Abstract
Meiosis is a specialized form of cell division required for the formation of haploid gametes and therefore is essential for successful sexual reproduction. Various steps are exquisitely coordinated to ensure accurate chromosome segregation during meiosis, thereby promoting the formation of haploid gametes from diploid cells. Recent studies are demonstrating that an important form of regulation during meiosis is exerted by the post-translational protein modification known as sumoylation. Here, we review and discuss the various critical steps of meiosis in which SUMO-mediated regulation has been implicated thus far. These include the maintenance of meiotic centromeric heterochromatin , meiotic DNA double-strand break repair and homologous recombination, centromeric coupling, and the assembly of a proteinaceous scaffold between homologous chromosomes known as the synaptonemal complex.
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References
Agarwal S, Roeder GS (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102:245–255
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
Bachant J, Alcasabas A, Blat Y, Kleckner N, Elledge SJ (2002) The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA topoisomerase II. Mol Cell 9:1169–1182
Bencsath KP, Podgorski MS, Pagala VR, Slaughter CA, Schulman BA (2002) Identification of a multifunctional binding site on Ubc9p required for Smt3p conjugation. J Biol Chem 277:47938–47945
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
Branzei D, Sollier J, Liberi G, Zhao X, Maeda D, Seki M, Enomoto T, Ohta K, Foiani M (2006) Ubc9- and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 127:509–522
Broday L, Kolotuev I, Didier C, Bhoumik A, Gupta BP, Sternberg PW, Podbilewicz B, Ronai Z (2004) The small ubiquitin-like modifier (SUMO) is required for gonadal and uterine-vulval morphogenesis in Caenorhabditis elegans. Genes Dev 18:2380–2391
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 23:2850–2857
Cheng CH, Lo YH, Liang SS, Ti SC, Lin FM, Yeh CH, Huang HY, Wang TF (2006) SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev 20:2067–2081
Cheng CH, Lin FM, Lo YH, Wang TF (2007) Tying SUMO modifications to dynamic behaviors of chromosomes during meiotic prophase of Saccharomyces cerevisiae. J Biomed Sci 14:481–490
Cotta-Ramusino C, McDonald ER 3rd, Hurov K, Sowa ME, Harper JW, Elledge SJ (2011) A DNA damage response screen identifies RHINO, a 9-1-1 and TopBP1 interacting protein required for ATR signaling. Science 332:1313–1317
de Carvalho CE, Colaiácovo MP (2006) SUMO-mediated regulation of synaptonemal complex formation during meiosis. Genes Dev 20:1986–1992
Denison C, Rudner AD, Gerber SA, Bakalarski CE, Moazed D, Gygi SP (2005) A proteomic strategy for gaining insights into protein sumoylation in yeast. Mol Cell Proteomics 4:246–254
Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94:387–398
Eladad S, Ye TZ, Hu P, Leversha M, Beresten S, Matunis MJ, Ellis NA (2005) Intra-nuclear trafficking of the BLM helicase to DNA damage-induced foci is regulated by SUMO modification. Hum Mol Genet 14:1351–1365
Gill G (2004) SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev 18:2046–2059
Hannich JT, Lewis A, Kroetz MB, Li SJ, Heide H, Emili A, Hochstrasser M (2005) Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J Biol Chem 280:4102–4110
Hartsuiker E, Bahler J, Kohli J (1998) The role of topoisomerase II in meiotic chromosome condensation and segregation in Schizosaccharomyces pombe. Mol Biol Cell 9:2739–2750
Hassold T, Hunt P (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2:280–291
Hay RT (2005) SUMO: a history of modification. Mol Cell 18:1–12
Henderson KA, Keeney S (2005) Synaptonemal complex formation: where does it start? Bioessays 27:995–998
Hoffmann ER, Borts RH (2004) Meiotic recombination intermediates and mismatch repair proteins. Cytogenet Genome Res 107:232–248
Holway AH, Hung C, Michael WM (2005) Systematic, RNA-interference-mediated identification of mus-101 modifier genes in Caenorhabditis elegans. Genetics 169:1451–1460
Hooker GW, Roeder GS (2006) A role for SUMO in meiotic chromosome synapsis. Curr Biol 16:1238–1243
Jantsch V, Pasierbek P, Mueller MM, Schweizer D, Jantsch M, Loidl J (2004) Targeted gene knockout reveals a role in meiotic recombination for ZHP-3, a Zip3-related protein in Caenorhabditis elegans. Mol Cell Biol 24:7998–8006
Johnson ES (2004) Protein modification by SUMO. Annu Rev Biochem 73:355–382
Jones D, Crowe E, Stevens TA, Candido EP (2002) Functional and phylogenetic analysis of the ubiquitylation system in Caenorhabditis elegans: ubiquitin-conjugating enzymes, ubiquitin-activating enzymes, and ubiquitin-like proteins. Genome Biol 3:0002.1–0002.15
Kim HM, Colaiácovo MP (2014) ZTF-8 Interacts with the 9-1-1 Complex and is required for DNA damage response and double-strand break repair in the C. elegans germline. PLoS Genet 10:e1004723
Kim HM, Colaiácovo MP (2015) New insights into the post-translational regulation of DNA damage response and double-strand break repair in Caenorhabditis elegans. Genetics 200:495–504
La Salle S, Sun F, Zhang XD, Matunis MJ, Handel MA (2008) Developmental control of sumoylation pathway proteins in mouse male germ cells. Dev Biol 321:227–237
Lehembre F, Badenhorst P, Muller S, Travers A, Schweisguth F, Dejean A (2000) Covalent modification of the transcriptional repressor tramtrack by the ubiquitin-related protein Smt3 in Drosophila flies. Mol Cell Biol 20:1072–1082
Li SJ, Hochstrasser M (2000) The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol Cell Biol 20:2367–2377
Meluh PB, Koshland D (1995) Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the mammalian centromere protein CENP-C. Mol Biol Cell 6:793–807
Metzler-Guillemain C, Depetris D, Luciani JJ, Mignon-Ravix C, Mitchell MJ, Mattei MG (2008) In human pachytene spermatocytes, SUMO protein is restricted to the constitutive heterochromatin. Chromosom Res 16:761–782
Nagai S, Dubrana K, Tsai-Pflugfelder M, Davidson MB, Roberts TM, Brown GW, Varela E, Hediger F, Gasser SM, Krogan NJ (2008) Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322:597–602
Page SL, Hawley RS (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20:525–558
Panse VG, Hardeland U, Werner T, Kuster B, Hurt E (2004) A proteome-wide approach identifies sumoylated substrate proteins in yeast. J Biol Chem 279:41346–41351
Pfander B, Moldovan GL, Sacher M, Hoege C, Jentsch S (2005) SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436:428–433
Rockmill B, Sym M, Scherthan H, Roeder GS (1995) Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev 9:2684–2695
Rockmill B, Fung JC, Branda SS, Roeder GS (2003) The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr Biol 13:1954–1962
Rogers RS, Inselman A, Handel MA, Matunis MJ (2004) SUMO modified proteins localize to the XY body of pachytene spermatocytes. Chromosoma 113:233–243
Sacher M, Pfander B, Hoege C, Jentsch S (2006) Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat Cell Biol 8:1284–1290
Shin JA, Choi ES, Kim HS, Ho JC, Watts FZ, Park SD, Jang YK (2005) SUMO modification is involved in the maintenance of heterochromatin stability in fission yeast. Mol Cell 19:817–828
Soustelle C, Vernis L, Freon K, Reynaud-Angelin A, Chanet R, Fabre F, Heude M (2004) A new Saccharomyces cerevisiae strain with a mutant Smt3-deconjugating Ulp1 protein is affected in DNA replication and requires Srs2 and homologous recombination for its viability. Mol Cell Biol 24:5130–5143
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 172:783–794
Talamillo A, Sanchez J, Barrio R (2008) Functional analysis of the SUMOylation pathway in Drosophila. Biochem Soc Trans 36:868–873
Torres-Rosell J, Sunjevaric I, De Piccoli G, Sacher M, Eckert-Boulet N, Reid R, Jentsch S, Rothstein R, Aragon L, Lisby M (2007) The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat Cell Biol 9:923–931
Trelles-Sticken E, Dresser ME, Scherthan H (2000) Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J Cell Biol 151:95–106
Tsubouchi T, Roeder GS (2005) A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308:870–873
Tsubouchi T, Macqueen AJ, Roeder GS (2008) Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22:3217–3226
Veaute X, Jeusset J, Soustelle C, Kowalczykowski SC, Le Cam E, Fabre F (2003) The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423:309–312
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
Vigodner M, Ishikawa T, Schlegel PN, Morris PL (2006) SUMO-1, human male germ cell development, and the androgen receptor in the testis of men with normal and abnormal spermatogenesis. Am J Physiol Endocrinol Metab 290:E1022–E1033
Villeneuve AM, Hillers KJ (2001) Whence meiosis? Cell 106:647–650
Watts FZ, Skilton A, Ho JC, Boyd LK, Trickey MA, Gardner L, Ogi FX, Outwin EA (2007) The role of Schizosaccharomyces pombe SUMO ligases in genome stability. Biochem Soc Trans 35:1379–1384
Xhemalce B, Seeler JS, Thon G, Dejean A, Arcangioli B (2004) Role of the fission yeast SUMO E3 ligase Pli1p in centromere and telomere maintenance. EMBO J 23:3844–3853
Yan W, Santti H, Janne OA, Palvimo JJ, Toppari J (2003) Expression of the E3 SUMO-1 ligases PIASx and PIAS1 during spermatogenesis in the rat. Gene Expr Patterns 3:301–308
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
Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754
Acknowledgements
Our research is supported by grants from the National Institutes of Health (R01GM072551 and R01GM105853 to M.P.C.) and the Kafker Family Research Fund.
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Nottke, A.C., Kim, HM., Colaiácovo, M.P. (2017). Wrestling with Chromosomes: The Roles of SUMO During Meiosis. In: Wilson, V. (eds) SUMO Regulation of Cellular Processes. Advances in Experimental Medicine and Biology, vol 963. Springer, Cham. https://doi.org/10.1007/978-3-319-50044-7_11
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DOI: https://doi.org/10.1007/978-3-319-50044-7_11
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