tandemly-repeated C/D snoRNA genes at the imprinted human 14q32 domain reminiscent of those at the Prader-Willi/Angelman syndrome region. Hum Mol Genet 11:1527–1538.PubMedCrossRefGoogle Scholar
  13. Chabowski A, Coort SLM, Calles-Escandon J, et al. (2004) Insulin stimulates fatty acid transport by regulating expression of FAT/CD36 but not FABPpm. Am J Physiol Endocrinol Metab 287:781–789.CrossRefGoogle Scholar
  14. Chaillet JR (1994) Genomic imprinting: lessons from mouse transgenes. Mutat Res 307:441–449.PubMedCrossRefGoogle Scholar
  15. Charlier C, Segers K, Wagenaar D, et al. (2001) Human-ovine comparative sequencing of a 250-kb imprinted domain encompassing the callipyge (clpg) locus and identification of six imprinted transcripts: DLK1, DAT, GTL2, PEG11, antiPEG11, and MEG8. Genome Res 11:850–862.PubMedCrossRefGoogle Scholar
  16. Cockburn A (1997) Living slow and dying young: senescence in marsupials. In: Saunders N, Hinds L (eds) Marsupial Biology: Recent Research, New Perspectives. University of New South Wales Press, Sydney.Google Scholar
  17. Cockett NE, Jackson SP, Shay TL, et al. (1996) Polar overdominance at the ovine callipyge locus. Science 273:236–238.PubMedCrossRefGoogle Scholar
  18. Colosi DC, Martin D, More K, Lalande M (2006) Genomic organization and allelic expression of UBE3A in chicken. Gene 383:93–98.PubMedCrossRefGoogle Scholar
  19. Constancia M, Hemberger M, Hughes J, et al. (2002) Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417:945–948.PubMedCrossRefGoogle Scholar
  20. Cooper DW, VandeBerg JL, Sharman GB, Poole WE (1971) Phosphoglycerate kinase polymorphism in kangaroos provides further evidence for paternal X inactivation. Nat New Biol 230:155–157.PubMedCrossRefGoogle Scholar
  21. Curley JP, Barton S, Surani A, Keverne EB (2004) Coadaptation in mother and infant regulated by a paternally expressed imprinted gene. Proc Biol Sci 271:1303–1309.PubMedCrossRefGoogle Scholar
  22. da Rocha ST, Edwards CA, Ito M, Ogata T, Ferguson-Smith AC (2008) Genomic imprinting at the mammalian Dlk1-Dio3 domain. Trends Genet 24:306–316.PubMedCrossRefGoogle Scholar
  23. Davidow LS, Breen M, Duke SE, et al. (2007) The search for a marsupial XIC reveals a break with vertebrate synteny. Chromosome Res 15:137–146.PubMedCrossRefGoogle Scholar
  24. Davis E, Caiment F, Tordoir X, et al. (2005) RNAi-mediated allelic trans-interaction at the imprinted Rtl1/Peg11 locus. Curr Biol 15:743–749.PubMedCrossRefGoogle Scholar
  25. Day T, Bonduriansky R (2004) Intralocus sexual conflict can drive the evolution of genomic imprinting. Genetics 167:1537–1546.PubMedCrossRefGoogle Scholar
  26. Deakin JE, Hore TA, Koina E, Graves JAM (2008) The status of dosage compensation in the multiple X chromosomes of the platypus. PLoS Genet 4:e1000140.PubMedCrossRefGoogle Scholar
  27. DeChiara TM, Robertson EJ, Efstratiadis A (1991) Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64:849–859.PubMedCrossRefGoogle Scholar
  28. Deltour L, Montagutelli X, Guenet JL, Jami J, Paldi A (1995) Tissue- and developmental stage-specific imprinting of the mouse proinsulin gene, Ins2. Dev Biol 168:686–688.PubMedCrossRefGoogle Scholar
  29. Dindot SV, Farin PW, Farin CE, et al. (2004) Epigenetic and genomic imprinting analysis in nuclear transfer derived Bos gaurus/Bos taurus hybrid fetuses. Biol Reprod 71:470–478.PubMedCrossRefGoogle Scholar
  30. Dunzinger U, Nanda I, Schmid M, Haaf T, Zechner U (2005) Chicken orthologues of mammalian imprinted genes are clustered on macrochromosomes and replicate asynchronously. Trends Genet 21:488–492.PubMedCrossRefGoogle Scholar
  31. Duret L, Chureau C, Samain S, Weissenbach J, Avner P (2006) The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 312:1653–1655.PubMedCrossRefGoogle Scholar
  32. Edwards CA, Mungall AJ, Matthews L, et al. (2008) The evolution of the DLK1-DIO3 imprinted domain in mammals. PLoS Biol 6:e135.PubMedCrossRefGoogle Scholar
  33. Elisaphenko EA, Kolesnikov NN, Shevchenko AI, et al. (2008) A dual origin of the Xist gene from a protein-coding gene and a set of transposable elements. PLoS ONE 3:e2521.PubMedCrossRefGoogle Scholar
  34. Fehlmann M, Le Cam A, Freychet P (1979) Insulin and glucagon stimulation of amino acid transport in isolated rat hepatocytes. Synthesis of a high affinity component of transport. J Biol Chem 254:10431–10437.PubMedGoogle Scholar
  35. Filippova GN (2008) Genetics and epigenetics of the multifunctional protein CTCF. Curr Top Dev Biol 80:337–360.PubMedCrossRefGoogle Scholar
  36. Fisher DO, Double MC, Blomberg SP, Jennions MD, Cockburn A (2006) Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild. Nature 444:89–92.PubMedCrossRefGoogle Scholar
  37. Freeman SJ (1990) Functions of extraembryonic membranes. In: Postimplantation Mammalian Embryos: A Practical Approach. Oxford University Press, New York.Google Scholar
  38. Genevieve D, Sanlaville D, Faivre L, et al. (2005) Paternal deletion of the GNAS imprinted locus (including Gnasxl) in two girls presenting with severe pre- and post-natal growth retardation and intractable feeding difficulties. Eur J Hum Genet 13:1033–1039.PubMedCrossRefGoogle Scholar
  39. Giddings SJ, King CD, Harman KW, Flood JF, Carnaghi LR (1994) Allele specific inactivation of insulin 1 and 2, in the mouse yolk sac, indicates imprinting. Nat Genet 6:310–313.PubMedCrossRefGoogle Scholar
  40. Goll MG, Bestor TH (2005) Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74:481–514.PubMedCrossRefGoogle Scholar
  41. Graves JAM (1996) Mammals that break the rules: genetics of marsupials and monotremes. Annu Rev Genet 30:233–260.PubMedCrossRefGoogle Scholar
  42. Gray TA, Saitoh S, Nicholls RD (1999a). An imprinted, mammalian bicistronic transcript encodes two independent proteins. Proc Natl Acad Sci USA 96:5616–5621.PubMedCrossRefGoogle Scholar
  43. Gray TA, Smithwick MJ, Schaldach MA, et al. (1999b). Concerted regulation and molecular evolution of the duplicated SNRPB’/B and SNRPN loci. Nucleic Acids Res 27:4577–4584.PubMedCrossRefGoogle Scholar
  44. Gray TA, Hernandez L, Carey AH, et al. (2000) The ancient source of a distinct gene family encoding proteins featuring RING and C(3)H zinc-finger motifs with abundant expression in developing brain and nervous system. Genomics 66:76–86.PubMedCrossRefGoogle Scholar
  45. Gulbis B, Jauniaux E, Cotton F, Stordeur P (1998) Protein and enzyme patterns in the fluid cavities of the first trimester gestational sac: relevance to the absorptive role of secondary yolk sac. Mol Hum Reprod 4:857–862.PubMedCrossRefGoogle Scholar
  46. Haig D, Westoby M (1989) Parent-specific gene-expression and the triploid endosperm. American Naturalist 134:147–155.CrossRefGoogle Scholar
  47. Haig D (2000) The kinship theory of genomic imprinting. Ann Rev Ecol Syst 31:9–32.CrossRefGoogle Scholar
  48. Haig D, Wharton R (2003) Prader-Willi syndrome and the evolution of human childhood. Am J Hum Biol 15:320–329.PubMedCrossRefGoogle Scholar
  49. Haig D (2004) Genomic imprinting and kinship: how good is the evidence? Annu Rev Genet 38:553–585.PubMedCrossRefGoogle Scholar
  50. Han L, Lee DH, Szabo PE (2008) CTCF is the master organizer of domain-wide allele-specific chromatin at the H19/Igf2 imprinted region. Mol Cell Biol 28:1124–1135.PubMedCrossRefGoogle Scholar
  51. Happle R (1985) Lyonization and the lines of Blaschko. Hum Genet 70:200–206.PubMedCrossRefGoogle Scholar
  52. Hark AT, Schoenherr CJ, Katz DJ, et al. (2000) CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405:486–489.PubMedCrossRefGoogle Scholar
  53. Hata K, Okano M, Lei H, Li E (2002) Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129:1983–1993.PubMedGoogle Scholar
  54. Heard E, Chaumeil J, Masui O, Okamoto I (2004) Mammalian X-chromosome inactivation: an epigenetics paradigm. Cold Spring Harb Symp Quant Biol 69:89–102.PubMedCrossRefGoogle Scholar
  55. Hernandez-Sanchez C, Mansilla A, de la Rosa EJ, de Pablo F (2006) Proinsulin in development: new roles for an ancient prohormone. Diabetologia 49:1142–1150.PubMedCrossRefGoogle Scholar
  56. Holleley CE, Dickman CR, Crowther MS, Oldroyd BP (2006) Size breeds success: multiple paternity, multivariate selection and male semelparity in a small marsupial, Antechinus stuartii. Mol Ecol 15:3439–3448.PubMedCrossRefGoogle Scholar
  57. Hore TA, Koina E, Wakefield MJ, Graves JAM (2007a). The region homologous to the X-chromosome inactivation centre has been disrupted in marsupial and monotreme mammals. Chromosome Res 15:147–161.PubMedCrossRefGoogle Scholar
  58. Hore TA, Rapkins RW, Graves JAM (2007b). Construction and evolution of imprinted loci in mammals. Trends Genet 23:440–448.PubMedCrossRefGoogle Scholar
  59. Hore TA (2008) The Evolution of Genomic Imprinting and X-Chromosome Inactivation in Mammals. PhD thesis, Research School of Biological Sciences, Canberra.Google Scholar
  60. Hore TA, Deakin JE, Graves JAM (2008) The evolution of epigenetic regulators CTCF and BORIS/CTCFL in amniotes. PLoS Genet 4:e1000169.PubMedCrossRefGoogle Scholar
  61. Jelinic P, Stehle JC, Shaw P (2006) The testis-specific factor CTCFL cooperates with the protein methyltransferase PRMT7 in H19 imprinting control region methylation. PLoS Biol 4:e355.PubMedCrossRefGoogle Scholar
  62. Jia D, Jurkowska RZ, Zhang X, Jeltsch A, Cheng X (2007) Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449:248–251.PubMedCrossRefGoogle Scholar
  63. Jones CJ, Jauniaux E (1995) Ultrastructure of the materno-embryonic interface in the first trimester of pregnancy. Micron 26:145–173.PubMedCrossRefGoogle Scholar
  64. Kaneda M, Okano M, Hata K, et al. (2004) Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429:900–903.PubMedCrossRefGoogle Scholar
  65. Kaneko-Ishino T, Kohda T, Ishino F (2003) The regulation and biological significance of genomic imprinting in mammals. J Biochem 133:699–711.PubMedCrossRefGoogle Scholar
  66. Kawahara M, Wu Q, Takahashi N, et al. (2007) High-frequency generation of viable mice from engineered bi-maternal embryos. Nat Biotechnol 25:1045–1050.PubMedCrossRefGoogle Scholar
  67. Keverne EB, Curley JP (2008) Epigenetics, brain evolution and behaviour. Front Neuroendocrinol 29:398–412.PubMedCrossRefGoogle Scholar
  68. Kholmanskikh O, Loriot A, Brasseur F, De Plaen E, De Smet C (2008) Expression of BORIS in melanoma: lack of association with MAGE-A1 activation. Int J Cancer 122:777–784.PubMedCrossRefGoogle Scholar
  69. Killian JK, Byrd JC, Jirtle JV, et al. (2000) M6P/IGF2R imprinting evolution in mammals. Mol Cell 5:707–716.PubMedCrossRefGoogle Scholar
  70. Killian JK, Nolan CM, Wylie AA, et al. (2001a). Divergent evolution in M6P/IGF2R imprinting from the Jurassic to the Quaternary. Hum Mol Genet 10:1721–1728.PubMedCrossRefGoogle Scholar
  71. Killian JK, Nolan CM, Stewart N, et al. (2001b). Monotreme IGF2 expression and ancestral origin of genomic imprinting. J Exp Zool 291:205–212.PubMedCrossRefGoogle Scholar
  72. Klenova EM, Nicolas RH, Paterson HF, et al. (1993) CTCF, a conserved nuclear factor required for optimal transcriptional activity of the chicken c-myc gene, is an 11-Zn-finger protein differentially expressed in multiple forms. Mol Cell Biol 13:7612–7624.PubMedGoogle Scholar
  73. Klenova EM, Fagerlie S, Filippova GN, et al. (1998) Characterization of the chicken CTCF genomic locus, and initial study of the cell cycle-regulated promoter of the gene. J Biol Chem 273:26571–26579.PubMedCrossRefGoogle Scholar
  74. Kono T, Obata Y, Wu Q, et al. (2004) Birth of parthenogenetic mice that can develop to adulthood. Nature 428:860–864.PubMedCrossRefGoogle Scholar
  75. Kornfeld S (1992) Structure and function of the mannose 6-phosphate/insulinlike growth factor II receptors. Annu Rev Biochem 61:307–330.PubMedCrossRefGoogle Scholar
  76. Lawton BR, Sevigny L, Obergfell C, et al. (2005) Allelic expression of IGF2 in live-bearing, matrotrophic fishes. Dev Genes Evol 215:207–212.PubMedCrossRefGoogle Scholar
  77. Lawton BR, Carone BR, Obergfell CJ, et al. (2008) Genomic imprinting of IGF2 in marsupials is methylation dependent. BMC Genomics 9:205.PubMedCrossRefGoogle Scholar
  78. Li L, Keverne EB, Aparicio SA, et al. (1999) Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science 284:330–333.PubMedCrossRefGoogle Scholar
  79. Livesey G, Williams KE (1981) Rates of pinocytic capture of simple proteins by rat yolk sacs incubated in vitro. Biochem J 198:581–586.PubMedGoogle Scholar
  80. Loukinov DI, Pugacheva E, Vatolin S, et al. (2002) BORIS, a novel male germ-line-specific protein associated with epigenetic reprogramming events, shares the same 11-zinc-finger domain with CTCF, the insulator protein involved in reading imprinting marks in the soma. Proc Natl Acad Sci USA 99:6806–6811.PubMedCrossRefGoogle Scholar
  81. Luo ZX, Ji Q, Wible JR, Yuan CX (2003) An Early Cretaceous tribosphenic mammal and metatherian evolution. Science 302:1934–1940.PubMedCrossRefGoogle Scholar
  82. Lyle R, Watanabe D, Vruchte D, et al. (2000) The imprinted antisense RNA at the Igf2r locus overlaps but does not imprint Mas1. Nat Genet 25:19–21.PubMedCrossRefGoogle Scholar
  83. Lyon MF (1961) Gene action in the X-chromosome of the mouse (Mus musculus L). Nature 190:372–373.PubMedCrossRefGoogle Scholar
  84. Mann JR, Lovell-Badge RH (1984) Inviability of parthenogenones is determined by pronuclei, not egg cytoplasm. Nature 310:66–67.PubMedCrossRefGoogle Scholar
  85. Matsuoka S, Thompson JS, Edwards MC, et al. (1996) Imprinting of the gene encoding a human cyclin-dependent kinase inhibitor, p57KIP2, on chromosome 11p15. Proc Natl Acad Sci USA 93:3026–3030.PubMedCrossRefGoogle Scholar
  86. McGrath J, Solter D (1984) Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37:179–183.PubMedCrossRefGoogle Scholar
  87. McGrath KE, Palis J (2005) Hematopoiesis in the yolk sac:more than meets the eye. Exp Hematol 33:1021–1028.PubMedCrossRefGoogle Scholar
  88. Migeon BR, Wolf SF, Axelman J, Kaslow DC, Schmidt M (1985) Incomplete X chromosome dosage compensation in chorionic villi of human placenta. Proc Natl Acad Sci USA 82:3390–3394.PubMedCrossRefGoogle Scholar
  89. Monk M, Hitchins M, Hawes S (2008) Differential expression of the embryo/cancer gene ECSA(DPPA2), the cancer/testis gene BORIS and the pluripotency structural gene OCT4, in human preimplantation development. Mol Hum Reprod 14:347–355.PubMedCrossRefGoogle Scholar
  90. Moon H, Filippova G, Loukinov D, et al. (2005) CTCF is conserved from Drosophila to humans and confers enhancer blocking of the Fab-8 insulator. EMBO Rep 6:165–170.PubMedCrossRefGoogle Scholar
  91. Moore GE, Abu-Amero SN, Bell G, et al. (2001) Evidence that insulin is imprinted in the human yolk sac. Diabetes 50:199–203.PubMedCrossRefGoogle Scholar
  92. Moore T, Haig D (1991) Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet 7:45–49.PubMedGoogle Scholar
  93. Morison IM, Ramsay JP, Spencer HG (2005) A census of mammalian imprinting. Trends Genet 21:457–465.PubMedCrossRefGoogle Scholar
  94. Nahkuri S, Taft RJ, Korbie DJ, Mattick JS (2008) Molecular Evolution of the HBII-52 snoRNA Cluster. J Mol Biol 381:810–815.PubMedCrossRefGoogle Scholar
  95. Nicholls RD, Knepper JL (2001) Genome organization, function, and imprinting in Prader-Willi and Angelman syndromes. Annu Rev Genomics Hum Genet 2:153–175.PubMedCrossRefGoogle Scholar
  96. Nolan CM, Killian JK, Petitte JN, Jirtle RL (2001) Imprint status of M6P/IGF2R and IGF2 in chickens. Dev Genes Evol 211:179–183.PubMedCrossRefGoogle Scholar
  97. O’Neill MJ, Ingram RS, Vrana PB, Tilghman SM (2000) Allelic expression of IGF2 in marsupials and birds. Dev Genes Evol 210:18–20.PubMedCrossRefGoogle Scholar
  98. O’Neill MJ, Lawton BR, Mateos M, et al. (2007) Ancient and continuing Darwinian selection on insulin-like growth factor II in placental fishes. Proc Natl Acad Sci USA 104:12404–12409.PubMedCrossRefGoogle Scholar
  99. O’Sullivan FM, Murphy SK, Simel LR, et al. (2007) Imprinted expression of the canine IGF2R, in the absence of an anti-sense transcript or promoter methylation. Evol Dev 9:579–589.PubMedCrossRefGoogle Scholar
  100. Ogawa O, Eccles MR, Szeto J, et al. (1993) Relaxation of insulin-like growth factor II gene imprinting implicated in Wilms’ tumour. Nature 362:749–751.PubMedCrossRefGoogle Scholar
  101. Ono R, Kobayashi S, Wagatsuma H, et al. (2001) A retrotransposon-derived gene, PEG10, is a novel imprinted gene located on human chromosome 7q21. Genomics 73:232–237.PubMedCrossRefGoogle Scholar
  102. Ooi SK, Qiu C, Bernstein E, et al. (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448:714–717.PubMedCrossRefGoogle Scholar
  103. Otto SP, Goldstein DB (1992) Recombination and the evolution of diploidy. Genetics 131:745–751.PubMedGoogle Scholar
  104. Oudejans CB, Westerman B, Wouters D, et al. (2001) Allelic IGF2R repression does not correlate with expression of antisense RNA in human extraembryonic tissues. Genomics 73:331–337.PubMedCrossRefGoogle Scholar
  105. Pask AJ, Papenfuss AT, Ager EI, et al. (2009) Analysis of the platypus genome suggests a transposon origin for mammalian imprinting. Genome Biol 10:R1.PubMedCrossRefGoogle Scholar
  106. Payer B, Lee JT (2008) X chromosome dosage compensation: how mammals keep the balance. Annu Rev Genet 42:733–772.PubMedCrossRefGoogle Scholar
  107. Plagge A, Gordon E, Dean W, et al. (2004) The imprinted signaling protein XL alpha s is required for postnatal adaptation to feeding. Nat Genet 36:818–826.PubMedCrossRefGoogle Scholar
  108. Pugacheva EM, Kwon YW, Hukriede NA, et al. (2006) Cloning and characterization of zebrafish CTCF: developmental expression patterns, regulation of the promoter region, and evolutionary aspects of gene organization. Gene 375:26–36.PubMedCrossRefGoogle Scholar
  109. Pugliese A, Zeller M, Fernandez A Jr., et al. (1997) The insulin gene is transcribed in the human thymus and transcription levels correlated with allelic variation at the INS VNTR-IDDM2 susceptibility locus for type 1 diabetes. Nat Genet 15:293–297.PubMedCrossRefGoogle Scholar
  110. Rainier S, Johnson LA, Dobry CJ, et al. (1993) Relaxation of imprinted genes in human cancer. Nature 362:747–749.PubMedCrossRefGoogle Scholar
  111. Rapkins RW, Hore T, Smithwick M, et al. (2006) Recent assembly of an imprinted domain from non-imprinted components. PLoS Genet 2:e182.PubMedCrossRefGoogle Scholar
  112. Reik W, Dean W, Walter J (2001) Epigenetic reprogramming in mammalian development. Science 293:1089–1093.PubMedCrossRefGoogle Scholar
  113. Reik W, Constancia M, Fowden A, et al. (2003) Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. J Physiol 547:35–44.PubMedCrossRefGoogle Scholar
  114. Renfree MB (1972) Influence of the embryo on the marsupial uterus. Nature 240:475–477.PubMedCrossRefGoogle Scholar
  115. Renfree MB (1982) Implantation and placentation. Reprod Mamm 2:26–69.Google Scholar
  116. Renfree MB, Ager EI, Shaw G, Pask AJ (2008) Genomic imprinting in marsupial placentation. Reproduction 136:523–531.PubMedCrossRefGoogle Scholar
  117. Renfree MB, Hore TA, Shaw G, Marshall Graves JAM, Pask AJ (2009) Evolution of genomic imprinting: insights from marsupials and monotremes. Annu Rev Genomics Hum Genet. 10:241–262.PubMedCrossRefGoogle Scholar
  118. Richardson BJ, Czuppon AB, Sharman GB (1971) Inheritance of glucose-6-phosphate dehydrogenase variation in kangaroos. Nat New Biol 230:154–155.PubMedGoogle Scholar
  119. Runte M, Huttenhofer A, Gross S, et al. (2001) The IC-SNURF-SNRPN transcript serves as a host for multiple small nucleolar RNA species and as an antisense RNA for UBE3A. Hum Mol Genet 10:2687–2700.PubMedCrossRefGoogle Scholar
  120. Runte M, Kroisel PM, Gillessen-Kaesbach G, et al. (2004) SNURF-SNRPN and UBE3A transcript levels in patients with Angelman syndrome. Hum Genet 114:553–561.PubMedCrossRefGoogle Scholar
  121. Russo VEA, Martienssen RA, Riggs AD (1996) Epigenetic Mechanisms of Gene Regulation. Cold Spring Harbor Laboratory Press, Plainview.Google Scholar
  122. Scott RJ, Spielman M (2006) Genomic imprinting in plants and mammals: how life history constrains convergence. Cytogenet Genome Res 113:53–67.PubMedCrossRefGoogle Scholar
  123. Seitz H, Royo H, Bortolin ML, et al. (2004) A large imprinted microRNA gene cluster at the mouse Dlk1-Gtl2 domain. Genome Res 14:1741–1748.PubMedCrossRefGoogle Scholar
  124. Shevchenko AI, Zakharova IS, Elisaphenko EA, et al. (2007) Genes flanking Xist in mouse and human are separated on the X chromosome in American marsupials. Chromosome Res 15:127–136.PubMedCrossRefGoogle Scholar
  125. Sleutels F, Zwart R, Barlow DP (2002) The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 415:810–813.PubMedCrossRefGoogle Scholar
  126. Smits G, Mungall AJ, Griffiths-Jones S, et al. (2008) Conservation of the H19 noncoding RNA and H19-IGF2 imprinting mechanism in therians. Nat Genet 40:971–976.PubMedCrossRefGoogle Scholar
  127. Surani MA, Barton SC, Norris ML (1984) Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308:548–550.PubMedCrossRefGoogle Scholar
  128. Suzuki S, Renfree MB, Pask AJ, et al. (2005) Genomic imprinting of IGF2, p57(KIP2) and PEG1/MEST in a marsupial, the tammar wallaby. Mech Dev 122:213–222.PubMedCrossRefGoogle Scholar
  129. Suzuki S, Ono R, Narita T, et al. (2007) Retrotransposon silencing by DNA methylation can drive mammalian genomic imprinting. PLoS Genet 3:e55.PubMedCrossRefGoogle Scholar
  130. Takagi N, Sasaki M (1975) Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse. Nature 256:640–642.PubMedCrossRefGoogle Scholar
  131. Tremblay KD, Duran KL, Bartolomei MS (1997) A 5 2-kilobase-pair region of the imprinted mouse H19 gene exhibits exclusive paternal methylation throughout development. Mol Cell Biol 17:4322–4329.PubMedGoogle Scholar
  132. Ubeda F (2008) Evolution of genomic imprinting with biparental care: implications for Prader-Willi and Angelman syndromes. PLoS Biol 6:e208.PubMedCrossRefGoogle Scholar
  133. Vafiadis P, Bennett ST, Todd JA, et al. (1997) Insulin expression in human thymus is modulated by INS VNTR alleles at the IDDM2 locus. Nat Genet 15:289–292.PubMedCrossRefGoogle Scholar
  134. Varmuza S, Mann M (1994) Genomic imprinting–defusing the ovarian time bomb. Trends Genet 10:118–123.PubMedCrossRefGoogle Scholar
  135. Wake N, Takagi N, Sasaki M (1976) Non-random inactivation of X chromosome in the rat yolk sac. Nature 262:580–581.PubMedCrossRefGoogle Scholar
  136. Warren WC, Hillier LW, Graves JAM, et al. (2008) Genome analysis of the platypus reveals unique signatures of evolution. Nature 453:175–183.PubMedCrossRefGoogle Scholar
  137. Webster KE, O’Bryan MK, Fletcher S, et al. (2005) Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis. Proc Natl Acad Sci USA 102:4068–4073.PubMedCrossRefGoogle Scholar
  138. Weidman JR, Dolinoy DC, Maloney KA, Cheng JF, Jirtle RL (2006a). Imprinting of Opossum Igf2r in the absence of differential methylation and air. Epigenetics 1:49–54.PubMedCrossRefGoogle Scholar
  139. Weidman JR, Maloney KA, Jirtle RL (2006b). Comparative phylogenetic analysis reveals multiple non-imprinted isoforms of opossum Dlk1. Mamm Genome 17:157–167.PubMedCrossRefGoogle Scholar
  140. West JD, Frels WI, Chapman VM, Papaioannou VE (1977) Preferential expression of the maternally derived X chromosome in the mouse yolk sac. Cell 12:873–882.PubMedCrossRefGoogle Scholar
  141. Wilkins JF, Haig D (2003) What good is genomic imprinting: the function of parent-specific gene expression. Nat Rev Genet 4:359–368.PubMedCrossRefGoogle Scholar
  142. Yokomine T, Kuroiwa A, Tanaka K, et al. (2001) Sequence polymorphisms, allelic expression status and chromosome locations of the chicken IGF2 and MPR1 genes. Cytogenet Cell Genet 93:109–113.PubMedCrossRefGoogle Scholar
  143. Yokomine T, Hata K, Tsudzuki M, Sasaki H (2006) Evolution of the vertebrate DNMT3 gene family: a possible link between existence of DNMT3L and genomic imprinting. Cytogenet Genome Res 113:75–80.PubMedCrossRefGoogle Scholar
  144. Yotova IY, Vlatkovic IM, Pauler FM, et al. (2008) Identification of the human homolog of the imprinted mouse Air non-coding RNA. Genomics 92:464–473.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Timothy A. Hore
    • 1
  • Marilyn B. Renfree
    • 2
  • Andrew J. Pask
    • 3
    • 2
  • Jennifer A. Marshall Graves
    • 4
  1. 1.Laboratory of Developmental Genetics and ImprintingThe Babraham InstituteCambridgeUK
  2. 2.Department of Zoology, ARC Centre of Excellence for Kangaroo GenomicsThe University of MelbourneMelbourneAustralia
  3. 3.Department of Molecular and Cell BiologyUniversity of Connecticiut StorrsStorrsUSA
  4. 4.ARC Centre of Excellence for Kangaroo Genomics, Evolution, Ecology and Genetics, Research School of BiologyThe Australian National UniversityCanberraAustralia

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