SUMO meets meiosis: An encounter at the synaptonemal complex: SUMO chains and sumoylated proteins suggest that heterogeneous and complex interactions lie at the centre of the synaptonemal complex

BioEssays

Volumn 33, Issue 7, 2011, Pages 529-537

  Watts, Felicity Z ^a   Hoffmann, Eva ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

Chromosome morphology; Meiosis; Red1; SUMO; Synaptonemal complex

Indexed keywords

PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEIN; PROTEIN RED1; PROTEIN ZIP3; SUMO PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

CELL HETEROGENEITY; CHROMOSOME; CHROMOSOME PAIRING; CHROMOSOME STRUCTURE; CONJUGATION; HUMAN; MEIOSIS; NONHUMAN; PROTEIN ANALYSIS; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; REVIEW; SCHIZOSACCHAROMYCES POMBE; SPERMATOCYTE; STAINING; SYNAPTONEMAL COMPLEX; YEAST;

ANIMALS; HUMANS; MEIOSIS; SUMO-1 PROTEIN; SYNAPTONEMAL COMPLEX;

SACCHAROMYCETALES;

EID: 79959263567     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201100002     Document Type: Review

References (73)

1. Zickler D, Kleckner N. 1999. Meiotic chromosomes: Integrating structure and function. Annu Rev Genet 33: 603-754.
2. Page SL, Hawley RS. 2004. The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20: 525-58.
3. Macqueen AJ, Roeder GS. 2009. Fpr3 and Zip3 ensure that initiation of meiotic recombination precedes chromosome synapsis in budding yeast. Curr Biol 19: 1519-26.
4. Jin H, Guacci V, Yu HG. 2009. Pds5 is required for homologue pairing and inhibits synapsis of sister chromatids during yeast meiosis. J Cell Biol 186: 713-25.
5. Henderson KA, Keeney S. 2005. Synaptonemal complex formation: Where does it start? BioEssays 27: 995-8.
6. Osman K, Sanchez-Moran E, Higgins JD, Jones GH, et al. 2006. Chromosome synapsis in Arabidopsis: Analysis of the transverse filament protein ZYP1 reveals novel functions for the synaptonemal complex. Chromosoma 115: 212-9.
7. Brown PW, Judis L, Chan ER, Schwartz S, et al. 2005. Meiotic synapsis proceeds from a limited number of subtelomeric sites in the human male. Am J Hum Genet 77: 556-66.
8. Tsubouchi T, Macqueen AJ, Roeder GS. 2008. Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22: 3217-26.
9. Tarsounas M, Pearlman RE, Gasser PJ, Park MS, et al. 1997. Protein-protein interactions in the synaptonemal complex. Mol Biol Cell 8: 1405-14.
10. Hooker GW, Roeder GS. 2006. A Role for SUMO in meiotic chromosome synapsis. Curr Biol 16: 1238-43.
11. Kovalenko OV, Plug AW, Haaf T, Gonda DK, et al. 1996. Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. Proc Natl Acad Sci USA 93: 2958-63.
12. La Salle S, Sun F, Zhang XD, Matunis MJ, et al. 2008. Developmental control of sumoylation pathway proteins in mouse male germ cells. Dev Biol 321: 227-37.
13. Koshiyama A, Hamada FN, Namekawa SH, Iwabata K, et al. 2006. Sumoylation of a meiosis-specific RecA homolog, Lim15/Dmc1, via interaction with the small ubiquitin-related modifier (SUMO)-conjugating enzyme Ubc9. FEBS J 273: 4003-12.
14. 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: 480-92.
15. Rogers RS, Inselman A, Handel MA, Matunis MJ. 2004. SUMO modified proteins localize to the XY body of pachytene spermatocytes. Chromosoma 113: 233-43.
16. Brown PW, Hwang K, Schlegel PN, Morris PL. 2008. Small ubiquitin-related modifier (SUMO)-1, SUMO-2/3 and SUMOylation are involved with centromeric heterochromatin of chromosomes 9 and 1 and proteins of the synaptonemal complex during meiosis in men. Hum Reprod 23: 2850-7.
17. Cheng CH, Lo YH, Liang SS, Ti SC, et al. 2006. SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae Genes Dev 20: 2067-81.
18. Hay RT. 2005. SUMO: A history of modification. Mol Cell 18: 1-12.
19. Ulrich HD. 2008. The fast-growing business of SUMO chains. Mol Cell 32: 301-5.
20. Saitoh H, Pu R, Cavenagh M, Dasso M. 1997. RanBP2 associates with Ubc9p and a modified form of RanGAP1. Proc Natl Acad Sci USA 94: 3736-41.
21. Pfander B, Moldovan GL, Sacher M, Hoege C, et al. 2005. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436: 428-33.
22. Papouli E, Chen S, Davies AA, Huttner D, et al. 2005. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol Cell 19: 123-33.
23. Minty A, Dumont X, Kaghad M, Caput D. 2000. Covalent modification of p73alpha by SUMO-1. Two-hybrid screening with p73 identifies novel SUMO-1-interacting proteins and a SUMO-1 interaction motif. J Biol Chem 275: 36316-23.
24. Song J, Durrin LK, Wilkinson TA, Krontiris TG, et al. 2004. Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc Natl Acad Sci USA 101: 14373-8.
25. Hannich JT, Lewis A, Kroetz MB, Li SJ, et al. 2005. Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae J Biol Chem 280: 4102-10.
26. Hecker CM, Rabiller M, Haglund K, Bayer P, et al. 2006. Specification of SUMO1- and SUMO2-interacting motifs. J Biol Chem 281: 16117-27.
27. Lorenz A, Wells JL, Pryce DW, Novatchkova M, et al. 2004. S. pombe meiotic linear elements contain proteins related to synaptonemal complex components. J Cell Sci 117: 3343-51.
28. Spirek M, Estreicher A, Csaszar E, Wells J, et al. SUMOylation is required for normal development of linear elements and wild-type meiotic recombination in Schizosaccharomyces pombe Chromosoma 119: 59-72.
29. Kleckner N. 2006. Chiasma formation: Chromatin/axis interplay and the role(s) of the synaptonemal complex. Chromosoma 115: 175-94.
30. Sym M, Engebrecht JA, Roeder GS. 1993. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365-78.
31. Zavec AB, Lesnik U, Komel R, Comino A. 2004. The Saccharomyces cerevisiae gene ECM11 is a positive effector of meiosis. FEMS Microbiol Lett 241: 193-9.
32. Zavec AB, Comino A, Lenassi M, Komel R. 2008. Ecm11 protein of yeast Saccharomyces cerevisiae is regulated by sumoylation during meiosis. FEMS Yeast Res 8: 64-70.
33. Altmannova V, Eckert-Boulet N, Arneric M, Kolesar P, et al. 2010. Rad52 SUMOylation affects the efficiency of the DNA repair. Nucleic Acids Res 38: 4708-21.
34. Pan J, Sasaki M, Kniewel R, Murakami H, et al. 2011. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144: 719-31.
35. Storlazzi A, Tesse S, Ruprich-Robert G, Gargano S, et al. 2008. Coupling meiotic chromosome axis integrity to recombination. Genes Dev 22: 796-809.
36. Hamant O, Ma H, Cande WZ. 2006. Genetics of meiotic prophase I in plants. Annu Rev Plant Biol 57: 267-302.
37. de Carvalho CE, Colaiacovo MP. 2006. SUMO-mediated regulation of synaptonemal complex formation during meiosis. Genes Dev 20: 1986-92.
38. Agarwal S, Roeder GS. 2000. Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102: 245-55.
39. Shinohara M, Oh SD, Hunter N, Shinohara A. 2008. Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nat Genet 40: 299-309.
40. Bhalla N, Wynne DJ, Jantsch V, Dernburg AF. 2008. ZHP-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in C. elegans PLoS Genet 4: e1000235.
41. Perry J, Kleckner N, Borner GV. 2005. Bioinformatic analyses implicate the collaborating meiotic crossover/chiasma proteins Zip2, Zip3, and Spo22/Zip4 in ubiquitin labeling. Proc Natl Acad Sci USA 102: 17594-9.
42. Uzunova K, Gottsche K, Miteva M, Weisshaar SR, et al. 2007. Ubiquitin-dependent proteolytic control of SUMO conjugates. J Biol Chem 282: 34167-75.
43. Xie Y, Kerscher O, Kroetz MB, McConchie HF, et al. 2007. The yeast Hex3.Slx8 heterodimer is a ubiquitin ligase stimulated by substrate sumoylation. J Biol Chem 282: 34176-84.
44. Wang Z, Jones GM, Prelich G. 2006. Genetic analysis connects SLX5 and SLX8 to the SUMO pathway in Saccharomyces cerevisiae Genetics 172: 1499-509.
45. Mullen JR, Brill SJ. 2008. Activation of the Slx5-Slx8 ubiquitin ligase by poly-small ubiquitin-like modifier conjugates. J Biol Chem 283: 19912-21.
46. Weger S, Hammer E, Heilbronn R. 2005. Topors acts as a SUMO-1 E3 ligase for p53 in vitro and in vivo FEBS Lett 579: 5007-12.
47. Eichinger CS, Jentsch S. Synaptonemal complex formation and meiotic checkpoint signaling are linked to the lateral element protein Red1. Proc Natl Acad Sci USA 107: 11370-5.
48. Roeder GS. 1997. Meiotic chromosomes: It takes two to tango. Genes Dev 11: 2600-21.
49. Chua PR, Roeder GS. 1998. Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93: 349-59.
50. Storlazzi A, Xu L, Schwacha A, Kleckner N. 1996. Synaptonemal complex component Zip1 plays a role in meiotic recombination independent of SC polymerisation along the chromosomes. Proc Natl Acad Sci USA 93: 9043-8.
51. Lin FM, Lai YJ, Shen HJ, Cheng YH, et al. 2010. Yeast axial-element protein, Red1, binds SUMO chains to promote meiotic interhomologue recombination and chromosome synapsis. EMBO J 29: 586-96.
52. Baba D, Maita N, Jee JG, Uchimura Y, et al. 2005. Crystal structure of thymine DNA glycosylase conjugated to SUMO-1. Nature 435: 979-82.
53. Smith AV, Roeder GS. 1997. The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol 136: 957-67.
54. Jordan P, Copsey A, Newnham L, Kolar E, et al. 2009. Ipl1/Aurora B kinase coordinates synaptonemal complex disassembly with cell cycle progression and crossover formation in budding yeast meiosis. Genes Dev 23: 2237-51.
55. Tsubouchi H, Roeder GS. 2006. Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev 20: 1766-75.
56. Nagai S, Davoodi N, Gasser SM. 2011. Nuclear organization in genome stability: SUMO connections. Cell Res 21: 474-85.
57. Zhong S, Salomoni P, Pandolfi PP. 2000. The transcriptional role of PML and the nuclear body. Nat Cell Biol 2: E85-90.
58. Tatham MH, Geoffroy MC, Shen L, Plechanovova A, et al. 2008. RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat Cell Biol 10: 538-46.
59. Shen TH, Lin HK, Scaglioni PP, Yung TM, et al. 2006. The mechanisms of PML-nuclear body formation. Mol Cell 24: 331-9.
60. Yeager TR, Neumann AA, Englezou A, Huschtscha LI, et al. 1999. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res 59: 4175-9.
61. Yan W, Santti H, Janne OA, Palvimo JJ, et al. 2003. Expression of the E3 SUMO-1 ligases PIASx and PIAS1 during spermatogenesis in the rat. Gene Expr Patterns 3: 301-8.
62. Hietakangas V, Anckar J, Blomster HA, Fujimoto M, et al. 2006. PDSM, a motif for phosphorylation-dependent SUMO modification. Proc Natl Acad Sci USA 103: 45-50.
63. Schmekel K, Daneholt B. 1995. The central region of the synaptonemal complex revealed in three dimensions. Trends Cell Biol 5: 239-42.
64. Tatham MH, Chen Y, Hay RT. 2003. Role of two residues proximal to the active site of Ubc9 in substrate recognition by the Ubc9.SUMO-1 thiolester complex. Biochemistry 42: 3168-79.
65. Bylebyl GR, Belichenko I, Johnson ES. 2003. The SUMO isopeptidase Ulp2 prevents accumulation of SUMO chains in yeast. J Biol Chem 278: 44113-20.
66. Cooper HJ, Tatham MH, Jaffray E, Heath JK, et al. 2005. Fourier transform ion cyclotron resonance mass spectrometry for the analysis of small ubiquitin-like modifier (SUMO) modification: Identification of lysines in RanBP2 and SUMO targeted for modification during the E3 autoSUMOylation reaction. Anal Chem 77: 6310-9.
67. Li SJ, Hochstrasser M. 1999. A new protease required for cell-cycle progression in yeast. Nature 398: 246-51.
68. Li SJ, Hochstrasser M. 2000. The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol Cell Biol 20: 2367-77.
69. Yeh ET. 2009. SUMOylation and De-SUMOylation: Wrestling with life's processes. J Biol Chem 284: 8223-7.
70. Lin DY, Huang YS, Jeng JC, Kuo HY, et al. 2006. Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. Mol Cell 24: 341-54.
71. Meulmeester E, Kunze M, Hsiao HH, Urlaub H, et al. 2008. Mechanism and consequences for paralog-specific sumoylation of ubiquitin-specific protease 25. Mol Cell 30: 610-9.
72. Takahashi Y, Yong-Gonzalez V, Kikuchi Y, Strunnikov A. 2006. SIZ1/SIZ2 control of chromosome transmission fidelity is mediated by the sumoylation of topoisomerase II. Genetics 172: 783-94.
73. Geoffroy MC, Hay RT. 2009. An additional role for SUMO in ubiquitin-mediated proteolysis. Nat Rev Mol Cell Biol 10: 564-8.