Epigenetic and phenotypic consequences of a truncation disrupting the imprinted domain on distal mouse chromosome 7

Molecular and Cellular Biology

Volumn 28, Issue 3, 2008, Pages 1092-1103

  Oh, Rosemary ^a   Ho, Rita ^a   Mar, Lynn ^b   Gertsenstein, Marina ^c   Paderova, Jana ^d   Hsien, John ^c   Squire, Jeremy A ^d,e   Higgins, Michael J ^f   Nagy, Andras ^c   Lefebvre, Louis ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c MOUNT SINAI HOSPITAL   (Canada)

^d PRINCESS MARGARET HOSPITAL   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

^f ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RECOMBINASE;

ALLELE; ANIMAL CELL; ARTICLE; CHROMOSOME 7; CHROMOSOME BREAKAGE; CONTROLLED STUDY; DEVELOPMENT; EMBRYO; EMBRYONIC STEM CELL; EPIGENETICS; GENE CLUSTER; GENE EXPRESSION; GENE SILENCING; GENETIC CONSERVATION; GENETIC LINKAGE; GENOME IMPRINTING; HETEROZYGOTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

ALLELES; ANIMALS; CHROMOSOMES, MAMMALIAN; DNA METHYLATION; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; GENOMIC IMPRINTING; HETEROZYGOTE; MICE; PHENOTYPE; SEQUENCE DELETION;

EID: 38549176258     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01019-07     Document Type: Article

References (71)

1. Adams, D. J., P. J. Biggs, T. Cox, R. Davies, L. van der Weyden, J. Jonkers, J. Smith, B. Plumb, R. Taylor, I. Nishijima, Y. Yu, J. Rogers, and A. Bradley. 2004. Mutagenic insertion and chromosome engineering resource (MICER). Nat. Genet. 36:867-871.
2. Ainscough, J. F., T. Koide, M. Tada, S. Barton, and M. A. Surani. 1997. Imprinting of Igf2 and H19 from a 130 kb YAC transgene. Development 124:3621-3632.
3. Barnett, M. A., V. J. Buckle, E. P. Evans, A. C. Porter, D. Rout, A. G. Smith, and W. R. Brown. 1993. Telomere directed fragmentation of mammalian chromosomes. Nucleic Acids Res. 21:27-36.
4. Bartolomei, M. S., A. L. Webber, M. E. Brunkow, and S. M. Tilghman. 1993. Epigenetic mechanisms underlying the imprinting of the mouse H19 gene. Genes Dev. 7:1663-1673.
5. Bartolomei, M. S., S. Zemel, and S. M. Tilghman. 1991. Parental imprinting of the mouse H19 gene. Nature 351:153-155.
6. Bell, A. C., and G. Felsenfeld. 2000. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405:482-485.
7. Bock, C. 2005. BiQ Analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing. Bioinformatics 21:4067-4068.
8. Caspary, T., M. A. Cleary, C. C. Baker, X. J. Guan, and S. M. Tilghman. 1998. Multiple mechanisms regulate imprinting of the mouse distal chromosome 7 gene cluster. Mol. Cell. Biol. 18:3466-3474.
9. Cerrato, F., A. Sparago, I. Di Matteo, X. Zou, W. Dean, H. Sasaki, P. Smith, R. Genesio, M. Bruggemann, W. Reik, and A. Riccio. 2005. The two-domain hypothesis in Beckwith-Wiedemann syndrome: autonomous imprinting of the telomeric domain of the distal chromosome 7 cluster. Hum. Mol. Genet. 14:503-511.
10. Clark, S. J., J. Harrison, C. L. Paul, and M. Frommer. 1994. High sensitivity mapping of methylated cytosines. Nucleic Acids Res. 22:2990-2997.
11. Cleary, M. A., C. D. van Raamsdonk, J. Levorse, B. Zheng, A. Bradley, and S. M. Tilghman. 2001. Disruption of an imprinted gene cluster by a targeted chromosomal translocation in mice. Nat. Genet. 29:78-82.
12. Davis, T. L., J. M. Trasler, S. B. Moss, G. J. Yang, and M. S. Bartolomei. 1999. Acquisition of the H19 methylation imprint occurs differentially on the parental alleles during spermatogenesis. Genomics 58:18-28.
13. Day, C. D., N. J. Smilinich, G. V. Fitzpatrick, P. J. dejong, T. B. Shows, and M. J. Higgins. 1999. The imprinted domain in mouse distal chromosome 7: reagents for mutagenesis and sequencing. Mamm. Genome 10:182-185.
14. DeChiara, T. M., E. J. Robertson, and A. Efstratiadis. 1991. Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64:849-859.
15. Deltour, L., X. Montagutelli, J. L. Guenet, J. Jami, and A. Paldi. 1995. Tissue- and developmental stage-specific imprinting of the mouse proinsulin gene, Ins2. Dev. Biol. 168:686-688.
16. KIP2) is associated with hypomethylation at KvDMR1 in Beckwith-Wiedemann syndrome. J. Med. Genet. 40:797-801.
17. Duvillie, B., N. Cordonnier, L. Deltour, F. Dandoy-Dron, J. M. Itier, E. Monthioux, J. Jami, R. L. Joshi, and D. Bucchini. 1997. Phenotypic alterations in insulin-deficient mutant mice. Proc. Natl. Acad. Sci. USA 94:5137-5140.
18. Elson, D. A., and M. S. Bartolomei. 1997. A 5′ differentially methylated sequence and the 3′-flanking region are necessary for H19 transgene imprinting. Mol. Cell. Biol. 17:309-317.
19. Engemann, S., M. Strodicke, M. Paulsen, O. Franck, R. Reinhardt, N. Lane, W. Reik, and J. Walter. 2000. Sequence and functional comparison in the Beckwith-Wiedemann region: implications for a novel imprinting centre and extended imprinting. Hum. Mol. Genet. 9:2691-2706.
20. Fantl, V., G. Stamp, A. Andrews, I. Rosewell, and C. Dickson. 1995. Mice lacking cyclin D1 are small and show defects in eye and mammary gland development. Genes Dev. 9:2364-2372.
21. Farr, C., J. Fantes, P. Goodfellow, and H. Cooke. 1991. Functional reintroduction of human telomeres into mammalian cells. Proc. Natl. Acad. Sci. USA 88:7006-7010.
22. Farr, C. J., M. Stevanovic, E. J. Thomson, P. N. Goodfellow, and H. J. Cooke. 1992. Telomere-associated chromosome fragmentation: applications in genome manipulation and analysis. Nat. Genet. 2:275-282.
23. Feldman, B., W. Poueymirou, V. E. Papaioannou, T. M. DeChiara, and M. Goldfarb. 1995. Requirement of FGF-4 for postimplantation mouse development. Science 267:246-249.
24. Ferguson-Smith, A. C., H. Sasaki, B. M. Cattanach, and M. A. Surani. 1993. Parental-origin-specific modification of the mouse H19 gene. Nature 362:751-755.
25. Fitzpatrick, G. V., E. M. Pugacheva, J. Y. Shin, Z. Abdullaev, Y. Yang, K. Khatod, V. V. Lobanenkov, and M. J. Higgins. 2007. Allele-specific binding of CTCF to the multipartite imprinting control region KvDMR1. Mol. Cell. Biol. 27:2636-2647.
26. Fitzpatrick, G. V., P. D. Soloway, and M. J. Higgins. 2002. Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMR1. Nat. Genet. 32:426-431.
27. Friedrich, G., and P. Soriano. 1991. Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev. 5:1513-1523.
28. Fukushige, S., and B. Sauer. 1992. Genomic targeting with a positive-selection lox integration vector allows highly reproducible gene expression in mammalian cells. Proc. Natl. Acad. Sci. USA 89:7905-7909.
29. Giddings, S. J., C. D. King, K. W. Harman, J. F. Flood, and L. R. Carnaghi. 1994. Allele specific inactivation of insulin 1 and 2, in the mouse yolk sac, indicates imprinting. Nat. Genet. 6:310-313.
30. kip2 expression in vivo and in vitro: implications for Beckwith-Wiedemann syndrome. Proc. Natl. Acad. Sci. USA 97:5279-5284.
31. Guillemot, F., T. Caspary, S. M. Tilghman, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, D. J. Anderson, A. L. Joyner, J. Rossant, and A. Nagy. 1995. Genomic imprinting of Mash2, a mouse gene required for trophoblast development. Nat. Genet. 9:235-242.
32. Guillemot, F., A. Nagy, A. Auerbach, J. Rossant, and A. L. Joyner. 1994. Essential role of Mash-2 in extraembryonic development. Nature 371:333-336.
33. Hanish, J. P., J. L. Yanowitz, and T. de Lange. 1994. Stringent sequence requirements for the formation of human telomeres. Proc. Natl. Acad. Sci. USA 91:8861-8865.
34. Hardouin, N., and A. Nagy. 2000. Gene-trap-based target site for cre-mediated transgenic insertion. Genesis 26:245-252.
35. Hark, A. T., C. J. Schoenherr, D. J. Katz, R. S. Ingram, J. M. Levorse, and S. M. Tilghman. 2000. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405:486-489.
36. Hatada, I., and T. Mukai. 1995. Genomic imprinting of p57KIP2, a cyclin-dependent kinase inhibitor, in mouse. Nat. Genet. 11:204-206.
37. Itzhaki, J. E., M. A. Barnett, A. B. MacCarthy, V. J. Buckle, W. R. A. Brown, and A. C. G. Porter. 1992. Targeted breakage of a human chromosome mediated by cloned human telomeric DNA. Nat. Genet. 2:283.
38. Kaiser-Rogers, K. A., D. E. McFadden, C. A. Livasy, J. Dansereau, R. Jiang, J. F. Knops, L. Lefebvre, K. W. Rao, and W. P. Robinson. 2006. Androgenetic/biparental mosaicism causes placental mesenchymal dysplasia. J. Med. Genet. 43:187-192.
39. Kanduri, C., V. Pant, D. Loukinov, E. Pugacheva, C. F. Qi, A. Wolffe, R. Ohlsson, and V. V. Lobanenkov. 2000. Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Curr. Biol. 10:853-856.
40. Kato, M. V., Y. Ikawa, Y. Hayashizaki, and H. Shibata. 1998. Paternal imprinting of mouse serotonin receptor 2A gene Htr2 in embryonic eye: a conserved imprinting regulation on the RB/Rb locus. Genomics 47:146-148.
41. Lee, M. P., R. J. Hu, L. A. Johnson, and A. P. Feinberg. 1997. Human KVLQT1 gene shows tissue-specific imprinting and encompasses Beckwith-Wiedemann syndrome chromosomal rearrangements. Nat. Genet. 15:181-185.
42. Lefebvre, L., N. Dionne, J. Karaskova, J. A. Squire, and A. Nagy. 2001. Selection for transgene homozygosity in embryonic stem cells results in extensive loss of heterozygosity. Nat. Genet. 27:257-258.
43. Lefebvre, L., S. Viville, S. C. Barton, F. Ishino, E. B. Keverne, and M. A. Surani. 1998. Abnormal maternal behaviour and growth retardation associated with loss of the imprinted gene Mest. Nat. Genet. 20:163-169.
44. Lefebvre, L., S. Viville, S. C. Barton, F. Ishino, and M. A. Surani. 1997. Genomic structure and parent-of-origin-specific methylation of Peg1. Hum. Mol. Genet. 6:1907-1915.
45. Lewis, A., K. Mitsuya, D. Umlauf, P. Smith, W. Dean, J. Walter, M. Higgins, R. Feil, and W. Reik. 2004. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nat. Genet. 36:1291-1295.
46. Maher, E. R., and W. Reik. 2000. Beckwith-Wiedemann syndrome: imprinting in clusters revisited. J. Clin. Investig. 105:247-252.
47. Mancini-Dinardo, D., S. J. Steele, J. M. Levorse, R. S. Ingram, and S. M. Tilghman. 2006. Elongation of the Kcnq1ot1 transcript is required for genomic imprinting of neighboring genes. Genes Dev. 20:1268-1282.
48. Mansour, S. L., J. M. Goddard, and M. R. Capecchi. 1993. Mice homozygous for a targeted disruption of the proto-oncogene int-2 have developmental defects in the tail and inner ear. Development 117:13-28.
49. McLaughlin, K. J., H. Kochanowski, D. Solter, G. Schwarzkopf, P. E. Szabo, and J. R. Mann. 1997. Roles of the imprinted gene Igf2 and paternal duplication of distal chromosome 7 in the perinatal abnormalities of androgenetic mouse chimeras. Development 124:4897-4904.
50. McLaughlin, K. J., P. Szabo, H. Haegel, and J. R. Mann. 1996. Mouse embryos with paternal duplication of an imprinted chromosome 7 region die at midgestation and lack placental spongiotrophoblast. Development 122: 265-270.
51. Melton, D. A., P. A. Krieg, M. R. Rebagliati, T. Maniatis, K. Zinn, and M. R. Green. 1984. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 12:7035-7056.
52. Morison, I. M., M. R. Eccles, and A. E. Reeve. 2000. Imprinting of insulin-like growth factor 2 is modulated during hematopoiesis. Blood 96:3023-3028.
53. Nagy, A., M. Gertsenstein, K. Vintersten, and R. Behringer. 2003. Manipulating the mouse embryo: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
54. Nagy, A., J. Rossant, R. Nagy, W. Abramow-Newerly, and J. C. Roder. 1993. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA 90:8424-8428.
55. Negre, B., and A. Ruiz. 2007. HOM-C evolution in Drosophila: is there a need for Hox gene clustering? Trends Genet. 23:55-59.
56. Okabe, M., M. Ikawa, K. Kominami, T. Nakanishi, and Y. Nishimune. 1997. "Green mice" as a source of ubiquitous green cells. FEBS Lett. 407:313-319.
57. Pedram, M., C. N. Sprung, Q. Gao, A. W. Lo, G. E. Reynolds, and J. P. Murnane. 2006. Telomere position effect and silencing of transgenes near telomeres in the mouse. Mol. Cell. Biol. 26:1865-1878.
58. Qian, N., D. Frank, D. O'Keefe, D. Dao, L. Zhao, L. Yuan, Q. Wang, M. Keating, C. Walsh, and B. Tycko. 1997. The IPL gene on chromosome 11p15.5 is imprinted in humans and mice and is similar to TDAG51, implicated in Fas expression and apoptosis. Hum. Mol. Genet. 6:2021-2029.
59. Salas, M., R. John, A. Saxena, S. Barton, D. Frank, G. Fitzpatrick, M. J. Higgins, and B. Tycko. 2004. Placental growth retardation due to loss of imprinting of Phlda2. Mech. Dev. 121:1199-1210.
60. Sauer, B., M. Whealy, A. Robbins, and L. Enquist. 1987. Site-specific insertion of DNA into a pseudorabies virus vector. Proc. Natl. Acad. Sci. USA 84:9108-9112.
61. Searle, A. G., and C. V. Beechey. 1990. Genome imprinting phenomena on mouse chromosome 7. Genet. Res. 56:237-244.
62. Smilinich, N. J., C. D. Day, G. V. Fitzpatrick, G. M. Caldwell, A. C. Lossie, P. R. Cooper, A. C. Smallwood, J. A. Joyce, P. N. Schofield, W. Reik, R. D. Nicholls, R. Weksberg, D. J. Driscoll, E. R. Maher, T. B. Shows, and M. J. Higgins. 1999. A maternally methylated CpG island in KvLQT1 is associated with an antisense paternal transcript and loss of imprinting in Beckwith-Wiedemann syndrome. Proc. Natl. Acad. Sci. USA 96:8064-8069.
63. Smith, R. J., P. Arnaud, G. Konfortova, W. L. Dean, C. V. Beechey, and G. Kelsey. 2002. The mouse Zac1 locus: basis for imprinting and comparison with human ZAC. Gene 292:101-112.
64. Sprung, C. N., G. E. Reynolds, M. Jasin, and J. P. Murnane. 1999. Chromosome healing in mouse embryonic stem cells. Proc. Natl. Acad. Sci. USA 96:6781-6786.
65. Srivastava, M., S. Hsieh, A. Grinberg, L. Williams-Simons, S. P. Huang, and K. Pfeifer. 2000. H19 and Igf2 monoallelic expression is regulated in two distinct ways by a shared eis acting regulatory region upstream of H19. Genes Dev. 14:1186-1195.
66. Thorvaldsen, J. L., K. L. Duran, and M. S. Bartolomei. 1998. Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev. 12:3693-3702.
67. Tremblay, K. D., J. R. Saam, R. S. Ingram, S. M. Tilghman, and M. S. Bartolomei. 1995. A paternal-specific methylation imprint marks the alleles of the mouse H19 gene. Nat. Genet. 9:407-413.
68. Umlauf, D., Y. Goto, R. Cao, F. Cerqueira, A. Wagschal, Y. Zhang, and R. Feil. 2004. Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes. Nat. Genet. 36:1296-1300.
69. Verona, R. I., M. R. Mann, and M. S. Bartolomei. 2003. Genomic imprinting: intricacies of epigenetic regulation in clusters. Annu. Rev. Cell Dev. Biol. 19:237-259.
70. Wright, T. J., R. Ladher, J. McWhirter, C. Murre, G. C. Schoenwolf, and S. L. Mansour. 2004. Mouse FGF15 is the ortholog of human and chick FGF19, but is not uniquely required for otic induction. Dev. Biol. 269:264-275.
71. Yeh, W. C., J. L. Pompa, M. E. McCurrach, H. B. Shu, A. J. Elia, A. Shahinian, M. Ng, A. Wakeham, W. Khoo, K. Mitchell, W. S. El-Deiry, S. W. Lowe, D. V. Goeddel, and T. W. Mak. 1998. FADD: essential for embryo development and signaling from some, but not all, inducers of apoptosis. Science 279:1954-1958.