The regulation and biological significance of genomic imprinting in mammals

Journal of Biochemistry

Volumn 133, Issue 6, 2003, Pages 699-711

  Kaneko Ishino, Tomoko ^a,b   Kohda, Takashi ^b   Ishino, Fumitoshi ^b,c  

^a TOKAI UNIVERSITY   (Japan)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Complementation hypothesis; Development; Evolution; Genomic imprinting; Parental imprinting; Peg and Meg; Placenta hypothesis

Indexed keywords

CELL AGING; CELL LINEAGE; CELL PROTECTION; COMPLEMENTATION HYPOTHESIS; DEVELOPMENT; EVOLUTION; GENDER; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENOME IMPRINTING; GERM CELL; HYPOTHESIS; INHERITANCE; MAMMAL; MEG GENE; MOLECULAR GENETICS; NON MENDELIAN INHERITANCE; NONHUMAN; OOCYTE; PARENTAL IMPRINTING; PARTHENOGENESIS; PEG GENE; PLACENTA; PLACENTA HYPOTHESIS; REVIEW; SOMATIC CELL; SPERM; TROPHOBLASTIC DISEASE;

ANIMALS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOMIC IMPRINTING; HUMANS; MALE; SEX CHARACTERISTICS;

MAMMALIA;

EID: 0042311441     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/jb/mvg090     Document Type: Review

References (87)

1. Surani, M.A., Barton, S.C., and Norris, M.L. (1984) Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308, 548-550
2. McGrath, J. and Solter, D. (1984) Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37, 179-183
3. Cattanach, B.M. and Kirk, M. (1985) Differential activity of maternally and paternally derived chromosome regions in mice. Nature 315, 496-498
4. Beechey, C.V., Cattanach, B.M., and Searl, R.L. (2000) Mouse imprinting data and references. MRC Mammalian Genetics Unit [online] «http://www.mg-u.har.mrc.ac.uk/imprinting/imprinting.html»
5. Ledbetter, D.H. and Engel, E. (1995) Uniparental disomy in humans: development of an imprinting map and its implications for prenatal diagnosis. Hum. Mol. Genet. 4, 1757-1764
6. DeChiara, T.M., Robertson E.J., and Efstratiadis, A. (1991) Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64, 849-859
7. Barlow, D.P., Stoger, R., Hermann, B.C., Saito, K., and Schweifer, N. (1991) The mouse insulin-like growth factor type 2 receptor is imprinted and closely linked to the Tme locus. Nature 349, 84-87
8. Bartolomei, M.S., Zemel, S., and Tilghman, S.M. (1991) Parental imprinting of the mouse H19 gene. Nature 351, 153-155
9. Nakao, M. and Sasaki, H. (1996) Genomic imprinting: significance in development and diseases and the molecular mechanisms. J. Biochem. 120, 467-473
10. Reik, W. and Walter, J. (2001) Genomic imprinting: parental influence on the genome. Nat. Rev. Genet. 2, 21-32
11. Hayashizaki, Y., Shibata, H., Hirotsune, S., Sugino, H., Okazaki, Y., Sasaki, N., Hirose, K., Imoto, H., Okuizumi, H., Muramatsu, M., Komatsubara, H., Shiroishi, T., Moriwaki, K., Katsuki, M., and Chapman, V.M. (1994) Identification of an imprinted U2af binding-protein-related sequence on mouse chromosome 11 using the RLGS method. Nat. Genet. 6, 33-40
12. Mizuno, Y., Sotomaru, Y., Katsuzawa, Y., Kono, T., Meguro, M., Oshimura, M., Kawai, J., Tomaru, Y., Kiyosawa, H., Nikaido, I., Amanuma, H., Hayashizaki, Y., and Okazaki, Y. (2002) Asb4, Ata3, and Dcn are novel imprinted genes identified by high-throughput screening using RIKEN cDNA microarray. Biochem. Biophys. Res. Commun. 290, 1499-1505
13. Kelsey, G., Bodle, D., Miller, H.J., Beechey, C.V., Coombes, C., Peters, J., and Williamson, C.M. (1999) Identification of imprinted loci by methylation-sensitive representational difference analysis: application to mouse distal chromosome 2. Genomics 62, 129-138
14. Hatada, I., Morita, S., Obata, Y., Sotomaru, Y., Shimoda, M., and Kono, T. (2001) Identification of a new imprinted gene, Rian, on mouse chromosome 12 by fluorescent differential display screening. J. Biochem. 130, 187-90
15. Kaneko-Ishino, T., Kuroiwa, Y., Miyoshi, Y., Kohda, T., Suzuki, R., Yokoyama, M., Viville, S., Barton, S.C., Ishino F., and Surani, A. (1995) Peg1/Mest imprinted gene on chromosome 6 identified by cDNA subtraction hybridization. Nat. Genet. 11, 52-59
16. Kuroiwa, Y., Kaneko-Ishino, T., Kagitani, F., Kohda, T., Li, L-L., Tada, M., Suzuki, R., Yokoyama, M., Shiroishi, T., Wakana, S., Barton, S.C., Ishino F., and Surani, A. (1996) Peg3 imprinted gene on proximal chromosome 7 encodes for a zinc finger protein. Nat. Genet. 12, 186-190
17. Miyoshi, N., Kuroiwa, Y., Kohda, T., Shitara, H., Yonekawa, H., Kawabe, T., Hasegawa, H., Barton, S.C., Surani, M.A., Kaneko-Ishino, T., and Ishino, F. (1998) Identification of the Meg1/Grb10 imprinted gene on mouse proximal chromosome 11, a candidate for the Silver-Russell syndrome gene. Proc. Natl Acad. Sci. USA 95, 1102-1107
18. Kobayashi, S., Wagatsuma, H., Ono, R., Ichikawa, H., Yamazaki, M., Tashiro, H., Aisaka, K., Miyoshi, N., Kohda, T., Ogura, A., Ohki, M., Kaneko-Ishino, T., and Ishino, F. (2000) Mouse Peg9/Dlk1 and human PEG9/DLK1 are paternally expressed imprinted genes closely located to the maternally expressed imprinted genes: mouse Meg3/Gt12 and human MEG3. Genes Cells 5, 1029-1037
19. Kono, T., Obata, Y., Yoshimizu, T., Nakahara, T., and Carroll, J. (1996) Epigenetic modifications during oocyte growth correlates with extended parthenogenetic development in the mouse. Nat. Genet. 13, 91-94
20. Obata, Y., Kaneko-Ishino, T., Koide, T., Takai, Y., Ueda, T., Domeki, I., Shiroishi, T., Ishino F., and Kono, T. (1998) Disruption of primary imprinting during oocyte growth leads to the modified expression of imprinted genes during embryogenesis. Development 125, 1553-1560
21. Obata, Y. and Kono, T. (2002) Maternal primary imprinting is established at a specific time for each gene throughout oocyte growth. J. Biol. Chem. 277, 5285-5289
22. Kafri, T., Ariel, M., Brandeis, M., Shemer, R., Urven, L., McCarrey, J., Ceder, H., and Razin, A. (1992) Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes Dev. 6, 705-714
23. Szabo, P.E. and Mann, J.R. (1995) Biallelic expression of imprinted genes in the mouse germ line: implications for erasure, establishment, and mechanism of genomic imprinting. Genes Dev. 9, 1857-1868
24. Labosky, P.A., Barlow, D.P., and Hogan, B.L. (1994) Mouse embryonic germ (EG) cell lines; transmission through the germline and differences in the methylation imprint of insulin-like growth factor 2 receptor (Igf2r) gene compared with embryonic stem (ES) cell lines. Development 120, 3195-3205
25. Tada, T., Tada, M., Hilton, K., Sado, T., Takagi, N., and Surani, M.A. (1998) Epigenotype switching of imprintable loci in embryonic germ cells. Dev. Genes Evol. 207, 551-561
26. Kato, Y., Rideout, W.M., Hilton, K., Barton, S.C., Tsunoda, Y., and Surani, M.A. (1999) Developmental potential of mouse primordial germ cells. Development 126, 1823-1832
27. Lee, J., Inoue, K., Ono, R., Ogonuki, N., Kohda, T., Kaneko-Ishino, T., Ogura, A., and Ishino, F. (2002) Erasing genomic imprinting memory in mouse clone embryos produced from day 11.5 primordial germ cells. Development, 129, 1807-1817
28. Molyneau, K.A., Stallock, J., Schaible, K., and Wylie, C. (2001) Time-lapse analysis of living mouse germ cell migration. Dev. Biol. 240, 488-498
29. Santos, F., Hendrich, B., Reik, W., and Dean, W. (2002) Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev. Biol. 241, 172-182
30. Li, E., Beard, C., and Jaenisch, R. (1993) Role for DNA methylation in genomic imprinting. Nature 366, 362-365
31. Tanaka, M., Puchyr, M., Gertsenstein, M., Harpal, K., Jaenisch, R., Rossant, J., and Nagy, A. (1999) Parental origin-specific expression of Mash2 is established at the time of implantation with its imprinting mechanism highly resistant to genome-wide demethylation. Mech. Dev. 87, 129-142
32. Caspary, T., Cleary, M.A., Backer, C.C., Guan, X.J., and Tilghman, S.M. (1998) Multiple mechanisms regulate imprinting of the mouse distal chromosome 7 gene cluster. Mol. Cell. Biol. 18, 3466-3474
33. Bourc'his, D., Xu, G.L., Lin, C.S., Bollman, B., and Bestor, T.H. (2001) Dnmt31 and the establishment of maternal genomic imprints. Science 294, 2536-2539
34. Hata, K., Okano, M., Lei, H., and Li, E. (2002) Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129, 1983-1993
35. Okano, M., Bell, D.W., Haber, D.A., and Li, E. (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257
36. Judson, H., Hayward, B.E., Sheridan, E., and Bonthron, D.B. (2002) A global disorder of imprinting in the human female germ line. Nature 416, 539-542
37. Thorvaldsen, J.L., Duran, K.L., and Bartolomei, M.S. (1998) Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev. 12, 3693-3702
38. Hark, A.T., Schoenherr, C.J., Katz, D.J., Ingram, R.S., Levorse, J.M., and Tilghman, S.M. (2000) CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405, 486-489
39. Bell, A.C. and Fesenfeld, G. (2000) Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405, 482-485
40. Ripoche, M.A., Kress, C., Poirier, F., and Dandolo, L. (1997) Deletion of the H19 transcription unit reveals the existence of a putative imprinting control element. Genes Dev. 11, 1596-1604
41. Hitchins, M.P., Monk, D., Bell, G.M., Ali, Z., Preece, M.A., Stanier, P., and Moore, G.E. (2001) Maternal repression of the human GRB10 gene in the developing central nervous system; evaluation of the role for GRB10 in Silver-Russell syndrome. Eur. J. Hum. Genet. 9, 82-90
42. Hikichi, T., Kohda, T., Kaneko-Ishino, T., and Ishino, F. (2003) Imprinting regulation of the murine Meg1/Grb10 and human GRB10 genes; roles of brain-specific promoters and mouse-specific CTCF-binding sites. Nucleic Acids Res. 31, 1398-1406
43. Blagitko, N., Mergenthaler, S., Schulz, U., Wollmann, H.A., Craigen, W., Eggermann, T., Ropers, H.H., and Kalscheuer, V.M. (2000) Human GRB10 is imprinted and expressed from the paternal and maternal allele in a highly tissue- and isoform-specific fashion. Hum. Mol. Genet. 9, 1587-1595
44. Hitchins, M.P., Bentley, L., Monk, D., Beechey, C., Peters, J., Kelsey, G., Ishino, F., Preece, M.A., Stanier, P., and Moore, G.E. (2003) DDC and COBL, flanking the imprinted GRB10 gene on 7p12, are biallelically expressed. Mamm. Genome 13, 686-691
45. Sleutels, F., Zwart, R., and Barlow, D.P. (2002) The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 415, 810-813
46. Okazaki, Y., Furuno, M., Kasukawa, T., Adachi, J., Bono, H., Kondo, S., Nikaido, I., Osato, N., Saito, R., Suzuki, H. et al. (2002) Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 420, 563-573
47. Runte, M., Hütternhofer, A., Gross, S., Kiefmann, M., Horsthemke, B., and Buiting, K. (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
48. Cavaille, J., Paulsen, M., Ferguson-Smith, A., and Bachellerie, J-P. (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
49. Moore, T. and Haig, D. (1991) Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet. 7, 45-49
50. Lefebvre, L., Viville, S., Barton, S.C., Ishino, F., Keverne, E.B., and Surani, M.A. (1998) Abnormal maternal behaviour and growth retardation associated with loss of the imprinted gene Mest. Nat. Genet. 20, 163-169
51. Constancia, M., Hemberger, M., Hughes, J., Dean, W., Ferguson-Smith, A., Fundele, R., Stewart, F., Kelsey, G., Fowden, A., Sibley, C. and Reik, W. (2002) Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417, 945-948
52. Li, L-L., Keverne, E.B., Aparicio, S.A., Ishino, F., Barton, S.C. and Surani, M.A. (1999) Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science 284, 330-333
53. Moon, Y.S., Smas, C.M., Lee, K., Villena, J.A., Kim, K.H., Yun, E.J., and Sul, H.S. (2002) Mice lacking paternally expressed Pref-1/Dlk1 display growth retardation and accelerated adiposity. Mol. Cell. Biol. 22, 5585-5592
54. Itier, J., Tremp, G., Leonard, J., Multon, M., Ret, G., Schweighoffer, F., Tocque, B., Bluet-Pajot, M., Cormier, V., and Dautry, F. (1998) Imprinted gene in postnatal growth role. Nature 393, 125-126
55. Hernandez, A., Fiering, S., Martinez, E., Galton, V.A., and St Germain, D. (2002) The gene locus encoding iodothyronine deiodinase type 3 (Dio3) is imprinted in the fetus and expresses antisense transcripts. Endocrinology 143, 4483-4486
56. Wang, Z.Q., Fung, M.R., Barlow, D.P., and Wagner, E.F. (1994) Regulation of embryonic growth and lysosomal targeting by the imprinted Igf2/Mpr gene. Nature 372, 464-467
57. Solter, D. (1988) Differential imprinting and expression of maternal and paternal genomes. Annu. Rev. Genet. 22, 127-146
58. Varmuza, S. and Mann, M. (1994) Genomic imprinting - defusing the ovarian time bomb. Trends Genet. 10, 118-123
59. Barlow, D.P. (1993) Methylation and imprinting: from host defense to gene regulation? Science, 260, 309-310
60. Yoder, J.A., Walsh, C.P., and Bestor, T.H. (1997) Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 12, 469-472
61. Ono, R., Kobayashi, S., Wagatsuma, H., Aisaka, K., Kohda, T., Kaneko-Ishino, T., and Ishino, F. (2001) A retrotransposon-derived gene, Peg10, is a novel imprinted gene located on human chromosome 7q21. Genomics 73, 232-237
62. Charlier, C., Segers, K., Wagenaar, D., Karim, L., Berghmans, S., Jaillon, O., Shay, T., Weissenbach, J., Cockett, N., Gyapay, G., and Georges, M. (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. 5, 850-862
63. Gerard, M., Hernandez, L., Wevrick, R., and Stewart, C.L. (1999) Disruption of the mouse necdin gene results in early post-natal lethality. Nat. Genet. 23, 199-202
64. Muscatelli, F., Abrous, D.N., Massacrier, A., Boccaccio, I., Le Moal, M., Cau, P., and Cremer, H. (2000) Disruption of the mouse Necdin gene results in hypothalamic and behavioral alterations reminiscent of the human Prader-Willi syndrome. Hurn. Mol. Genet. 9, 3101-3110
65. Ludwig, T., Eggenschwiler, J., Fisher, P., D'Ercole, A.J., Davenport, M.L., and Efstratiadis, A. (1996) Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Dev. Biol. 177, 517-535.
66. Zhang, P., Liegeois, N.J., Wong, C., Finegold, M., Hou, H., Thompson, J.C., Silverman, A., Harper, J.W., DePinho, R.A., and Elledge, S.J. (1997) Altered cell differentiation and proliferation in mice lacking p57KIP2 indicates a role in Beckwith-Wiedemann syndrome. Nature 387, 151-158
67. Yan, Y., Frisen, J., Lee, M.H., Massague, J., and Barbacid, M. (1997) Ablation of the CDK inhibitor p57Kip2 results in increased apoptosis and delayed differentiation during mouse development. Genes Dev. 11, 973-983
68. Guillemot, F., Caspary, T., Tilghman, S.M., Copeland, N.G., Gilbert, D.J., Jenkins, N.A., Anderson, D.J., Joyner, A.L., Rossant, J., and Nagy, A. (1995) Genomic imprinting of Mash2, a mouse gene required for trophoblast development. Nat. Genet. 9, 235-242
69. Hall, J.G. (1990) Genomic imprinting: review and relevance to human diseases. Amer. J. Hum. Genet. 46, 857-873
70. O'Neill, M.J., Ingram, R.S., Vrana, P.B., and Tilghman, S.M. (2000) Allelic expression of IGF2 in marsupials and birds. Dev. Genes Evol. 210, 18-20
71. Killian, J.K., Byrd, J.C., Jirtle, J.V., Munday, B.L., Stoskopf, M.K., MacDonald, R.G., and Jirtle, R.L. (2000) M6P/IGF2R imprinting evolution in mammals. Mol. Cell 5, 707-716
72. Killian, J.K., Nolan, C.M., Stewart, N., Munday, B.L., Andersen, N.A., Nicol, S., and Jirtle, R.L. (2001) Monotreme IGF2 expression and ancestral origin of genomic imprinting. J. Exp. Zool. 291, 205-212
73. Nolan, C.M., Killian, J.K., Petitte, J.N., and Jirtle, R.L. (2001) Imprint status of M6P/IGF2R and IGF2 in chickens. Dev. Genes Evol. 211, 179-183
74. Kuroiwa, Y. (1997) Systematic screening and analysis of paternally expressed imprited genes. Doctoral thesis; Tokyo Institute of Technology, Japan.
75. Schuster-Gossler, K., Bilinski, P., Sado, T., Ferguson-Smith, A., and Gossler, A. (1998) The mouse Gtl2 gene is differentially expressed during embryonic development, encodes multiple alternatively spliced transcripts, and may act as an RNA. Dev. Dyn. 212, 214-28
76. Leff, S.E., Brannan, C.I., Reed, M.L., Ozcelik, T., Francke, U., Copeland, N.G., and Jenkins, N.A. (1992) Maternal imprinting of the mouse gene and conserved linkage homology with the human Prader-Willi syndrome region. Nat. Genet. 2, 259-264
77. Kagitani, F., Kuroiwa, Y., Wakana, S., Shiroishi, T., Kobayashi, S., Kohda, T., Kaneko-Ishino, T., and Ishino, F. (1997) Peg5/Neuronatin is an imprinted gene located on sub-distal chromosome 2 in the mouse. Nucleic Acids Res. 25, 428-432
78. Moore, T., Constancia, M., Zubair, M., Bailleul, B., Feil, R., Sasaki, H., and Reik, W. (1997) Multiple imprinted sense and antisense transcripts, differential methylation and tandem repeats in a putative imprinting control region upstream of mouse Igf2. Proc. Natl Acad. Sci. USA 94, 12509-12514
79. Okutsu, T., Kuroiwa, Y., Kagitani, F., Kai, M., Aisaka, K., Tsutsumi, O., Kaneko, Y., Yokomori, K., Surani, M.A., Kohda, T., Kaneko-Ishino, T., and Ishino F. (2000) Expression and imprinting status of human PEG8/IGF2AS, a paternally expressed antisense transcript from the IGF2 locus, in Wilms' tumors. J. Biochem. 127, 475-483
80. kip2 in trophoblast giant cells defines G2-like gap phase of the endocycle. Mol. Biol. Cell 11, 1039-1045
81. Frank, D., Fortino, W., Clark, L., Musalo, R., Wang, W., Saxena, A., Li, C.M., Reik, W., Ludwig, T., and Tycko, B. (2002) Placental overgrowth in mice lacking the imprinted gene Ipl. Proc. Natl Acad. Sci. USA 99, 7490-7495
82. Constancia, M., Hemberger, M., Hughes, J., Dean, W., Ferguson-Smith, A., Fundele, R., Stewart, F., Kelsey, G., Fowden, A., Sibley, C., and Reik, W. (2002) Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417, 945-948
83. Marahrens, Y., Panning, B., Dausman, J., Strauss, W., and Jaenisch, R. (1997) Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Genes Dev. 11, 156-166
84. Takagi, N. and Sasaki, M. (1975) Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse. Nature 256, 640-642
85. Ueda, T., Abe, K., Miura, A., Yuzuriha, M., Zubair, M., Noguchi, M., Niwa, K., Kawase, Y., Kono, T., Matsuda, Y., Fujimoto, H., Shibata, H., Hayashizaki, Y., and Sasaki, H. (2000) The paternal methylation imprint of the mouse H19 locus is acquired in the gonocyte stage during foetal testis development. Genes Cells 5, 649-659
86. Davis, T.L., Yang, G.J., McCarrey, J.R., and Bartolomei, M.S. (2000) The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum. Mol. Genet. 9, 2885-2894
87. Kim, J., Kollhoff, A., Bergmann, A., and Stubbs, L. (2003) Methylation-sensitive binding of transcription factor YY1 to an insulator sequence within the paternally expressed imprinted gene, Peg3. Hum. Mol. Genet. 12, 233-245