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. 1998 Apr;148(4):1507–1524. doi: 10.1093/genetics/148.4.1507

Factors affecting inverted repeat stimulation of recombination and deletion in Saccharomyces cerevisiae.

K S Lobachev 1, B M Shor 1, H T Tran 1, W Taylor 1, J D Keen 1, M A Resnick 1, D A Gordenin 1
PMCID: PMC1460095  PMID: 9560370

Abstract

Inverted DNA repeats are an at-risk motif for genetic instability that can induce both deletions and recombination in yeast. We investigated the role of the length of inverted repeats and size of the DNA separating the repeats for deletion and recombination. Stimulation of both deletion and recombination was directly related to the size of inverted repeats and inversely related to the size of intervening spacers. A perfect palindrome, formed by two 1.0-kb URA3-inverted repeats, increased intra- and interchromosomal recombination in the adjacent region 2,400-fold and 17,000-fold, respectively. The presence of a strong origin of replication in the spacer reduced both rates of deletion and recombination. These results support a model in which the stimulation of deletion and recombination by inverted repeats is initiated by a secondary structure formed between single-stranded DNA of inverted repeats during replication.

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Selected References

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  1. Akgün E., Zahn J., Baumes S., Brown G., Liang F., Romanienko P. J., Lewis S., Jasin M. Palindrome resolution and recombination in the mammalian germ line. Mol Cell Biol. 1997 Sep;17(9):5559–5570. doi: 10.1128/mcb.17.9.5559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bell A. J., Hardman N. Characterization of foldback sequences in hamster DNA using electron microsocpy. Nucleic Acids Res. 1977 Jan;4(1):247–268. doi: 10.1093/nar/4.1.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berg D. E., Egner C., Hirschel B. J., Howard J., Johnsrud L., Jorgensen R. A., Tlsty T. D. Insertion, excision, and inversion of Tn5. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 1):115–123. doi: 10.1101/sqb.1981.045.01.020. [DOI] [PubMed] [Google Scholar]
  4. Biezunski N. Structure and distribution of inverted repeats (Palindromes). I. Analysis of DNA of Drosophila melanogaster. Chromosoma. 1981;84(1):87–109. doi: 10.1007/BF00293365. [DOI] [PubMed] [Google Scholar]
  5. Biezunski N. Structure and distribution of inverted repeats (palindromes). II. Analysis of DNA of the mouse. Chromosoma. 1981;84(1):111–129. doi: 10.1007/BF00293366. [DOI] [PubMed] [Google Scholar]
  6. Boeke J. D., LaCroute F., Fink G. R. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet. 1984;197(2):345–346. doi: 10.1007/BF00330984. [DOI] [PubMed] [Google Scholar]
  7. Bonneaud N., Ozier-Kalogeropoulos O., Li G. Y., Labouesse M., Minvielle-Sebastia L., Lacroute F. A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast. 1991 Aug-Sep;7(6):609–615. doi: 10.1002/yea.320070609. [DOI] [PubMed] [Google Scholar]
  8. Bonneaud N., Ozier-Kalogeropoulos O., Li G. Y., Labouesse M., Minvielle-Sebastia L., Lacroute F. A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast. 1991 Aug-Sep;7(6):609–615. doi: 10.1002/yea.320070609. [DOI] [PubMed] [Google Scholar]
  9. Brewer B. J., Fangman W. L. Initiation at closely spaced replication origins in a yeast chromosome. Science. 1993 Dec 10;262(5140):1728–1731. doi: 10.1126/science.8259517. [DOI] [PubMed] [Google Scholar]
  10. Calabretta B., Robberson D. L., Barrera-Saldaña H. A., Lambrou T. P., Saunders G. F. Genome instability in a region of human DNA enriched in Alu repeat sequences. Nature. 1982 Mar 18;296(5854):219–225. doi: 10.1038/296219a0. [DOI] [PubMed] [Google Scholar]
  11. Canceill D., Ehrlich S. D. Copy-choice recombination mediated by DNA polymerase III holoenzyme from Escherichia coli. Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6647–6652. doi: 10.1073/pnas.93.13.6647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cech T. R., Hearst J. E. An electron microscopic study of mouse foldback DNA. Cell. 1975 Aug;5(4):429–446. doi: 10.1016/0092-8674(75)90062-8. [DOI] [PubMed] [Google Scholar]
  13. Celniker S. E., Sweder K., Srienc F., Bailey J. E., Campbell J. L. Deletion mutations affecting autonomously replicating sequence ARS1 of Saccharomyces cerevisiae. Mol Cell Biol. 1984 Nov;4(11):2455–2466. doi: 10.1128/mcb.4.11.2455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Chalker A. F., Okely E. A., Davison A., Leach D. R. The effects of central asymmetry on the propagation of palindromic DNA in bacteriophage lambda are consistent with cruciform extrusion in vivo. Genetics. 1993 Feb;133(2):143–148. doi: 10.1093/genetics/133.2.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Collick A., Drew J., Penberth J., Bois P., Luckett J., Scaerou F., Jeffreys A., Reik W. Instability of long inverted repeats within mouse transgenes. EMBO J. 1996 Mar 1;15(5):1163–1171. [PMC free article] [PubMed] [Google Scholar]
  16. Collins J. Instability of palindromic DNA in Escherichia coli. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 1):409–416. doi: 10.1101/sqb.1981.045.01.055. [DOI] [PubMed] [Google Scholar]
  17. Collins J., Volckaert G., Nevers P. Precise and nearly-precise excision of the symmetrical inverted repeats of Tn5; common features of recA-independent deletion events in Escherichia coli. Gene. 1982 Jul-Aug;19(1):139–146. doi: 10.1016/0378-1119(82)90198-6. [DOI] [PubMed] [Google Scholar]
  18. Colì G., Frascaroli G., Giubilei G., Grillone G., Nanni Costa A., Piccinni L., Pierangeli A., Prandini R. Il rene da shock. Nuova tecnica sperimentale per l'induzione dello shock controllato. Nota I. Boll Soc Ital Biol Sper. 1981 Oct 15;57(19):1981–1984. [PubMed] [Google Scholar]
  19. DasGupta U., Weston-Hafer K., Berg D. E. Local DNA sequence control of deletion formation in Escherichia coli plasmid pBR322. Genetics. 1987 Jan;115(1):41–49. doi: 10.1093/genetics/115.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Deumling B. Localisation of foldback DNA sequences in nuclei chromosomes of Scilla, Secale, and of mouse. Nucleic Acids Res. 1978 Oct;5(10):3589–3602. doi: 10.1093/nar/5.10.3589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Egner C., Berg D. E. Excision of transposon Tn5 is dependent on the inverted repeats but not on the transposase function of Tn5. Proc Natl Acad Sci U S A. 1981 Jan;78(1):459–463. doi: 10.1073/pnas.78.1.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fearon E. R., Cho K. R., Nigro J. M., Kern S. E., Simons J. W., Ruppert J. M., Hamilton S. R., Preisinger A. C., Thomas G., Kinzler K. W. Identification of a chromosome 18q gene that is altered in colorectal cancers. Science. 1990 Jan 5;247(4938):49–56. doi: 10.1126/science.2294591. [DOI] [PubMed] [Google Scholar]
  23. Ferguson B. M., Fangman W. L. A position effect on the time of replication origin activation in yeast. Cell. 1992 Jan 24;68(2):333–339. doi: 10.1016/0092-8674(92)90474-q. [DOI] [PubMed] [Google Scholar]
  24. Formosa T., Alberts B. M. DNA synthesis dependent on genetic recombination: characterization of a reaction catalyzed by purified bacteriophage T4 proteins. Cell. 1986 Dec 5;47(5):793–806. doi: 10.1016/0092-8674(86)90522-2. [DOI] [PubMed] [Google Scholar]
  25. Foster T. J., Lundblad V., Hanley-Way S., Halling S. M., Kleckner N. Three Tn10-associated excision events: relationship to transposition and role of direct and inverted repeats. Cell. 1981 Jan;23(1):215–227. doi: 10.1016/0092-8674(81)90286-5. [DOI] [PubMed] [Google Scholar]
  26. Freudenreich C. H., Stavenhagen J. B., Zakian V. A. Stability of a CTG/CAG trinucleotide repeat in yeast is dependent on its orientation in the genome. Mol Cell Biol. 1997 Apr;17(4):2090–2098. doi: 10.1128/mcb.17.4.2090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Glickman B. W., Ripley L. S. Structural intermediates of deletion mutagenesis: a role for palindromic DNA. Proc Natl Acad Sci U S A. 1984 Jan;81(2):512–516. doi: 10.1073/pnas.81.2.512. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Gordenin D. A., Lobachev K. S., Degtyareva N. P., Malkova A. L., Perkins E., Resnick M. A. Inverted DNA repeats: a source of eukaryotic genomic instability. Mol Cell Biol. 1993 Sep;13(9):5315–5322. doi: 10.1128/mcb.13.9.5315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Gordenin D. A., Malkova A. L., Peterzen A., Kulikov V. N., Pavlov Y. I., Perkins E., Resnick M. A. Transposon Tn5 excision in yeast: influence of DNA polymerases alpha, delta, and epsilon and repair genes. Proc Natl Acad Sci U S A. 1992 May 1;89(9):3785–3789. doi: 10.1073/pnas.89.9.3785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Gordenin D. A., Malkova A. L., Peterzen A., Kulikov V. N., Pavlov Y. I., Perkins E., Resnick M. A. Transposon Tn5 excision in yeast: influence of DNA polymerases alpha, delta, and epsilon and repair genes. Proc Natl Acad Sci U S A. 1992 May 1;89(9):3785–3789. doi: 10.1073/pnas.89.9.3785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Gordenin D. A., Proscyavichus Y. Y., Malkova A. L., Trofimova M. V., Peterzen A. Yeast mutants with increased bacterial transposon Tn5 excision. Yeast. 1991 Jan;7(1):37–50. doi: 10.1002/yea.320070105. [DOI] [PubMed] [Google Scholar]
  32. Gordenin D. A., Proscyavichus Y. Y., Malkova A. L., Trofimova M. V., Peterzen A. Yeast mutants with increased bacterial transposon Tn5 excision. Yeast. 1991 Jan;7(1):37–50. doi: 10.1002/yea.320070105. [DOI] [PubMed] [Google Scholar]
  33. Gordenin D. A., Trofimova M. V., Shaburova O. N., Pavlov Y. I., Chernoff Y. O., Chekuolene Y. V., Proscyavichus Y. Y., Sasnauskas K. V., Janulaitis A. A. Precise excision of bacterial transposon Tn5 in yeast. Mol Gen Genet. 1988 Aug;213(2-3):388–393. doi: 10.1007/BF00339607. [DOI] [PubMed] [Google Scholar]
  34. Haber J. E. In vivo biochemistry: physical monitoring of recombination induced by site-specific endonucleases. Bioessays. 1995 Jul;17(7):609–620. doi: 10.1002/bies.950170707. [DOI] [PubMed] [Google Scholar]
  35. Hanke J. H., Hambor J. E., Kavathas P. Repetitive Alu elements form a cruciform structure that regulates the function of the human CD8 alpha T cell-specific enhancer. J Mol Biol. 1995 Feb 10;246(1):63–73. doi: 10.1006/jmbi.1994.0066. [DOI] [PubMed] [Google Scholar]
  36. Hardman N., Bell A. J., McLachlan A. Organisation of inverted repeat sequences in hamster cell nuclear DNA. Biochim Biophys Acta. 1979 Oct 25;564(3):372–389. doi: 10.1016/0005-2787(79)90029-7. [DOI] [PubMed] [Google Scholar]
  37. Henderson S. T., Petes T. D. Instability of a plasmid-borne inverted repeat in Saccharomyces cerevisiae. Genetics. 1993 May;134(1):57–62. doi: 10.1093/genetics/134.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Herrmann R., Neugebauer K., Zentgraf H., Schaller H. Transposition of a DNA sequence determining kanamycin resistance into the single-stranded genome of bacteriophage fd. Mol Gen Genet. 1978 Feb 16;159(2):171–178. doi: 10.1007/BF00270890. [DOI] [PubMed] [Google Scholar]
  39. Houck C. M., Rinehart F. P., Schmid C. W. A ubiquitous family of repeated DNA sequences in the human genome. J Mol Biol. 1979 Aug 15;132(3):289–306. doi: 10.1016/0022-2836(79)90261-4. [DOI] [PubMed] [Google Scholar]
  40. Huang C. C., Hearst J. E., Alberts B. M. Two types of replication proteins increase the rate at which T4 DNA polymerase traverses the helical regions in a single-stranded DNA template. J Biol Chem. 1981 Apr 25;256(8):4087–4094. [PubMed] [Google Scholar]
  41. Jalanko A., Manninen T., Peltonen L. Deletion of the C-terminal end of aspartylglucosaminidase resulting in a lysosomal accumulation disease: evidence for a unique genomic rearrangement. Hum Mol Genet. 1995 Mar;4(3):435–441. doi: 10.1093/hmg/4.3.435. [DOI] [PubMed] [Google Scholar]
  42. Jannière L., Ehrlich S. D. Recombination between short repeated sequences is more frequent in plasmids than in the chromosome of Bacillus subtilis. Mol Gen Genet. 1987 Nov;210(1):116–121. doi: 10.1007/BF00337766. [DOI] [PubMed] [Google Scholar]
  43. Jinks-Robertson S., Michelitch M., Ramcharan S. Substrate length requirements for efficient mitotic recombination in Saccharomyces cerevisiae. Mol Cell Biol. 1993 Jul;13(7):3937–3950. doi: 10.1128/mcb.13.7.3937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Kil' Iu V., Goryshin I. Iu, Lantsov V. A. Rekombinatsionnyi mekhanizm tochnoi ékstsizii mobil'nogo élementa IS50 v kletkakh Escherichia coli K12. Mol Biol (Mosk) 1994 May-Jun;28(3):563–573. [PubMed] [Google Scholar]
  45. Kiyosawa H., Chance P. F. Primate origin of the CMT1A-REP repeat and analysis of a putative transposon-associated recombinational hotspot. Hum Mol Genet. 1996 Jun;5(6):745–753. doi: 10.1093/hmg/5.6.745. [DOI] [PubMed] [Google Scholar]
  46. Koda Y., Soejima M., Wang B., Kimura H. Structure and expression of the gene encoding secretor-type galactoside 2-alpha-L-fucosyltransferase (FUT2). Eur J Biochem. 1997 Jun 15;246(3):750–755. doi: 10.1111/j.1432-1033.1997.t01-1-00750.x. [DOI] [PubMed] [Google Scholar]
  47. Krayev A. S., Kramerov D. A., Skryabin K. G., Ryskov A. P., Bayev A. A., Georgiev G. P. The nucleotide sequence of the ubiquitous repetitive DNA sequence B1 complementary to the most abundant class of mouse fold-back RNA. Nucleic Acids Res. 1980 Mar 25;8(6):1201–1215. doi: 10.1093/nar/8.6.1201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Kuzminov A. Collapse and repair of replication forks in Escherichia coli. Mol Microbiol. 1995 May;16(3):373–384. doi: 10.1111/j.1365-2958.1995.tb02403.x. [DOI] [PubMed] [Google Scholar]
  49. LaDuca R. J., Fay P. J., Chuang C., McHenry C. S., Bambara R. A. Site-specific pausing of deoxyribonucleic acid synthesis catalyzed by four forms of Escherichia coli DNA polymerase III. Biochemistry. 1983 Oct 25;22(22):5177–5188. doi: 10.1021/bi00291a018. [DOI] [PubMed] [Google Scholar]
  50. Leach D. R. Long DNA palindromes, cruciform structures, genetic instability and secondary structure repair. Bioessays. 1994 Dec;16(12):893–900. doi: 10.1002/bies.950161207. [DOI] [PubMed] [Google Scholar]
  51. Lehrman M. A., Russell D. W., Goldstein J. L., Brown M. S. Alu-Alu recombination deletes splice acceptor sites and produces secreted low density lipoprotein receptor in a subject with familial hypercholesterolemia. J Biol Chem. 1987 Mar 5;262(7):3354–3361. [PubMed] [Google Scholar]
  52. Lehrman M. A., Russell D. W., Goldstein J. L., Brown M. S. Exon-Alu recombination deletes 5 kilobases from the low density lipoprotein receptor gene, producing a null phenotype in familial hypercholesterolemia. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3679–3683. doi: 10.1073/pnas.83.11.3679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Lehrman M. A., Schneider W. J., Südhof T. C., Brown M. S., Goldstein J. L., Russell D. W. Mutation in LDL receptor: Alu-Alu recombination deletes exons encoding transmembrane and cytoplasmic domains. Science. 1985 Jan 11;227(4683):140–146. doi: 10.1126/science.3155573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Lin C. T., Lyu Y. L., Liu L. F. A cruciform-dumbbell model for inverted dimer formation mediated by inverted repeats. Nucleic Acids Res. 1997 Aug 1;25(15):3009–3016. doi: 10.1093/nar/25.15.3009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Mandel J. L. Human genetics. Breaking the rule of three. Nature. 1997 Apr 24;386(6627):767–769. doi: 10.1038/386767a0. [DOI] [PubMed] [Google Scholar]
  56. Michel B., Ehrlich S. D., Uzest M. DNA double-strand breaks caused by replication arrest. EMBO J. 1997 Jan 15;16(2):430–438. doi: 10.1093/emboj/16.2.430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Nag D. K., Kurst A. A 140-bp-long palindromic sequence induces double-strand breaks during meiosis in the yeast Saccharomyces cerevisiae. Genetics. 1997 Jul;146(3):835–847. doi: 10.1093/genetics/146.3.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Nelson D. L., Ledbetter S. A., Corbo L., Victoria M. F., Ramírez-Solis R., Webster T. D., Ledbetter D. H., Caskey C. T. Alu polymerase chain reaction: a method for rapid isolation of human-specific sequences from complex DNA sources. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6686–6690. doi: 10.1073/pnas.86.17.6686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Pauly M., Kayser I., Schmitz M., Ries F., Hentges F., Dicato M. The human mdr1 (multidrug-resistance) gene harbours a long homopyrimidine.homopurine sequence next to a cluster of Alu repeated sequences in intron 14. Gene. 1995 Feb 14;153(2):299–300. doi: 10.1016/0378-1119(95)00716-j. [DOI] [PubMed] [Google Scholar]
  60. Pinder D. J., Blake C. E., Leach D. R. DIR: a novel DNA rearrangement associated with inverted repeats. Nucleic Acids Res. 1997 Feb 1;25(3):523–529. doi: 10.1093/nar/25.3.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Rosche W. A., Trinh T. Q., Sinden R. R. Differential DNA secondary structure-mediated deletion mutation in the leading and lagging strands. J Bacteriol. 1995 Aug;177(15):4385–4391. doi: 10.1128/jb.177.15.4385-4391.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Ross D. G., Swan J., Kleckner N. Nearly precise excision: a new type of DNA alteration associated with the translocatable element Tn10. Cell. 1979 Apr;16(4):733–738. doi: 10.1016/0092-8674(79)90089-8. [DOI] [PubMed] [Google Scholar]
  63. Ruskin B., Fink G. R. Mutations in POL1 increase the mitotic instability of tandem inverted repeats in Saccharomyces cerevisiae. Genetics. 1993 May;134(1):43–56. doi: 10.1093/genetics/134.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Russell G. C., Mann N. H. Analysis of inverted repeat DNA in the genome of Rhodomicrobium vannielii. J Gen Microbiol. 1986 Feb;132(2):325–330. doi: 10.1099/00221287-132-2-325. [DOI] [PubMed] [Google Scholar]
  65. Sargent R. G., Brenneman M. A., Wilson J. H. Repair of site-specific double-strand breaks in a mammalian chromosome by homologous and illegitimate recombination. Mol Cell Biol. 1997 Jan;17(1):267–277. doi: 10.1128/mcb.17.1.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Schroth G. P., Ho P. S. Occurrence of potential cruciform and H-DNA forming sequences in genomic DNA. Nucleic Acids Res. 1995 Jun 11;23(11):1977–1983. doi: 10.1093/nar/23.11.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Sinden R. R., Zheng G. X., Brankamp R. G., Allen K. N. On the deletion of inverted repeated DNA in Escherichia coli: effects of length, thermal stability, and cruciform formation in vivo. Genetics. 1991 Dec;129(4):991–1005. doi: 10.1093/genetics/129.4.991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Stotz A., Linder P. The ADE2 gene from Saccharomyces cerevisiae: sequence and new vectors. Gene. 1990 Oct 30;95(1):91–98. doi: 10.1016/0378-1119(90)90418-q. [DOI] [PubMed] [Google Scholar]
  69. Tran H. T., Degtyareva N. P., Koloteva N. N., Sugino A., Masumoto H., Gordenin D. A., Resnick M. A. Replication slippage between distant short repeats in Saccharomyces cerevisiae depends on the direction of replication and the RAD50 and RAD52 genes. Mol Cell Biol. 1995 Oct;15(10):5607–5617. doi: 10.1128/mcb.15.10.5607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Tran H., Degtyareva N., Gordenin D., Resnick M. A. Altered replication and inverted repeats induce mismatch repair-independent recombination between highly diverged DNAs in yeast. Mol Cell Biol. 1997 Feb;17(2):1027–1036. doi: 10.1128/mcb.17.2.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Trinh T. Q., Sinden R. R. Preferential DNA secondary structure mutagenesis in the lagging strand of replication in E. coli. Nature. 1991 Aug 8;352(6335):544–547. doi: 10.1038/352544a0. [DOI] [PubMed] [Google Scholar]
  72. Unfried I., Entler B., Prohaska R. The organization of the gene (EPB72) encoding the human erythrocyte band 7 integral membrane protein (protein 7.2b). Genomics. 1995 Dec 10;30(3):521–528. doi: 10.1006/geno.1995.1273. [DOI] [PubMed] [Google Scholar]
  73. Warren S. T. The expanding world of trinucleotide repeats. Science. 1996 Mar 8;271(5254):1374–1375. doi: 10.1126/science.271.5254.1374. [DOI] [PubMed] [Google Scholar]
  74. Weiner A. M., Deininger P. L., Efstratiadis A. Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu Rev Biochem. 1986;55:631–661. doi: 10.1146/annurev.bi.55.070186.003215. [DOI] [PubMed] [Google Scholar]
  75. Wells R. D. Molecular basis of genetic instability of triplet repeats. J Biol Chem. 1996 Feb 9;271(6):2875–2878. doi: 10.1074/jbc.271.6.2875. [DOI] [PubMed] [Google Scholar]
  76. Weston-Hafer K., Berg D. E. Palindromy and the location of deletion endpoints in Escherichia coli. Genetics. 1989 Apr;121(4):651–658. doi: 10.1093/genetics/121.4.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Wilson D. A., Thomas C. A., Jr Palindromes in chromosomes. J Mol Biol. 1974 Mar 25;84(1):115–138. doi: 10.1016/0022-2836(74)90216-2. [DOI] [PubMed] [Google Scholar]
  78. Yu S., Mangelsdorf M., Hewett D., Hobson L., Baker E., Eyre H. J., Lapsys N., Le Paslier D., Doggett N. A., Sutherland G. R. Human chromosomal fragile site FRA16B is an amplified AT-rich minisatellite repeat. Cell. 1997 Feb 7;88(3):367–374. doi: 10.1016/s0092-8674(00)81875-9. [DOI] [PubMed] [Google Scholar]
  79. Zheng G. X., Kochel T., Hoepfner R. W., Timmons S. E., Sinden R. R. Torsionally tuned cruciform and Z-DNA probes for measuring unrestrained supercoiling at specific sites in DNA of living cells. J Mol Biol. 1991 Sep 5;221(1):107–122. doi: 10.1016/0022-2836(91)80208-c. [DOI] [PubMed] [Google Scholar]
  80. Zou H., Rothstein R. Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism. Cell. 1997 Jul 11;90(1):87–96. doi: 10.1016/s0092-8674(00)80316-5. [DOI] [PubMed] [Google Scholar]
  81. d'Alençon E., Petranovic M., Michel B., Noirot P., Aucouturier A., Uzest M., Ehrlich S. D. Copy-choice illegitimate DNA recombination revisited. EMBO J. 1994 Jun 1;13(11):2725–2734. doi: 10.1002/j.1460-2075.1994.tb06563.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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