Investigation of the mechanism of meiotic DNA cleavage by VMA1-derived endonuclease uncovers a meiotic alteration in chromatin structure around the target site

Eukaryotic Cell

Volumn 5, Issue 6, 2006, Pages 981-990

  Fukuda, Tomoyuki ^a,b   Ohta, Kunihiro ^b   Ohya, Yoshikazu ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL DNA; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; SACCHAROMYCES CEREVISIAE PROTEIN; TFP1 PROTEIN, S CEREVISIAE;

ACTIVE TRANSPORT; ARTICLE; CHEMISTRY; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; GENETICS; MEIOSIS; METABOLISM; MITOSIS; SACCHAROMYCES CEREVISIAE;

ACTIVE TRANSPORT, CELL NUCLEUS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA, FUNGAL; MEIOSIS; MITOSIS; PROTON-TRANSLOCATING ATPASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

ANIMALIA; SACCHAROMYCES CEREVISIAE;

EID: 33745120193     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00052-06     Document Type: Article

References (42)

1. Belfort, M., and R. J. Roberts. 1997. Homing endonucleases: keeping the house in order. Nucleic Acids Res. 25:3379-3388.
2. Hurt, A., and V. Koufopanou. 2004. Homing endonuclease genes: the rise and fall and rise again of a selfish element. Curr. Opin. Genet. Dev. 14:609-615.
3. Chevalier, B. S., and B. L. Stoddard. 2001. Homing endonucleases: structural and functional insight into the catalysts of intron/intein mobility. Nucleic Acids Res. 29:3757-3774.
4. Chu, S., and I. Herskowitz. 1998. Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol. Cell 1:685-696.
5. Church, G. M., and W. Gilbert. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81:1991-1995.
6. Dirick, L., L. Goetsch, G. Ammerer, and B. Byers. 1998. Regulation of meiotic S phase by Ime2 and a Clb5,6-associated kinase in Saccharomyces cerevisiae. Science 281:1854-1857.
7. Foiani, M., E. Nadjar-Boger, R. Capone, S. Sagee, T. Hashimshoni, and Y. Kassir. 1996. A meiosis-specific protein kinase. Ime2, is required for the correct timing of DNA replication and for spore formation in yeast meiosis. Mol. Gen. Genet. 253:278-288.
8. Fukuda, T., Y. Nagai, and Y. Ohya. 2004. Molecular mechanism of VDE-initiated intein homing in yeast nuclear genome. Adv. Biophys. 38:215-232.
9. Fukuda, T., S. Nogami, and Y. Ohya. 2003. VDE-initiated intein homing in Saccharomyces cerevisiae proceeds in a meiotic recombination-like manner. Genes Cells 8:587-602.
10. Fukuda, T., and Y. Ohya. 2006. Recruitment of RecA homologs Dmc1p and Rad51p to the double-strand break repair site initiated by meiosis-specific endonuclease VDE (PI-SceI). Mol. Genet. Genomics 275:204-214.
11. Gimble, F. S., and B. W. Stephens. 1995. Substitutions in conserved dodecapeptide motifs that uncouple the DNA binding and DNA cleavage activities of PI-SceI endonuclease. J. Biol. Chem. 270:5849-5856.
12. Gimble, F. S., and J. Thorner. 1992. Homing of a DNA endonuclease gene by meiotic gene conversion in Saccharomyces cerevisiae. Nature 357:301-306.
13. Gimble, F. S., and J. Thorner. 1993. Purification and characterization of VDE, a site-specific endonuclease from the yeast Saccharomyces cerevisiae. J. Biol. Chem. 268:21844-21853.
14. He, Z., M. Crist, H. Yen, X. Duan, F. A. Quiocho, and F. S. Gimble. 1998. Amino acid residues in both the protein splicing and endonuclease domains of the PI-SceI intein mediate DNA binding. J. Biol. Chem. 273:4607-4615.
15. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
16. Huang, Y. J., M. M. Parker, and M. Belfort. 1999. Role of exonucleolytic degradation in group I intron homing in phage T4. Genetics 153:1501-1512.
17. Jurica, M. S., and B. L. Stoddard. 1999. Homing endonucleases: structure, function and evolution. Cell. Mol. Life Sci. 55:1304-1326.
18. Kane, S. M., and R. Roth. 1974. Carbohydrate metabolism during ascospore development in yeast. J. Bacteriol. 118:8-14.
19. Kawasaki, M., S. Nogami, Y. Satow, Y. Ohya, and Y. Anraku. 1997. Identification of three core regions essential for protein splicing of the yeast Vma1 protozyme. A random mutagenesis study of the entire Vma1-derived endonuclease sequence. J. Biol. Chem. 272:15668-15674.
20. Koufopanou, V., M. R. Goddard, and A. Burt. 2002. Adaptation for horizontal transfer in a homing endonuclease. Mol. Biol. Evol. 19:239-246.
21. Mizumura, H., T. Shibata, and N. Morishima. 1999. Stable association of 70-kDa heat shock protein induces latent multisite specificity of a unisite-specific endonuclease in yeast mitochondria. J. Biol. Chem. 274:25682-25690.
22. Mizuno, K., Y. Emura, M. Baur, J. Kohli, K. Ohta, and T. Shibata. 1997. The meiotic recombination hot spot created by the single-base substitution ade6-M26 results in remodeling of chromatin structure in fission yeast. Genes Dev. 11:876-886.
23. Mueller, J. E., J. Clyman, Y. J. Huang, M. M. Parker, and M. Belfort. 1996. Intron mobility in phage T4 occurs in the context of recombination- dependent DNA replication by way of multiple pathways. Genes Dev. 10:351-364.
24. Nagai, Y., S. Nogami, F. Kumagai-Sano, and Y. Ohya. 2003. Karyopherin-mediated nuclear import of the homing endonuclease VMA1-derived endonuclease is required for self-propagation of the coding region. Mol. Cell. Biol. 23:1726-1736.
25. Neale, M. J., M. Ramachandran, E. Trelles-Sticken, H. Scherthan, and A. S. Goldman. 2002. Wild-type levels of Spo11-induced DSBs are required for normal single-strand resection during meiosis. Mol. Cell 9:835-846.
26. Nogami, S., T. Fukuda, Y. Nagai, S. Yabe, M. Sugiura, R. Mizutani, Y. Satow, Y. Anraku, and Y. Ohya. 2002. Homing: at an extragenic locus mediated by VDE (PI-SceI) in Saccharomyces cerevisiae. Yeast 19:773-782.
27. Ohta, K., A. Nicolas, M. Furuse, A. Nabetani, H. Ogawa, and T. Shibata. 1998. Mutations in the MRE11, RAD50, XRS2, and MRE2 genes alter chromatin configuration at meiotic DNA double-stranded break sites in premeiotic and meiotic cells. Proc. Natl. Acad. Sci. USA 95:646-651.
28. Ohta, K., T. Shibata, and A. Nicolas. 1994. Changes in chromatin structure at recombination initiation sites during yeast meiosis. EMBO J. 13:5754-5763.
29. Okuda, Y., D. Sasaki, S. Nogami, Y. Kaneko, Y. Ohya, and Y. Anraku. 2003. Occurrence, horizontal transfer and degeneration of VDE intein family in saccharomycete yeasts. Yeast 20:563-573.
30. Parker, M. M., D. A. Court, K. Preiter, and M. Belfort. 1996. Homology requirements for double-strand break-mediated recombination in a phage lambda-td intron model system. Genetics 143:1057-1068.
31. Posey, K. L., V. Koufopanou, A. Burt, and F. S. Gimble. 2004. Evolution of divergent DNA recognition specificities in VDE homing endonucleases from two yeast species. Nucleic Acids Res. 32:3947-3956.
32. Sakumoto, N., Y. Mukai, K. Uchida, T. Kouchi, J. Kuwajima, Y. Nakagawa, S. Sugioka, E. Yamamoto, T. Furuyama, H. Mizubuchi, N. Ohsugi, T. Sakuno, K. Kikuchi, I. Matsuoka, N. Ogawa, Y. Kaneko, and S. Harashima. 1999. A series of protein phosphatase gene disruptants in Saccharomyces cerevisiae. Yeast 15:1669-1679.
33. Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
34. Stotz, A., and P. Linder. 1990. The ADE2 gene from Saccharomyces cerevisiae: sequence and new vectors. Gene 95:91-93.
35. Stuart, D., and C. Wittenberg. 1998. CLB5 and CLB6 are required for premeiotic DNA replication and activation of the meiotic S/M checkpoint. Genes Dev. 12:2698-2710.
36. Tanaka, T., D. Knapp, and K. Nasmyth. 1997. Loading of an Mem protein onto DNA replication origins is regulated by Cdc6p and CDKs. Cell 90:649-660.
37. Vershon, A. K., and M. Pierce. 2000. Transcriptional regulation of meiosis in yeast. Curr. Opin. Cell Biol. 12:334-339.
38. Wang, R., Y. Jin, and D. Norris. 1997. Identification of a protein that binds to the Ho endonuclease recognition sequence at the yeast mating type locus. Mol. Cell. Biol. 17:770-777.
39. Wenzlau, J. M., R. J. Saldanha, R. A. Butow, and P. S. Perlman. 1989. A latent intron-encoded maturase is also an endonuclease needed for intron mobility. Cell 56:421-430.
40. Wu, T. C., and M. Lichten. 1994. Meiosis-induced double-strand break sites determined by yeast chromatin structure. Science 263:515-518.
41. Yamada, T., K. I. Mizuno, K. Hirota, N. Kon, W. P. Wahls, E. Hartsuiker, H. Murofushi, T. Shibata, and K. Ohta. 2004. Roles of histone acetylation and chromatin remodeling factor in a meiotic recombination hotspot. EMBO J. 23:1792-1803.
42. Zinn, A. R., and R. A. Butow. 1985. Nonreciprocal exchange between alleles of the yeast mitochondrial 21S rRNA gene: kinetics and the involvement of a double-strand break. Cell 40:887-895.