Sumoylation of a meiosis-specific RecA homolog, Lim15/Dmc1, via interaction with the small ubiquitin-related modifier (SUMO)-conjugating enzyme Ubc9

FEBS Journal

Volumn 273, Issue 17, 2006, Pages 4003-4012

  Koshiyama, Akiyo ^a   Hamada, Fumika N ^a   Namekawa, Satoshi H ^a   Iwabata, Kazuki ^a   Sugawara, Hiroko ^a   Sakamoto, Aiko ^a   Ishizaki, Takashi ^a   Sakaguchi, Kengo ^a  

^a TOKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

Coprinus cinereus; Meiotic recombination; Post translational modification; RecA; Sumoylation

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMINO ACID; LEPTOTENE; LIM15 PROTEIN; PROTEIN UBC9; RECA PROTEIN; SUMO PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BASIDIOMYCETES; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CONJUGATION; CONTROLLED STUDY; COPRINUS; COPRINUS CINEREUS; COVALENT BOND; GENETIC RECOMBINATION; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MEIOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PACHYTENE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SEQUENCE HOMOLOGY; SUMOYLATION;

ADENOSINE TRIPHOSPHATASES; AGARICALES; CELL CYCLE PROTEINS; DNA-BINDING PROTEINS; FUNGAL PROTEINS; MEIOSIS; MOLECULAR SEQUENCE DATA; REC A RECOMBINASES; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURAL HOMOLOGY, PROTEIN; SUMO-1 PROTEIN; TWO-HYBRID SYSTEM TECHNIQUES; UBIQUITIN-CONJUGATING ENZYMES;

COPRINOPSIS CINEREA;

EID: 33747446989     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05403.x     Document Type: Article

References (40)

1. Johnson ES & Blobel G (1997) Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J Biol Chem 272, 26799-26802.
2. Gong L, Kamitani T, Fujise K, Caskey LS & Yeh ET (1997) Preferential interaction of sentrin with a ubiquitin-conjugating enzyme, Ubc9. J Biol Chem 272, 28198-28201.
3. Desterro JM, Thomson J & Hay RT (1997) Ubch9 conjugates SUMO but not ubiquitin. FEBS Lett 417, 297-300.
4. Schwarz SE, Matuschewski K, Liakopoulos D, Scheffner M & Jentsch S (1998) The ubiquitin-like proteins SMT3 and SUMO-1 are conjugated by the UBC9 E2 enzyme. Proc Natl Acad Sci USA 95, 560-564.
5. Okuma T, Honda R, Ichikawa G, Tsumagari N & Yasuda H (1999) In vitro SUMO-1 modification requires two enzymatic steps, E1 and E2. Biochem Biophys Res Commun 254, 693-698.
6. Desterro JM, Rodriguez MS & Hay RT (1998) SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol Cell 2, 233-239.
7. Dohmen RJ (2004) SUMO protein modification. Biochim Biophys Acta 1695, 113-131.
8. Masson JY & West SC (2001) The Rad51 and Dmc1 recombinases: a non-identical twin relationship. Trends Biochem Sci 26, 131-136.
9. Golub EI, Gupta RC, Haaf T, Wold MS & Radding CM (1998) Interaction of human rad51 recombination protein with single-stranded DNA binding protein, RPA. Nucleic Acids Res 26, 5388-5393.
10. Shinohara A, Ogawa H & Ogawa T (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69, 457-470.
11. Jiang H, Xie Y, Houston P, Stemke-Hale K, Mortensen UH, Rothstein R & Kodadek T (1996) Direct association between the yeast Rad51 and Rad54 recombination proteins. J Biol Chem 271, 33181-33186.
12. Mizuta R, LaSalle JM, Cheng HL, Shinohara A, Ogawa H, Copeland N, Jenkins NA, Lalande M & Alt FW (1997) RAB22 and RAB163/mouse BRCA2: proteins that specifically interact with the RAD51 protein. Proc Natl Acad Sci USA 94, 6927-6932.
13. Sung P (1997) Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase. Genes Dev 11, 1111-1121.
14. Dresser ME, Ewing DJ, Conrad MN, Dominguez AM, Barstead R, Jiang H & Kodadek T (1997) DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. Genetics 147, 533-544.
15. Hayase A, Takagi M, Miyazaki T, Oshiumi H, Shinohara M & Shinohara A (2004) A protein complex containing Mei5 and Sae3 promotes the assembly of the meiosis-specific RecA homolog Dmc1. Cell 119, 927-940.
16. Tsubouchi H & Roeder GS (2004) The budding yeast mei5 and sae3 proteins act together with dmc1 during meiotic recombination. Genetics 168, 1219-1230.
17. Petukhova GV, Pezza RJ, Vanevski F, Ploquin M, Masson JY & Camerini-Otero RD (2005) The Hop2 and Mnd1 proteins act in concert with Rad51 and Dmc1 in meiotic recombination. Nat Struct Mol Biol 12, 449-453.
18. Iwabata K, Koshiyama A, Yamaguchi T, Sugawara H, Hamada FN, Namekawa SH, Ishii S, Ishizaki T, Chiku H, Nara T et al. (2005) DNA topoisomerase II interacts with Lim15/Dmc1 in meiosis. Nucleic Acids Res 33, 5809-5818.
19. Casselton LA & Olesnicky NS (1998) Molecular genetics of mating recognition in basidiomycete fungi. Microbiol Mol Biol Rev 62, 55-70.
20. Kues U (2000) Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol Mol Biol Rev 64, 316-353.
21. Kamada T (2002) Molecular genetics of sexual development in the mushroom Coprinus cinereus. Bioessays 24, 449-459.
22. Pukkila PJ, Yashar BM & Binninger DM (1984) Analysis of meiotic development in Coprinus cinereus. Symp Soc Exp Biol 38, 177-194.
23. Li L, Gerecke EE & Zolan ME (1999) Homolog pairing and meiotic progression in Coprinus cinereus. Chromosoma 108, 384-392.
24. Nara T, Saka T, Sawado T, Takase H, Ito Y, Hotta Y & Sakaguchi K (1999) Isolation of a LIM15/DMC1 homolog from the basidiomycete Coprinus cinereus and its expression in relation to meiotic chromosome pairing. Mol Gen Genet 262, 781-789.
25. Nara T, Hamada F, Namekawa S & Sakaguchi K (2001) Strand exchange reaction in vitro and DNA-dependent ATPase activity of recombinant LIM15/DMC1 and RAD51 proteins from Coprinus cinereus. Biochem Biophys Res Commun 285, 92-97.
26. Nara T, Yamamoto T & Sakaguchi K (2000) Characterization of interaction of C- and N-terminal domains in LIM15/DMC1 and RAD51 from a basidiomycetes, Coprinus cinereus. Biochem Biophys Res Commun 275, 97-102.
27. Kinebuchi T, Kagawa W, Kurumizaka H & Yokoyama S (2005) Role of the N-terminal domain of the human DMC1 protein in octamer formation and DNA binding. J Biol Chem 280, 28382-28387.
28. Lu BC & Jeng DY (1975) Meiosis in Coprinus VII. The prekaryogamy S-phase and the postkaryogamy DNA replication in C. lagopus. J Cell Sci 17, 461-470.
29. Yeh ET, Gong L & Kamitani T (2000) Ubiquitin-like proteins: new wines in new bottles. Gene 248, 1-14.
30. Rodriguez MS, Dargemont C & Hay RT (2001) SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J Biol Chem 276, 12654-12659.
31. Sampson DA, Wang M & Matunis MJ (2001) The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J Biol Chem 276, 21664-21669.
32. Vigodner M & Morris PL (2005) Testicular expression of small ubiquitin-related modifier-1 (SUMO-1) supports multiple roles in spermatogenesis: silencing of sex chromosomes in spermatocytes, spermatid microtubule nucleation, and nuclear reshaping. Dev Biol 282, 480-492.
33. Tarsounas M, Pearlman RE, Gasser PJ, Park MS & Moens PB (1997) Protein-protein interactions in the synaptonemal complex. Mol Biol Cell 8, 1405-1414.
34. Apionishev S, Malhotra D, Raghavachari S, Tanda S & Rasooly RS (2001) The Drosophila UBC9 homologue lesswright mediates the disjunction of homologues in meiosis I. Genes Cells 6, 215-224.
35. Kovalenko OV, Plug AW, Haaf T, Gonda DK, Ashley T, Ward DC, Radding CM & Golub EI (1996) Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. Proc Natl Acad Sci USA 93, 2958-2963.
36. Li W, Hesabi B, Babbo A, Pacione C, Liu J, Chen DJ, Nickoloff JA & Shen Z (2000) Regulation of double-strand break-induced mammalian homologous recombination by UBL1, a RAD51-interacting protein. Nucleic Acids Res 28, 1145-1153.
37. Ho JC, Warr NJ, Shimizu H & Watts FZ (2001) SUMO modification of Rad22, the Schizosaccharomyces pombe homologue of the recombination protein Rad52. Nucleic Acids Res 29, 4179-4186.
38. Sawado T & Sakaguchi K (1997) A DNA polymerase alpha catalytic subunit is purified independently from the tissues at meiotic prometaphase I of a basidiomycete, Coprinus cinereus. Biochem Biophys Res Commun 232, 454-460.
39. Ho SN, Hunt HD, Horton RM, Pullen JK & Pease LR (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59.
40. Namekawa S, Hamada F, Sawado T, Ishii S, Nara T, Ishizaki T, Ohuchi T, Arai T & Sakaguchi K (2003) Dissociation of DNA polymerase alpha-primase complex during meiosis in Coprinus cinereus. Eur J Biochem 270, 2137-2146.