Gene repeat expansion and contraction by spontaneous intrachromosomal homologous recombination in mammalian cells

Nucleic Acids Research

Volumn 32, Issue 3, 2004, Pages 1184-1196

  Read, L R ^a   Raynard, Steven J ^b   Rukść, Ania ^b   Baker, Mark D ^a,b  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN MU CHAIN; REPETITIVE DNA;

ACCURACY; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; GENE CONVERSION; GENE INTERACTION; GENE LOCUS; GENE STRUCTURE; GENETIC RECOMBINATION; HAPLOIDY; HOMOLOGOUS RECOMBINATION; HYBRIDOMA CELL CULTURE; MAMMAL CELL; MOUSE; NONHUMAN; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SISTER CHROMATID; TANDEM REPEAT; ANIMAL; CHROMOSOME; GENE DUPLICATION; GENETICS; HYBRIDOMA; IMMUNOGLOBULIN CONSTANT REGION;

MAMMALIA;

ANIMALS; CHROMOSOMES, MAMMALIAN; DNA REPEAT EXPANSION; GENE DUPLICATION; HYBRIDOMAS; IMMUNOGLOBULIN CONSTANT REGIONS; IMMUNOGLOBULIN MU-CHAINS; MICE; RECOMBINATION, GENETIC; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 2342576180     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkh280     Document Type: Article

References (80)

1. Pâques,F. and Haber,J.E. (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev., 63, 349-404.
2. Rouet,P., Smih,F. and Jasin,M. (1994) Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol. Cell. Biol., 14, 8096-8106.
3. Sargent,R.G., Brenneman,M.A. and Wilson,J.H. (1997) Repair of site-specific double-strand breaks in a mammalian chromosome by homologous and illegitimate recombination. Mol. Cell. Biol., 17, 267-277.
4. Liang.F., Han,M., Romanienko,P.J. and Jasin,M. (1998) Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc. Natl Acad. Sci. USA, 95, 5172-5177.
5. Takata,M., Sasaki,M.S., Sonoda,E., Morrison,C., Hashimoto,M., Utsumi,H., Yamaguchi-Iwai,Y., Shinohara,A. and Takeda,S. (1998) Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J., 17, 5497-5508.
6. Lin,Y., Lukacsovich,T. and Waldman,A.S. (1999) Multiple pathways of repair of DNA double-strand breaks in mammalian chromosomes. Mol. Cell. Biol., 19, 8353-8360.
7. Richardson,C. and Jasin,M. (2000) Coupled homologous and nonhomologous repair of a double-strand break preserves genomic integrity in mammalian cells. Mol. Cell. Biol., 20, 9068-9075.
8. Lin,F.L. and Sternberg,N. (1984) Homologous recombination between overlapping thymidine kinase gene fragments stably inserted into a mouse cell genome. Mol. Cell. Biol., 4, 852-861.
9. Lin,F.L., Sperle,K. and Sternberg, N. (1984) Model for homologous recombination during transfer of DNA into mouse L cells: role for DNA ends in the recombination process. Mol. Cell. Biol., 4, 1020-1034.
10. Fishman-Lobell,J., Rudin,N. and Haber,J.E. (1992) Two alternative pathways of double-strand break repair that are kinetically separable and independently modulated. Mol. Cell. Biol., 12, 1292-1303.
11. Belmaaza,A. and Chartrand,P. (1994) One-sided invasion events in homologous recombination at double-strand breaks. Mutat. Res., 314, 199-208.
12. Johnson,R.D. and Jasin,M. (2000) Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J., 19, 3398-3407.
13. Allers,T. and Lichten,M. (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell, 106, 47-57.
14. Cromie,G.A. and Leach,D.R. (2000) Control of crossing over. Mol. Cell., 6, 815-826.
15. Kraus,E., Leung,W.Y. and Haber,J.E. (2001) Break-induced replication: a review and an example in budding yeast. Proc. Natl Acad. Sci. USA, 98, 8255-8262.
16. Hunter,N. and Kleckner,N. (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination. Cell, 106, 59-70.
17. Orr-Weaver,T.L., Szostak,J.W. and Rothstein,R.J. (1981) Yeast transformation: a model system for the study of recombination. Proc. Natl Acad. Sci. USA, 78, 6354-6358.
18. Szostak,J.W., Orr-Weaver,T.L., Rothstein,R.J. and Stahl,F.W. (1983) The double-strand-break repair model for recombination. Cell, 33, 25-35.
19. Schwacha,A. and Kleckner,N, (1994) Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell, 76, 51-63.
20. Schwacha,A. and Kleckner,N. (1995) Identification of double Holliday junctions as intermediates in meiotic recombination. Cell, 83, 783-791.
21. Baker,M.D. and Birmingham,E.C. (2001) Evidence for biased Holliday junction cleavage and mismatch repair directed by junction cuts during double-strand-break repair in mammalian cells. Mol. Cell. Biol., 21, 3425-3435.
22. Gilbertson,L.A. and Stahl,F.W. (1996) A test of the double-strand break repair model for meiotic recombination in Saccharomyces cerevisiae. Genetics, 144, 27-41.
23. Foss,H.M., Hillers,K.J. and Stahl,F.W. (1999) The conversion gradient at HIS4 of Saccharomyces cerevisiae. II. A role for mismatch repair directed by biased resolution of the recombinational intermediate. Genetics, 153, 573-583.
24. Belmaaza,A., Wallenburg,J.C., Brouillette,S., Gusew,N. and Chartrand,P. (1990) Genetic exchange between endogenous and exogenous LINE-1 repetitive elements in mouse cells. Nucleic Acids Res., 18, 6385-6391.
25. Adair,G.M., Nairn,R.S., Wilson,J.H., Seidman,M.M., Brotherman,K.A., MacKinnon,C. and Scheerer,J.B. (1989) Targeted homologous recombination at the endogenous adenine phosphoribosyltransferase locus in Chinese hamster cells. Proc. Natl Acad. Sci. USA, 86, 4574-4578.
26. Ellis,J. and Bernstein,A. (1989) Gene targeting with retroviral vectors: recombination by gene conversion into regions of nonhomology. Mol. Cell. Biol., 9, 1621-1627.
27. Mudgett,J.S. and Taylor,W.D. (1990) Recombination between irrandiated shuttle vector DNA and chromosomal DNA in African green monkey kidney cells. Mol. Cell. Biol., 10, 37-46.
28. McCulloch,R.D., Read,L.R. and Baker,M.D. (2003) Strand invasion and DNA synthesis from the two 3′ ends of a double-strand break in mammalian cells. Genetics, 163, 1439-1447.
29. Köhler,G. and Shulman,M.J. (1980) Immunoglobulin M mutants. Eur. J. Immunol., 10, 467-476.
30. Köhler,G., Potash,M.J., Lehrach,H. and Shulman,M.J. (1982) Deletions in immunoglobulin mu chains. EMBO J., 1, 555-563.
31. Baker,M.D., Pennell,N., Bosnoyan,L. and Shulman,M.J. (1988) Homologous recombination can restore normal immunoglobulin production in a mutant hybridoma cell line. Proc. Natl Acad. Sci. USA, 85, 6432-6436.
32. Li,J. and Baker,M.D. (2000) Use of a small palindrome genetic marker to investigate mechanisms of double-strand-break repair in mammalian cells. Genetics, 154, 1281-1289.
33. Goldberg,G.I., Vanin,E.F., Zrolka,A.M. and Blattner,F.R. (1981) Sequence of the gene for the constant region of the p chain of Balb/c mouse immunoglobulin. Gene, 15, 33-42.
34. Gross-Bellard,M., Qudet,P. and Chambon,P. (1973) Isolation of high-molecular weight DNA from mammalian cells. Eur. J. Biochem., 36, 32-38.
35. Sambrook,J., Fritsch,E.F. and Maniatis,T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Ng,P. and Baker,M.D. (1999) Mechanisms of double-strand-break repair during gene targeting in mammalian cells. Genetics, 151, 1127-1141.
37. Nag,D.K., White,M.A. and Petes,T.D. (1989) Palindromic sequences in heteroduplex DNA inhibit mismatch repair in yeast. Nature, 340, 318-320.
38. Bollag,R.J. and Liskay,R.M. (1991) Direct-repeat analysis of chromatid interactions during intrachromosomal recombination in mouse cells. Mol. Cell. Biol., 11, 4839-4845.
39. Donoho,G., Jasin,M. and Berg,P. (1998) Analysis of gene targeting and intrachromosomal homologous recombination stimulated by genomic double-strand breaks in mouse embryonic stem cells. Mol. Cell. Biol., 18, 4070-4078.
40. Esposito,M.S. (1981) Postmeiotic segregation in Saccharomyces. Mol. Gen. Genet., 11, 297-299.
41. Ronne,H. and Rothstein,R. (1988) Mitotic sectored colonies: evidence of heteroduplex DNA formation during direct repeat recombination. Proc. Natl Acad. Sci. USA, 85, 2696-2700.
42. Ng,P. and Baker,M.D. (1999) The molecular basis of multiple vector insertion by gene targeting in mammalian cells. Genetics, 151, 1143-1155.
43. Baker,M.D. (1989) High-frequency homologous recombination between duplicate chromosomal immunoglobulin μ heavy chain constant regions. Mol. Cell. Biol., 9, 5500-5507.
44. Baker,M.D. and Read,L.R. (1995) High-frequency gene conversion between repeated Cμ sequences integrated at the chromosomal immunoglobulin μ locus in mouse hybridoma cells. Mol. Cell. Biol., 15, 766-771.
45. Liskay,R.M., Stachelek,J.L. and Letsou,A. (1984). Homologous recombination inbetween repeated chromosomal sequences in mouse cells. Cold Spring Harbor Symp. Quant. Biol., 49, 183-189.
46. Smith,A.J.H. and Berg,P. (1984) Homologous recombination between defective neo genes in mouse 3T6 cells. Cold Spring Harbor Symp. Quant. Biol., 49, 171-181.
47. Subramani,S. and Rubnitz,J. (1985) Recombination events after transient infection and stable integration into mouse cells. Mol. Cell. Biol., 5, 659-666.
48. Hasty,P., Ramirez-Solis,R., Krumlauf,R. and Bradley,A. (1991) Introduction of a subtle mutation into the Hox-2.6 locus in embryonic stem cells. Nature, 350, 243-246.
49. Raynard,S.L., Read,L.R. and Baker,M.D. (2002) Evidence for the murine IgH μ locus acting as a hotspot for intrachromosomal homologous recombination. J. Imnumol., 168, 2332-2339.
50. Streisinger,G., Okada,Y., Emrich,J., Newton,J., Tsugita,A., Terzaghi,E. and Inouye,M. (1966) Frameshift mutations and the genetic code. Cold Spring Harbor Symp. Quant. Biol., 31, 77-84.
51. Pâques,F., Leung,W.-Y. and Haber,J.E. (1998) Expansions and contractions in a tandem repeat induced by double-strand break repair. Mol. Cell. Biol., 18, 2045-2054.
52. Strand,M., Prolla,T.A., Liskay,R.M. and Petes,T.D. (1993) Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature, 365, 274-276.
53. Kadyk,L.C. and Hartwell,L.H. (1992) Sister chromatids are preferred over homologs as substrates for recombination repair in Saccharomyces cerevisiae. Genetics, 132, 387-402.
54. Arbel,A, Zenvirth,D. and Simchen,G. (1999) Sister chromatid-based DNA repair is mediated by RAD54, not by DMC1 or TID1. EMBO J., 18, 2648-2658.
55. Smith,G.P. (1973) Unequal crossover and the evolution of multigene families. Cold Spring Harbor Symp. Quant. Biol., 38, 507-513.
56. Klein,H.L. and Petes,T.D. (1981) Intrachromosomal gene conversion in yeast. Nature, 289, 144-148.
57. Dover,G. (1982) Molecular drive: a cohesive mode of species evolution. Nature, 299, 111-117.
58. Tartof,K.D. (1973) Regulation of ribosomal RNA gene multiplicity in Drosophila melanogaster. Genetics, 73, 57-71.
59. Petes,T.D. (1980) Unequal meiotic recombination within tandem arrays of yeast ribosomal DNA genes. Cell, 19, 765-774.
60. Szostak,J.W. and Wu,R. (1980) Unequal crossing over in the ribosomal RNA of Saccharomyces cerevisiae. Nature, 284, 426-430.
61. Welch,J.W., Maloney,D.H. and Fogel,S. (1990) Unequal crossing-over and gene conversion at the amplified CUP1 locus of yeast. Mol. Gen. Genet., 222, 304-310.
62. Orr-Weaver,T.L. and Szostak,J.W. (1985) Fungal recombination. Microbiol. Rev., 49, 33-58.
63. Egel,R. (1981) Intergenic conversion and reiterated genes. Nature, 290, 191-192.
64. Maeda,N. and Smithies,O. (1986) The evolution of multigene families: human haptoglobin genes. Annu. Rev. Genet., 20, 81-108.
65. Baltimore,D. (1981) Gene conversion: some implications for immunoglobulin genes. Cell, 24, 592-594.
66. Maizels,N. (1989) Might gene conversion be the mechanism of somatic hypermutation of mammalian immunoglobulin genes? Trends Genet., 5, 4-8.
67. Schiestl,R.H., Igarashi,S. and Hastings,P.J. (1988) Analysis of the mechanism for reversion of a disrupted gene. Genetics, 119, 237-247.
68. Gangloff,S., Zou,H. and Rothstein,R. (1996). Gene conversion plays the major role in controlling the stability of large tandem repeats in yeast. EMBO J., 15, 1715-1725.
69. Jackson,J.A. and Fink,G.R. (1981) Gene conversion between duplicated genetic elements in yeast. Nature, 292, 306-311.
70. Klein,H.L. and Petes,T.D. (1981) Intrachromosomal gene conversion in yeast. Nature, 289, 144-149.
71. Liskay,R.M., Letsou,A. and Stachelek,J.L. (1987) Homology requirement for efficient gene conversion between duplicated chromosomal sequences in mammalian cells. Genetics, 115, 161-167.
72. Haber,J.E. (2000) Partners and pathways: repairing a double-strand break. Trends Genet., 16, 259-264.
73. Karran,P. (2000) DNA double strand break repair in mammalian cells. Curr. Opin. Genet. Dev., 10, 144-150.
74. Maloney,D.H. and Fogel,S. (1987) Gene conversion, unequal crossing-over and mispairing at a non-tandem duplication during meiosis of Saccharomyces cerevisiae. Curr. Genet., 12, 1-7.
75. Petes,T.D., Malone,R.E. and Symington,L.S. (1991) Recombination in yeast. In Broach,J.R., Pringle,J.R. and Jones,E.W. (eds), The Molecular and Cellular Biology of the Yeast Saccharomyces: Genome Dynamics, Protein Synthesis and Energetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 407-521.
76. Li,J., Read,L.R. and Baker,M.D. (2001) The mechanism of mammalian gene replacement is consistent with the formation of long regions of heteroduplex DNA associated with two crossing-over events. Mol. Cell. Biol., 21, 501-510.
77. Elliott,B., Richardson,C., Winderbaum,J., Nickoloff,J.A. and Jasin,M. (1998) Gene conversion tracts from double-strand break repair in mammalian cells. Mol. Cell. Biol., 18, 93-101.
78. Elliot,B. and Jasin,M. (2001) Repair of double-strand breaks by homologous recombination in mismatch repair-defective mammalian cells. Mol. Cell. Biol., 21, 2671-2682.
79. Esposito,M.S. and Wagstaff,J.E. (1981) Mechanisms of mitotic recombination. In Strathern,J.N. (ed.), The Molecular Biology of the Yeast Saccharomyces: Life Cycle and Inheritance. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 341-370.
80. Smith,G.R. (2001) Homologous recombination near and far from DNA breaks: alternative roles and contrasting views. Annu. Rev. Genet., 35, 243-274.