Abstract
Meiotic recombination in the yeast Saccharomyces cerevisiae is initiated by double-strand breaks (DSB) in chromosomal DNA. These DSB, which can be mapped in the rad 50S mutant yeast strain, are caused by a topoisomerase II-like enzyme, the protein Spo11. Evidence suggests that this protein is located in the axial element of the meiotic chromosome which implies that the DSB are located in these chromosomes in the vicinity of the bases of the DNA loops. We have found that in the yeast artificial chromosomes carrying human DNA, at the level of resolution obtained by pulsed field gel electrophoresis (PFGE), the meiotic DSB in the diploid yeast are co-localized with the DNase I hypersensitive sites (HS) in a haploid strain of yeast. These HS are located close to sequences which, under stress, have the potential to form secondary structures containing unpaired nucleotides. Clusters of such sequences could be a hallmark of the bases of the chromatin loops.
Full Text
The Full Text of this article is available as a PDF (161.7 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Avril N., Deschavanne P., Bellis M., Filipski J. Loop-size spacings between CGCG clusters in long segments of human DNA. Biochem Biophys Res Commun. 1995 Aug 4;213(1):147–153. doi: 10.1006/bbrc.1995.2109. [DOI] [PubMed] [Google Scholar]
- Bechert T., Diekmann S., Arndt-Jovin D. J. Human 170 kDa and 180 kDa topoisomerases II bind preferentially to curved and left-handed linear DNA. J Biomol Struct Dyn. 1994 Dec;12(3):605–623. doi: 10.1080/07391102.1994.10508762. [DOI] [PubMed] [Google Scholar]
- Bergerat A., de Massy B., Gadelle D., Varoutas P. C., Nicolas A., Forterre P. An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature. 1997 Mar 27;386(6623):414–417. doi: 10.1038/386414a0. [DOI] [PubMed] [Google Scholar]
- Bode J., Kohwi Y., Dickinson L., Joh T., Klehr D., Mielke C., Kohwi-Shigematsu T. Biological significance of unwinding capability of nuclear matrix-associating DNAs. Science. 1992 Jan 10;255(5041):195–197. doi: 10.1126/science.1553545. [DOI] [PubMed] [Google Scholar]
- Boulikas T. Chromatin domains and prediction of MAR sequences. Int Rev Cytol. 1995;162A:279–388. doi: 10.1016/s0074-7696(08)61234-6. [DOI] [PubMed] [Google Scholar]
- Cockerill P. N., Garrard W. T. Chromosomal loop anchorage of the kappa immunoglobulin gene occurs next to the enhancer in a region containing topoisomerase II sites. Cell. 1986 Jan 31;44(2):273–282. doi: 10.1016/0092-8674(86)90761-0. [DOI] [PubMed] [Google Scholar]
- Dhar V., Nandi A., Schildkraut C. L., Skoultchi A. I. Erythroid-specific nuclease-hypersensitive sites flanking the human beta-globin domain. Mol Cell Biol. 1990 Aug;10(8):4324–4333. doi: 10.1128/mcb.10.8.4324. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dillon N., Grosveld F. Chromatin domains as potential units of eukaryotic gene function. Curr Opin Genet Dev. 1994 Apr;4(2):260–264. doi: 10.1016/s0959-437x(05)80053-x. [DOI] [PubMed] [Google Scholar]
- Fan Q. Q., Petes T. D. Relationship between nuclease-hypersensitive sites and meiotic recombination hot spot activity at the HIS4 locus of Saccharomyces cerevisiae. Mol Cell Biol. 1996 May;16(5):2037–2043. doi: 10.1128/mcb.16.5.2037. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Filipski J., Leblanc J., Youdale T., Sikorska M., Walker P. R. Periodicity of DNA folding in higher order chromatin structures. EMBO J. 1990 Apr;9(4):1319–1327. doi: 10.1002/j.1460-2075.1990.tb08241.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gaensler K. M., Burmeister M., Brownstein B. H., Taillon-Miller P., Myers R. M. Physical mapping of yeast artificial chromosomes containing sequences from the human beta-globin gene region. Genomics. 1991 Aug;10(4):976–984. doi: 10.1016/0888-7543(91)90188-k. [DOI] [PubMed] [Google Scholar]
- Gromova I. I., Nielsen O. F., Razin S. V. Long-range fragmentation of the eukaryotic genome by exogenous and endogenous nucleases proceeds in a specific fashion via preferential DNA cleavage at matrix attachment sites. J Biol Chem. 1995 Aug 4;270(31):18685–18690. doi: 10.1074/jbc.270.31.18685. [DOI] [PubMed] [Google Scholar]
- Gross D. S., Garrard W. T. Nuclease hypersensitive sites in chromatin. Annu Rev Biochem. 1988;57:159–197. doi: 10.1146/annurev.bi.57.070188.001111. [DOI] [PubMed] [Google Scholar]
- Heng H. H., Tsui L. C., Moens P. B. Organization of heterologous DNA inserts on the mouse meiotic chromosome core. Chromosoma. 1994 Oct;103(6):401–407. doi: 10.1007/BF00362284. [DOI] [PubMed] [Google Scholar]
- Henthorn P. S., Mager D. L., Huisman T. H., Smithies O. A gene deletion ending within a complex array of repeated sequences 3' to the human beta-globin gene cluster. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5194–5198. doi: 10.1073/pnas.83.14.5194. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hugerat Y., Spencer F., Zenvirth D., Simchen G. A versatile method for efficient YAC transfer between any two strains. Genomics. 1994 Jul 1;22(1):108–117. doi: 10.1006/geno.1994.1351. [DOI] [PubMed] [Google Scholar]
- Jackson D. A., Dickinson P., Cook P. R. The size of chromatin loops in HeLa cells. EMBO J. 1990 Feb;9(2):567–571. doi: 10.1002/j.1460-2075.1990.tb08144.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kay V., Bode J. Binding specificity of a nuclear scaffold: supercoiled, single-stranded, and scaffold-attached-region DNA. Biochemistry. 1994 Jan 11;33(1):367–374. doi: 10.1021/bi00167a047. [DOI] [PubMed] [Google Scholar]
- Keeney S., Giroux C. N., Kleckner N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell. 1997 Feb 7;88(3):375–384. doi: 10.1016/s0092-8674(00)81876-0. [DOI] [PubMed] [Google Scholar]
- Kimura K., Hirano T. ATP-dependent positive supercoiling of DNA by 13S condensin: a biochemical implication for chromosome condensation. Cell. 1997 Aug 22;90(4):625–634. doi: 10.1016/s0092-8674(00)80524-3. [DOI] [PubMed] [Google Scholar]
- Klein S., Zenvirth D., Sherman A., Ried K., Rappold G., Simchen G. Double-strand breaks on YACs during yeast meiosis may reflect meiotic recombination in the human genome. Nat Genet. 1996 Aug;13(4):481–484. doi: 10.1038/ng0896-481. [DOI] [PubMed] [Google Scholar]
- Koshland D., Strunnikov A. Mitotic chromosome condensation. Annu Rev Cell Dev Biol. 1996;12:305–333. doi: 10.1146/annurev.cellbio.12.1.305. [DOI] [PubMed] [Google Scholar]
- Lilley D. M. DNA--protein interactions. HMG has DNA wrapped up. Nature. 1992 May 28;357(6376):282–283. doi: 10.1038/357282a0. [DOI] [PubMed] [Google Scholar]
- Loidl J., Scherthan H., Den Dunnen J. T., Klein F. Morphology of a human-derived YAC in yeast meiosis. Chromosoma. 1995 Nov;104(3):183–188. doi: 10.1007/BF00352183. [DOI] [PubMed] [Google Scholar]
- Mielke C., Maass K., Tümmler M., Bode J. Anatomy of highly expressing chromosomal sites targeted by retroviral vectors. Biochemistry. 1996 Feb 20;35(7):2239–2252. doi: 10.1021/bi952393y. [DOI] [PubMed] [Google Scholar]
- Mirkovitch J., Mirault M. E., Laemmli U. K. Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell. 1984 Nov;39(1):223–232. doi: 10.1016/0092-8674(84)90208-3. [DOI] [PubMed] [Google Scholar]
- Møens P. B., Pearlman R. E. Chromatin organization at meiosis. Bioessays. 1988 Nov;9(5):151–153. doi: 10.1002/bies.950090503. [DOI] [PubMed] [Google Scholar]
- Nash H. A. Bending and supercoiling of DNA at the attachment site of bacteriophage lambda. Trends Biochem Sci. 1990 Jun;15(6):222–227. doi: 10.1016/0968-0004(90)90034-9. [DOI] [PubMed] [Google Scholar]
- Ohta K., Shibata T., Nicolas A. Changes in chromatin structure at recombination initiation sites during yeast meiosis. EMBO J. 1994 Dec 1;13(23):5754–5763. doi: 10.1002/j.1460-2075.1994.tb06913.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pognan F., Paoletti C. Does cruciform DNA provide a recognition signal for DNA-topoisomerase II? Biochimie. 1992 Nov;74(11):1019–1023. doi: 10.1016/0300-9084(92)90022-7. [DOI] [PubMed] [Google Scholar]
- Svetlova E., Avril-Fournout N., Ira G., Deschavanne P., Filipski J. DNase-hypersensitive sites in yeast artificial chromosomes containing human DNA. Mol Gen Genet. 1998 Feb;257(3):292–298. doi: 10.1007/s004380050650. [DOI] [PubMed] [Google Scholar]
- Targa F. R., Razin S. V., de Moura Gallo C. V., Scherrer K. Excision close to matrix attachment regions of the entire chicken alpha-globin gene domain by nuclease S1 and characterization of the framing structures. Proc Natl Acad Sci U S A. 1994 May 10;91(10):4422–4426. doi: 10.1073/pnas.91.10.4422. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tuan D., Solomon W., Li Q., London I. M. The "beta-like-globin" gene domain in human erythroid cells. Proc Natl Acad Sci U S A. 1985 Oct;82(19):6384–6388. doi: 10.1073/pnas.82.19.6384. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weiner B. M., Kleckner N. Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell. 1994 Jul 1;77(7):977–991. doi: 10.1016/0092-8674(94)90438-3. [DOI] [PubMed] [Google Scholar]
- Wu T. C., Lichten M. Meiosis-induced double-strand break sites determined by yeast chromatin structure. Science. 1994 Jan 28;263(5146):515–518. doi: 10.1126/science.8290959. [DOI] [PubMed] [Google Scholar]
