Roles of Small Ubiquitin-Related Modifiers in Male Reproductive Function

International Review of Cell and Molecular Biology

Volumn 288, Issue , 2011, Pages 227-259

  Vigodner, Margarita ^a,b  

^a YESHIVA UNIVERSITY   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Leydig cells; Myoepithelial cells; Sertoli cells; Spermatids; Spermatocytes; Spermatogenesis; Spermatogonia; Sumoylation

Indexed keywords

BRCA1 PROTEIN; DNA; N ETHYLMALEIMIDE; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN KINASE; PROTEIN UBC9; STAT PROTEIN; SUMO 1 PROTEIN; SUMO 2 PROTEIN; SUMO 3 PROTEIN; SUMO PROTEIN;

BOOK; CELL CYCLE; CELL TYPE; CELLULAR STRESS RESPONSE; CELLULAR STRESS SIGNAL; CHROMATIN STRUCTURE; DOUBLE STRANDED DNA BREAK; HISTONE MODIFICATION; HUMAN; MALE GENITAL SYSTEM FUNCTION; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SACCHAROMYCES CEREVISIAE; SEX CHROMOSOME; SOMATIC CELL; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; SUMOYLATION; SYNAPTONEMAL COMPLEX; TESTIS CELL;

EID: 79953792813     PISSN: 19376448     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386041-5.00006-6     Document Type: Chapter

References (152)

1. Agrawal N., Banerjee R. Human polycomb 2 protein is a SUMO E3 ligase and alleviates substrate-induced inhibition of cystathionine beta-synthase sumoylation. PLoS One 2008, 3:e4032.
2. Aitken R.J., Roman S.D. Antioxidant systems and oxidative stress in the testes. Adv. Exp. Med. Biol. 2008, 636:154-171.
3. Alarcon-Vargas D., Ronai Z. SUMO in cancer-wrestlers wanted. Cancer Biol. Ther. 2002, 1:237-242.
4. Albrecht M. Insights into the nature of human testicular peritubular cells. Ann. Anat. 2009, 191:532-540.
5. Alkuraya F.S., Saadi I., Lund J.J., Turbe-Doan A., Morton C.C., Maas R.L. SUMO1 haploinsufficiency leads to cleft lip and palate. Science 2006, 313:1751.
6. Amor D.J., Kalitsis P., Sumer H., Choo K.H. Building the centromere: from foundation proteins to 3D organization. Trends Cell Biol. 2004, 14:359-368.
7. Andersen J.S., Matic I., Vertegaal A.C. Identification of SUMO target proteins by quantitative proteomics. Methods Mol. Biol. 2009, 497:19-31.
8. Azuma Y., Arnaoutov A., Dasso M. SUMO-2/3 regulates topoisomerase II in mitosis. J. Cell Biol. 2003, 163:477-487.
9. Baarends W.M., Hoogerbrugge J.W., Roest H.P., Ooms M., Vreeburg J., Hoeijmakers J.H., et al. Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev. Biol. 1999, 207:322-333.
10. Baarends W.M., Wassenaar E., van der Laan R., Hoogerbrugge J., Sleddens-Linkels E., Hoeijmakers J.H., et al. Silencing of unpaired chromatin and histone H2A ubiquitination in mammalian meiosis. Mol. Cell. Biol. 2005, 25:1041-1053.
11. Baek S.H. A novel link between SUMO modification and cancer metastasis. Cell Cycle 2006, 5:1492-1495.
12. Bartek J., Hodny Z. SUMO boosts the DNA damage response barrier against cancer. Cancer Cell 2010, 17:9-11.
13. Bayer P., Arndt A., Metzger S., Mahajan R., Melchior F., Jaenicke R., et al. Structure determination of the small ubiquitin-related modifier SUMO-1. J. Mol. Biol. 1998, 280:275-286.
14. Bellve A.R., Cavicchia J.C., Millette C.F., O'Brien D.A., Bhatnagar Y.M., Dym M. Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J. Cell Biol. 1977, 74:68-85.
15. Bohren K.M., Nadkarni V., Song J.H., Gabbay K.H., Owerbach D. A M55V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. J. Biol. Chem. 2004, 279:27233-27238.
16. Brown P.W., Hwang K., Schlegel P.N., Morris P.L. 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. 2008, 23:2850-2857.
17. Burgoyne P.S., Mahadevaiah S.K., Turner J.M. The consequences of asynapsis for mammalian meiosis. Nat. Rev. Genet. 2009, 10:207-216.
18. Chen T., Liao X.P., Wen G.Q., Nong Z.G., Ouyang F., Deng Y.D., et al. Effect of SUMO-1 on mitochondria subcellular localization of alpha-synuclein and its degradation via ubiquitin-proteasome system. Zhonghua Yi Xue Yi Chuan Xue Za Zhi 2010, 27:267-271.
19. Cheng C.H., Lo Y.H., Liang S.S., Ti S.C., Lin F.M., Yeh C.H., et al. SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev. 2006, 20:2067-2081.
20. Chupreta S., Holmstrom S., Subramanian L., Iniguez-Lluhi J.A. A small conserved surface in SUMO is the critical structural determinant of its transcriptional inhibitory properties. Mol. Cell. Biol. 2005, 25:4272-4282.
21. Cobb J., Reddy R.K., Park C., Handel M.A. Analysis of expression and function of topoisomerase I and II during meiosis in male mice. Mol. Reprod. Dev. 1997, 46:489-498.
22. Cobb J., Miyaike M., Kikuchi A., Handel M.A. Meiotic events at the centromeric heterochromatin: histone H3 phosphorylation, topoisomerase II alpha localization and chromosome condensation. Chromosoma 1999, 108:412-425.
23. Cohen P.E., Pollard J.W. Regulation of meiotic recombination and prophase I progression in mammals. Bioessays 2001, 23:996-1009.
24. Cowell I.G., Aucott R., Mahadevaiah S.K., Burgoyne P.S., Huskisson N., Bongiorni S., et al. Heterochromatin, HP1 and methylation at lysine 9 of histone H3 in animals. Chromosoma 2002, 111:22-36.
25. Dann C.T., Alvarado A.L., Molyneux L.A., Denard B.S., Garbers D.L., Porteus M.H. Spermatogonial stem cell self-renewal requires OCT4, a factor downregulated during retinoic acid-induced differentiation. Stem Cells 2008, 26:2928-2937.
26. Dasso M. Emerging roles of the SUMO pathway in mitosis. Cell Div. 2008, 3:5.
27. David G., Neptune M.A., DePinho R.A. SUMO-1 modification of histone deacetylase 1 (HDAC1) modulates its biological activities. J. Biol. Chem. 2002, 277:23658-23663.
28. de Brito O.M., Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 2008, 456:605-610.
29. De Kretser D.M., Baker H.W. Infertility in men: recent advances and continuing controversies. J. Clin. Endocrinol. Metab. 1999, 84:3443-3450.
30. de Rooij D.G. Proliferation and differentiation of spermatogonial stem cells. Reproduction 2001, 121:347-354.
31. Dohmen R.J. SUMO protein modification. Biochim. Biophys. Acta 2004, 1695:113-131.
32. Dolci S., Pellegrini M., Di Agostino S., Geremia R., Rossi P. Signaling through extracellular signal-regulated kinase is required for spermatogonial proliferative response to stem cell factor. J. Biol. Chem. 2001, 276:40225-40233.
33. Dorval V., Fraser P.E. SUMO on the road to neurodegeneration. Biochim. Biophys. Acta 2007, 1773:694-706.
34. Dym M., Kokkinaki M., He Z. Spermatogonial stem cells: mouse and human comparisons. Birth Defects Res. C Embryo Today 2009, 87:27-34.
35. Escalier D., Garchon H.J. XMR is associated with the asynapsed segments of sex chromosomes in the XY body of mouse primary spermatocytes. Chromosoma 2000, 109:259-265.
36. Fernandez-Capetillo O., Mahadevaiah S.K., Celeste A., Romanienko P.J., Camerini-Otero R.D., Bonner W.M., et al. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell 2003, 4:497-508.
37. Ganesan A.K., Kho Y., Kim S.C., Chen Y., Zhao Y., White M.A. Broad spectrum identification of SUMO substrates in melanoma cells. Proteomics 2007, 7:2216-2221.
38. Geiss-Friedlander R., Melchior F. Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol. 2007, 8:947-956.
39. Geoffroy M.C., Hay R.T. An additional role for SUMO in ubiquitin-mediated proteolysis. Nat. Rev. Mol. Cell Biol. 2009, 10:564-568.
40. Gill G. Something about SUMO inhibits transcription. Curr. Opin. Genet. Dev. 2005, 15:536-541.
41. Gillot I., Matthews C., Puel D., Vidal F., Lopez P. Ret finger protein: an E3 ubiquitin ligase iuxtaposed to the XY body in meiosis. Int. J. Cell Biol. 2009, 2009:524858.
42. Golebiowski F., Matic I., Tatham M.H., Cole C., Yin Y., Nakamura A., et al. System-wide changes to SUMO modifications in response to heat shock. Sci. Signal. 2009, 2:ra24.
43. Golestaneh N., Kokkinaki M., Pant D., Jiang J., DeStefano D., Fernandez-Bueno C., et al. Pluripotent stem cells derived from adult human testes. Stem Cells Dev. 2009, 18:1115-1126.
44. Grootegoed J.A., Siep M., Baarends W.M. Molecular and cellular mechanisms in spermatogenesis. Baillières Best Pract. Res. Clin. Endocrinol. Metab. 2000, 14:331-343.
45. Guenatri M., Bailly D., Maison C., Almouzni G. Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J. Cell Biol. 2004, 166:493-505.
46. Guo W.H., Yuan L.H., Xiao Z.H., Liu D., Zhang J.X. Overexpression of SUMO-1 in hepatocellular carcinoma: a latent target for diagnosis and therapy of hepatoma. J. Cancer Res. Clin. Oncol. 2010.
47. Handel M.A. The XY body: a specialized meiotic chromatin domain. Exp. Cell Res. 2004, 296:57-63.
48. Hannoun Z., Greenhough S., Jaffray E., Hay R.T., Hay D.C. Post-translational modification by SUMO. Toxicology. 2010, 278, 288-293.
49. Haraguchi C.M., Mabuchi T., Hirata S., Shoda T., Tokumoto T., Hoshi K., et al. Possible function of caudal nuclear pocket: degradation of nucleoproteins by ubiquitin-proteasome system in rat spermatids and human sperm. J. Histochem. Cytochem. 2007, 55:585-595.
50. Hassold T., Hunt P. To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2001, 2:280-291.
51. Hazzouri M., Pivot-Pajot C., Faure A.K., Usson Y., Pelletier R., Sele B., et al. Regulated hyperacetylation of core histones during mouse spermatogenesis: involvement of histone deacetylases. Eur. J. Cell Biol. 2000, 79:950-960.
52. He Z., Kokkinaki M., Jiang J., Dobrinski I., Dym M. Isolation, characterization, and culture of human spermatogonia. Biol. Reprod. 2010, 82:363-372.
53. Hietakangas V., Anckar J., Blomster H.A., Fujimoto M., Palvimo J.J., Nakai A., et al. PDSM, a motif for phosphorylation-dependent SUMO modification. Proc. Natl. Acad. Sci. USA 2006, 103:45-50.
54. Hofmann M.C., Braydich-Stolle L., Dettin L., Johnson E., Dym M. Immortalization of mouse germ line stem cells. Stem Cells 2005, 23:200-210.
55. Hoyer-Fender S., Czirr E., Radde R., Turner J.M., Mahadevaiah S.K., Pehrson J.R., et al. Localisation of histone macroH2A1.2 to the XY-body is not a response to the presence of asynapsed chromosome axes. J. Cell Sci. 2004, 117:189-198.
56. Hsiao H.H., Meulmeester E., Frank B.T., Melchior F., Urlaub H. "ChopN Spice," a mass spectrometric approach that allows identification of endogenous small ubiquitin-like modifier-conjugated peptides. Mol. Cell Proteomics. 2009, 8:2664-2675.
57. Jadhav T., Wooten M.W. Defining an embedded code for protein ubiquitination. J. Proteomics Bioinform. 2009, 2:316.
58. Janne O.A., Moilanen A.M., Poukka H., Rouleau N., Karvonen U., Kotaja N., et al. Androgen-receptor-interacting nuclear proteins. Biochem. Soc. Trans. 2000, 28:401-405.
59. Jenuwein T., Allis C.D. Translating the histone code. Science 2001, 293:1074-1080.
60. Jeram S.M., Srikumar T., Pedrioli P.G., Raught B. Using mass spectrometry to identify ubiquitin and ubiquitin-like protein conjugation sites. Proteomics 2009, 9:922-934.
61. Johnson E.S. Protein modification by SUMO. Annu. Rev. Biochem. 2004, 73:355-382.
62. Kerscher O. SUMO junction-what's your function? New insights through SUMO-interacting motifs. EMBO Rep. 2007, 8:550-555.
63. Kerscher O., Felberbaum R., Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 2006, 22:159-180.
64. Kim J.H., Baek S.H. Emerging roles of desumoylating enzymes. Biochim. Biophys. Acta 2009, 1792:155-162.
65. Kirsh O., Seeler J.S., Pichler A., Gast A., Muller S., Miska E., et al. The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. EMBO J. 2002, 21:2682-2691.
66. Kotaja N., Vihinen M., Palvimo J.J., Janne O.A. Androgen receptor-interacting protein 3 and other PIAS proteins cooperate with glucocorticoid receptor-interacting protein 1 in steroid receptor-dependent signaling. J. Biol. Chem. 2002, 277:17781-17788.
67. La Salle S., Sun F., Zhang X.D., Matunis M.J., Handel M.A. Developmental control of sumoylation pathway proteins in mouse male germ cells. Dev. Biol. 2008, 321:227-237.
68. Leduc F., Maquennehan V., Nkoma G.B., Boissonneault G. DNA damage response during chromatin remodeling in elongating spermatids of mice. Biol. Reprod. 2008, 78:324-332.
69. Lee M.T., Bachant J. SUMO modification of DNA topoisomerase II: trying to get a CENse of it all. DNA Repair (Amst.) 2009, 8:557-568.
70. Leke R.J., Oduma J.A., Bassol-Mayagoitia S., Bacha A.M., Grigor K.M. Regional and geographical variations in infertility: effects of environmental, cultural, and socioeconomic factors. Environ. Health Perspect. 1993, 101(Suppl. 2):73-80.
71. Li M., Guo D., Isales C.M., Eizirik D.L., Atkinson M., She J.X., et al. SUMO wrestling with type 1 diabetes. J. Mol. Med. 2005, 83:504-513.
72. Li T., Santockyte R., Shen R.F., Tekle E., Wang G., Yang D.C., et al. Expression of SUMO-2/3 induced senescence through p53- and pRB-mediated pathways. J. Biol. Chem. 2006, 281:36221-36227.
73. Lin D.Y., Huang Y.S., Jeng J.C., Kuo H.Y., Chang C.C., Chao T.T., et al. Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. Mol. Cell 2006, 24:341-354.
74. Ling Y., Sankpal U.T., Robertson A.K., McNally J.G., Karpova T., Robertson K.D. Modification of de novo DNA methyltransferase 3a (Dnmt3a) by SUMO-1 modulates its interaction with histone deacetylases (HDACs) and its capacity to repress transcription. Nucleic Acids Res. 2004, 32:598-610.
75. Liu B., Liao J., Rao X., Kushner S.A., Chung C.D., Chang D.D., et al. Inhibition of Stat1-mediated gene activation by PIAS1. Proc. Natl. Acad. Sci. USA 1998, 95:10626-10631.
76. Luetjens C.M., Didolkar A., Kliesch S., Paulus W., Jeibmann A., Bocker W., et al. Tissue expression of the nuclear progesterone receptor in male non-human primates and men. J. Endocrinol. 2006, 189:529-539.
77. Luo J., Rodriguez-Sosa J.R., Tang L., Bondareva A., Megee S., Dobrinski I. Expression pattern of acetylated alpha-tubulin in porcine spermatogonia. Mol. Reprod. Dev. 2010, 77:348-352.
78. Lyst M.J., Stancheva I. A role for SUMO modification in transcriptional repression and activation. Biochem. Soc. Trans. 2007, 35:1389-1392.
79. Mahadevaiah S.K., Turner J.M., Baudat F., Rogakou E.P., de Boer P., Blanco-Rodriguez J., et al. Recombinational DNA double-strand breaks in mice precede synapsis. Nat. Genet. 2001, 27:271-276.
80. Marchiani S., Tamburrino L., Giuliano L., Nosi D., Sarli V., Gandini L., et al. Sumo1-ylation of human spermatozoa and its relationship with semen quality. Int. J. Androl. 2010.
81. Matafora V., D'Amato A., Mori S., Blasi F., Bachi A. Proteomics analysis of nucleolar SUMO-1 target proteins upon proteasome inhibition. Mol. Cell. Proteomics 2009, 8:2243-2255.
82. Matsuoka S., Ballif B.A., Smogorzewska A., McDonald E.R., Hurov K.E., Luo J., et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007, 316:1160-1166.
83. Matsuura T., Shimono Y., Kawai K., Murakami H., Urano T., Niwa Y., et al. PIAS proteins are involved in the SUMO-1 modification, intracellular translocation and transcriptional repressive activity of RET finger protein. Exp. Cell Res. 2005, 308:65-77.
84. Matunis M.J., Wu J., Blobel G. SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex. J. Cell Biol. 1998, 140:499-509.
85. Mauduit C., Hamamah S., Benahmed M. Stem cell factor/c-kit system in spermatogenesis. Hum. Reprod. Update 1999, 5:535-545.
86. Metzler-Guillemain C., Depetris D., Luciani J.J., Mignon-Ravix C., Mitchell M.J., Mattei M.G. In human pachytene spermatocytes, SUMO protein is restricted to the constitutive heterochromatin. Chromosome Res. 2008, 16:761-782.
87. Moilanen A.M., Karvonen U., Poukka H., Yan W., Toppari J., Janne O.A., et al. A testis-specific androgen receptor coregulator that belongs to a novel family of nuclear proteins. J. Biol. Chem. 1999, 274:3700-3704.
88. Morris J.R. More modifiers move on DNA damage. Cancer Res. 2010, 70:3861-3863.
89. Morris J.R. SUMO in the mammalian response to DNA damage. Biochem. Soc. Trans. 2010, 38:92-97.
90. Morris J.R., Boutell C., Keppler M., Densham R., Weekes D., Alamshah A., et al. The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 2009, 462:886-890.
91. Motzkus D., Singh P.B., Hoyer-Fender S. M31, a murine homolog of Drosophila HP1, is concentrated in the XY body during spermatogenesis. Cytogenet. Cell Genet. 1999, 86:83-88.
92. Mruk D.D., Cheng C.Y. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr. Rev. 2004, 25:747-806.
93. Mukhopadhyay D., Dasso M. Modification in reverse: the SUMO proteases. Trends Biochem. Sci. 2007, 32:286-295.
94. Nacerddine K., Lehembre F., Bhaumik M., Artus J., Cohen-Tannoudji M., Babinet C., et al. The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev. Cell 2005, 9:769-779.
95. Namekawa S.H., Park P.J., Zhang L.F., Shima J.E., McCarrey J.R., Griswold M.D., et al. Postmeiotic sex chromatin in the male germline of mice. Curr. Biol. 2006, 16:660-667.
96. Nathan D., Ingvarsdottir K., Sterner D.E., Bylebyl G.R., Dokmanovic M., Dorsey J.A., et al. Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. Genes Dev. 2006, 20:966-976.
97. Neuspiel M., Schauss A.C., Braschi E., Zunino R., Rippstein P., Rachubinski R.A., et al. Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr. Biol. 2008, 18:102-108.
98. Nishimune Y., Tanaka H. Infertility caused by polymorphisms or mutations in spermatogenesis-specific genes. J. Androl. 2006, 27:326-334.
99. O'Carroll D., Scherthan H., Peters A.H., Opravil S., Haynes A.R., Laible G., et al. Isolation and characterization of Suv39h2, a second histone H3 methyltransferase gene that displays testis-specific expression. Mol. Cell. Biol. 2000, 20:9423-9433.
100. Palvimo J.J. PIAS proteins as regulators of small ubiquitin-related modifier (SUMO) modifications and transcription. Biochem. Soc. Trans. 2007, 35:1405-1408.
101. Poukka H., Karvonen U., Janne O.A., Palvimo J.J. Covalent modification of the androgen receptor by small ubiquitin-like modifier 1 (SUMO-1). Proc. Natl. Acad. Sci. USA 2000, 97:14145-14150.
102. Poukka H., Karvonen U., Yoshikawa N., Tanaka H., Palvimo J.J., Janne O.A. The RING finger protein SNURF modulates nuclear trafficking of the androgen receptor. J. Cell Sci. 2000, 113(Pt 17):2991-3001.
103. Prudden J., Pebernard S., Raffa G., Slavin D.A., Perry J.J., Tainer J.A., et al. SUMO-targeted ubiquitin ligases in genome stability. EMBO J. 2007, 26:4089-4101.
104. Rajendra R., Malegaonkar D., Pungaliya P., Marshall H., Rasheed Z., Brownell J., et al. Topors functions as an E3 ubiquitin ligase with specific E2 enzymes and ubiquitinates p53. J. Biol. Chem. 2004, 279:36440-36444.
105. Ren J., Gao X., Jin C., Zhu M., Wang X., Shaw A., et al. Systematic study of protein sumoylation: development of a site-specific predictor of SUMOsp 2.0. Proteomics 2009, 9:3409-3412.
106. Rodriguez M.S., Dargemont C., Hay R.T. SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 2001, 276:12654-12659.
107. Rogers R.S., Inselman A., Handel M.A., Matunis M.J. SUMO modified proteins localize to the XY body of pachytene spermatocytes. Chromosoma 2004, 113:233-243.
108. Roth W., Sustmann C., Kieslinger M., Gilmozzi A., Irmer D., Kremmer E., et al. PIASy-deficient mice display modest defects in IFN and Wnt signaling. J. Immunol. 2004, 173:6189-6199.
109. Rytinki M.M., Kaikkonen S., Pehkonen P., Jaaskelainen T., Palvimo J.J. PIAS proteins: pleiotropic interactors associated with SUMO. Cell. Mol. Life Sci. 2009, 66:3029-3041.
110. Ryu H., Furuta M., Kirkpatrick D., Gygi S.P., Azuma Y. PIASy-dependent SUMOylation regulates DNA topoisomerase II{alpha} activity. J. Cell Biol. 2010, 191:783-794.
111. Sacher M., Pfander B., Hoege C., Jentsch S. Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat. Cell Biol. 2006, 8:1284-1290.
112. Saitoh H., Hinchey J. Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 2000, 275:6252-6258.
113. Saitoh H., Pu R., Cavenagh M., Dasso M. RanBP2 associates with Ubc9p and a modified form of RanGAP1. Proc. Natl. Acad. Sci. USA 1997, 94:3736-3741.
114. Santti H., Mikkonen L., Anand A., Hirvonen-Santti S., Toppari J., Panhuysen M., et al. Disruption of the murine PIASx gene results in reduced testis weight. J. Mol. Endocrinol. 2005, 34:645-654.
115. Sarge K.D., Park-Sarge O.K. Detection of proteins sumoylated in vivo and in vitro. Methods Mol. Biol. 2009, 590:265-277.
116. Sarge K.D., Park-Sarge O.K. Sumoylation and human disease pathogenesis. Trends Biochem. Sci. 2009, 34:200-205.
117. Scheschonka A., Tang Z., Betz H. Sumoylation in neurons: nuclear and synaptic roles?. Trends Neurosci. 2007, 30:85-91.
118. Shao R., Zhang F.P., Rung E., Palvimo J.J., Huhtaniemi I., Billig H. Inhibition of small ubiquitin-related modifier-1 expression by luteinizing hormone receptor stimulation is linked to induction of progesterone receptor during ovulation in mouse granulosa cells. Endocrinology 2004, 145:384-392.
119. Shiio Y., Eisenman R.N. Histone sumoylation is associated with transcriptional repression. Proc. Natl. Acad. Sci. USA 2003, 100:13225-13230.
120. Shrivastava V., Pekar M., Grosser E., Im J., Vigodner M. SUMO proteins are involved in the stress response during spermatogenesis and are localized to DNA double-strand breaks in germ cells. Reproduction 2010, 139:999-1010.
121. Skinner M.K., Fritz I.B. Androgen stimulation of Sertoli cell function is enhanced by peritubular cells. Mol. Cell. Endocrinol. 1985, 40:115-122.
122. Song J., Durrin L.K., Wilkinson T.A., Krontiris T.G., Chen Y. Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl. Acad. Sci. USA 2004, 101:14373-14378.
123. Song J., Zhang Z., Hu W., Chen Y. Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif: a reversal of the bound orientation. J. Biol. Chem. 2005, 280:40122-40129.
124. Takehashi M., Kanatsu-Shinohara M., Shinohara T. Generation of genetically modified animals using spermatogonial stem cells. Dev. Growth Differ. 2010, 52:303-310.
125. Tan J., Hall S.H., Hamil K.G., Grossman G., Petrusz P., Liao J., et al. Protein inhibitor of activated STAT-1 (signal transducer and activator of transcription-1) is a nuclear receptor coregulator expressed in human testis. Mol. Endocrinol. 2000, 14:14-26.
126. Tan J.A., Hall S.H., Hamil K.G., Grossman G., Petrusz P., French F.S. Protein inhibitors of activated STAT resemble scaffold attachment factors and function as interacting nuclear receptor coregulators. J. Biol. Chem. 2002, 277:16993-17001.
127. Tatham M.H., Geoffroy M.C., Shen L., Plechanovova A., Hattersley N., Jaffray E.G., et al. RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 2008, 10:538-546.
128. Tatham M.H., Rodriguez M.S., Xirodimas D.P., Hay R.T. Detection of protein SUMOylation in vivo. Nat. Protoc. 2009, 4:1363-1371.
129. Tempe D., Piechaczyk M., Bossis G. SUMO under stress. Biochem. Soc. Trans. 2008, 36:874-878.
130. Turner J.M. Meiotic sex chromosome inactivation. Development 2007, 134:1823-1831.
131. Turner J.M., Aprelikova O., Xu X., Wang R., Kim S., Chandramouli G.V., et al. BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr. Biol. 2004, 14:2135-2142.
132. Turner J.M., Mahadevaiah S.K., Fernandez-Capetillo O., Nussenzweig A., Xu X., Deng C.X., et al. Silencing of unsynapsed meiotic chromosomes in the mouse. Nat. Genet. 2005, 37:41-47.
133. Turner J.M., Mahadevaiah S.K., Ellis P.J., Mitchell M.J., Burgoyne P.S. Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids. Dev. Cell 2006, 10:521-529.
134. Vigodner M. Sumoylation precedes accumulation of phosphorylated H2AX on sex chromosomes during their meiotic inactivation. Chromosome Res. 2009, 17:37-45.
135. Vigodner M., Morris P.L. 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. 2005, 282:480-492.
136. Vigodner M., Ishikawa T., Schlegel P.N., Morris P.L. 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. 2006, 290:E1022-E1033.
137. Visconti P.E. Understanding the molecular basis of sperm capacitation through kinase design. Proc. Natl. Acad. Sci. USA 2009, 106:667-668.
138. Wang Y., Dasso M. SUMOylation and deSUMOylation at a glance. J. Cell Sci. 2009, 122:4249-4252.
139. Wang J., Schwartz R.J. Sumoylation and regulation of cardiac gene expression. Circ. Res. 2010, 107:19-29.
140. Weger S., Hammer E., Heilbronn R. Topors acts as a SUMO-1 E3 ligase for p53 in vitro and in vivo. FEBS Lett. 2005, 579:5007-5012.
141. Wei F., Scholer H.R., Atchison M.L. Sumoylation of Oct4 enhances its stability, DNA binding, and transactivation. J. Biol. Chem. 2007, 282:21551-21560.
142. Weinbauer G.F., Wessels J. 'Paracrine' control of spermatogenesis. Andrologia 1999, 31:249-262.
143. Wilkinson K.A., Henley J.M. Mechanisms, regulation and consequences of protein SUMOylation. Biochem. J. 2010, 428:133-145.
144. Wong K.A., Kim R., Christofk H., Gao J., Lawson G., Wu H. Protein inhibitor of activated STAT Y (PIASy) and a splice variant lacking exon 6 enhance sumoylation but are not essential for embryogenesis and adult life. Mol. Cell. Biol. 2004, 24:5577-5586.
145. Yan D., Davis F.J., Sharrocks A.D., Im H.J. Emerging roles of SUMO modification in arthritis. Gene 2010, 466:1-15.
146. Yang S.H., Sharrocks A.D. Interplay of the SUMO and MAP kinase pathways. Ernst Schering Res. Found. Workshop 2006, (57):193-209.
147. Yeh E.T. SUMOylation and De-SUMOylation: wrestling with life's processes. J. Biol. Chem. 2009, 284:8223-8227.
148. Yeh E.T., Gong L., Kamitani T. Ubiquitin-like proteins: new wines in new bottles. Gene 2000, 248:1-14.
149. Zhang J., Wong C.H., Xia W., Mruk D.D., Lee N.P., Lee W.M., et al. Regulation of Sertoli-germ cell adherens junction dynamics via changes in protein-protein interactions of the N-cadherin-beta-catenin protein complex which are possibly mediated by c-Src and myotubularin-related protein 2: an in vivo study using an androgen suppression model. Endocrinology 2005, 146:1268-1284.
150. Zhang F.P., Mikkonen L., Toppari J., Palvimo J.J., Thesleff I., Janne O.A. Sumo-1 function is dispensable in normal mouse development. Mol. Cell. Biol. 2008, 28:5381-5390.
151. Zhang X.D., Goeres J., Zhang H., Yen T.J., Porter A.C., Matunis M.J. SUMO-2/3 modification and binding regulate the association of CENP-E with kinetochores and progression through mitosis. Mol. Cell 2008, 29:729-741.
152. Zhu L., Doyle T.J., Kim K.H. Retinoic acid modulates the subcellular localization of small ubiquitin-related modifier-2/3 (SUMO-2/3) in the testis. J. Androl. 2010, 31:406-418.