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

Developmental Biology

Volumn 282, Issue 2, 2005, Pages 480-492

  Vigodner, Margarita ^a   Morris, Patricia L ^a,b  

^a POPULATION COUNCIL   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Centrosome; Chromatin; Manchette; Meiosis; Spermatocyte; Spermiogenesis; STAT; Testis; XY body

Indexed keywords

SUMO 1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ISOLATION; CELL SHAPE; CELL SPECIFICITY; CHROMATIN CONDENSATION; CHROMOSOME CONDENSATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GERM CELL; GONAD DEVELOPMENT; LEYDIG CELL; MALE; MEIOSIS; MICROTUBULE ASSEMBLY; MITOSIS INDEX; MOUSE; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEMINIFEROUS TUBULE; SERTOLI CELL; SEX CHROMOSOME; SOMATIC CELL; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON MATURATION; WESTERN BLOTTING; X CHROMOSOME; Y CHROMOSOME;

EID: 20444369153     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2005.03.034     Document Type: Article

References (83)

1. T. Arora, B. Liu, H. He, J. Kim, T.L. Murphy, K.M. Murphy, R.L. Modlin, and K. Shuai PIASx is a transcriptional co-repressor of signal transducer and activator of transcription 4 J. Biol. Chem. 278 2003 21327 21330
2. W.M. Baarends, J.W. Hoogerbrugge, H.P. Roest, M. Ooms, J. Vreeburg, J.H. Hoeijmakers, and J.A. Grootegoed Histone ubiquitination and chromatin remodeling in mouse spermatogenesis Dev. Biol. 207 1999 322 333
3. W.M. Baarends, H.P. Roest, and J.A. Grootegoed The ubiquitin system in gametogenesis Mol. Cell. Endocrinol. 151 1999 5 16
4. W.M. Baarends, E. Wassenaar, J.W. Hoogerbrugge, G. van Cappellen, H.P. Roest, J. Vreeburg, M. Ooms, J.H. Hoeijmakers, and J.A. Grootegoed Loss of HR6B ubiquitin-conjugating activity results in damaged synaptonemal complex structure and increased crossing-over frequency during the male meiotic prophase Mol. Cell. Biol. 23 2003 1151 1162
5. U.M. Bauer, S. Schneider-Hirsch, S. Reinhardt, R. Benavente, and A. Maelicke The murine nuclear orphan receptor GCNF is expressed in the XY body of primary spermatocytes FEBS Lett. 439 1998 208 214
6. C. Bebington, F.J. Doherty, and S.D. Fleming The possible biological and reproductive functions of ubiquitin Hum. Reprod. Update 7 2001 102 111
7. G. Berruti, and E. Martegani mUBPy and MSJ-1, a deubiquitinating enzyme and a molecular chaperone specifically expressed in testis, associate with the acrosome and centrosome in mouse germ cells Ann. N. Y. Acad. Sci. 973 2002 5 7
8. B.R. Brinkley, S.L. Brenner, J.M. Hall, A. Tousson, R.D. Balczon, and M.M. Valdivia Arrangements of kinetochores in mouse cells during meiosis and spermiogenesis Chromosoma 94 1986 309 317
9. W.R. Bruce, R. Furrer, R.B. Goldberg, M.L. Meistrich, and B. Mintz Genetic control of the kinetics of mouse spermatogenesis Genet. Res. 22 1973 155 167
10. Y. Clermont, and M. Antar Duration of the cycle of the seminiferous epithelium and the spermatogonial renewal in the monkey Macaca arctoides Am. J. Anat. 136 1973 153 165
11. A. Cole, M.L. Meistrich, L.M. Cherry, and P.K. Trostle-Weige Nuclear and manchette development in spermatids of normal and azh/azh mutant mice Biol. Reprod. 38 1988 385 401
12. M. Dasso Running on Ran: nuclear transport and the mitotic spindle Cell 104 2001 321 324
13. D.G. de Rooij, and L.D. Russell All you wanted to know about spermatogonia but were afraid to ask J. Androl. 21 2000 776 798
14. D. Escalier, and H.J. Garchon XMR is associated with the asynapsed segments of sex chromosomes in the XY body of mouse primary spermatocytes Chromosoma 109 2000 259 265
15. O. Fernandez-Capetillo, S.K. Mahadevaiah, A. Celeste, P.J. Romanienko, R.D. Camerini-Otero, W.M. Bonner, K. Manova, P. Burgoyne, and A. Nussenzweig H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis Dev. Cell 4 2003 497 508
16. G. Gill SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev. 18 2004 2046 2059
17. W. Goedecke, M. Eijpe, H.H. Offenberg, M. van Aalderen, and C. Heyting Mre11 and Ku70 interact in somatic cells, but are differentially expressed in early meiosis Nat. Genet. 23 1999 194 198
18. M. Guttenbach, M.J. Martinez-Exposito, W. Engel, and M. Schmid Interphase chromosome arrangement in Sertoli cells of adult mice Biol. Reprod. 54 1996 980 986
19. M.A. Handel The XY body: a specialized meiotic chromatin domain Exp. Cell Res. 296 2004 57 63
20. J. Hemelaar, A. Borodovsky, B.M. Kessler, D. Reverter, J. Cook, N. Kolli, T. Gan-Erdene, K.D. Wilkinson, G. Gill, C.D. Lima, H.L. Ploegh, and H. Ovaa Specific and covalent targeting of conjugating and deconjugating enzymes of ubiquitin-like proteins Mol. Cell. Biol. 24 2004 84 95
21. G. Herrada, and D.J. Wolgemuth The mouse transcription factor Stat4 is expressed in haploid male germ cells and is present in the perinuclear theca of spermatozoa J. Cell Sci. 110 1997 1543 1553
22. S. Hoyer-Fender Molecular aspects of XY body formation Cytogenet. Genome. Res. 103 2003 245 255
23. S. Hoyer-Fender, C. Costanzi, and J.R. Pehrson Histone macroH2A1.2 is concentrated in the XY-body by the early pachytene stage of spermatogenesis Exp. Cell Res. 258 2000 254 260
24. S. Hoyer-Fender, P.B. Singh, and D. Motzkus The murine heterochromatin protein M31 is associated with the chromocenter in round spermatids and is a component of mature spermatozoa Exp. Cell Res. 254 2000 72 79
25. S. Hoyer-Fender, E. Czirr, R. Radde, J.M. Turner, S.K. Mahadevaiah, J.R. Pehrson, and P.S. Burgoyne Localisation of histone macroH2A1.2 to the XY-body is not a response to the presence of asynapsed chromosome axes J. Cell Sci. 117 2004 189 198
26. S. Jenab, and S. Morris Testicular leukemia inhibitory factor (LIF) and LIF receptor mediate phosphorylation of signal transducers and activators of transcription (STAT)-3 and STAT-1 and induce c-fos transcription and activator protein-1 activation in rat Sertoli but not germ cells Endocrinology 139 1998 1883 1890
27. T. Jenuwein, and C.D. Allis Translating the histone code Science 293 2001 1074 1080
28. E.S. Johnson Protein modification by SUMO Annu. Rev. Biochem. 73 2004 355 382
29. M. Kanzaki, and P.L. Morris Identification and regulation of testicular interferon-gamma (IFNgamma) receptor subunits: IFNgamma enhances interferon regulatory factor-1 and interleukin-1beta converting enzyme expression Endocrinology 139 1998 2636 2644
30. M. Kanzaki, and P.L. Morris Growth hormone regulates steroidogenic acute regulatory protein expression and steroidogenesis in Leydig cell progenitors Endocrinology 140 1999 1681 1686
31. A. Kato, Y. Nagata, and K. Todokoro Delta-tubulin is a component of intercellular bridges and both the early and mature perinuclear rings during spermatogenesis Dev. Biol. 269 2004 196 205
32. A.M. Khalil, F.Z. Boyar, and D.J. Driscoll Dynamic histone modifications mark sex chromosome inactivation and reactivation during mammalian spermatogenesis Proc. Natl. Acad. Sci. U. S. A. 101 2004 16583 16587
33. A.L. Kierszenbaum Intramanchette transport (IMT): managing the making of the spermatid head, centrosome, and tail Mol. Reprod. Dev. 63 2002 1 4
34. A.L. Kierszenbaum, and L.L. Tres Bypassing natural sperm selection during fertilization: the azh mutant offspring experience and the alternative of spermiogenesis in vitro Mol. Cell. Endocrinol. 187 2002 133 138
35. A.L. Kierszenbaum, M. Gil, E. Rivkin, and L.L. Tres Ran, a GTP-binding protein involved in nucleocytoplasmic transport and microtubule nucleation, relocates from the manchette to the centrosome region during rat spermiogenesis Mol. Reprod. Dev. 63 2002 131 140
36. A.L. Kierszenbaum, E. Rivkin, and L.L. Tres Acroplaxome, an F-actin-keratin-containing plate, anchors the acrosome to the nucleus during shaping of the spermatid head Mol. Biol. Cell 14 2003 4628 4640
37. A.L. Kierszenbaum, L.L. Tres, E. Rivkin, N. Kang-Decker, and J.M. van Deursen The acroplaxome is the docking site of Golgi-derived myosin Va/Rab27a/b-containing proacrosomal vesicles in wild-type and Hrb mutant mouse spermatids Biol. Reprod. 70 2004 1400 1410
38. K.I. Kim, S.H. Baek, Y.J. Jeon, S. Nishimori, T. Suzuki, S. Uchida, N. Shimbara, H. Saitoh, K. Tanaka, and C.H. Chung A new SUMO-1-specific protease, SUSP1, that is highly expressed in reproductive organs J. Biol. Chem. 275 2000 14102 14106
39. N. Kotaja, M. Vihinen, J.J. Palvimo, and O.A. Janne Androgen receptor-interacting protein 3 and other PIAS proteins cooperate with glucocorticoid receptor-interacting protein 1 in steroid receptor-dependent signaling J. Biol. Chem. 277 2002 17781 17788
40. M. Kralewski, and R. Benavente XY body formation during rat spermatogenesis: an immunocytochemical study using antibodies against XY body-associated proteins Chromosoma 106 1997 304 307
41. M. Kralewski, A. Novello, and R. Benavente A novel Mr 77,000 protein of the XY body of mammalian spermatocytes: its localization in normal animals and in Searle's translocation carriers Chromosoma 106 1997 160 167
42. Y. Le Drean, N. Mincheneau, P. Le Goff, and D. Michel Potentiation of glucocorticoid receptor transcriptional activity by sumoylation Endocrinology 143 2002 3482 3489
43. F.J. Longo, and S. Cook Formation of the perinuclear theca in spermatozoa of diverse mammalian species: relationship of the manchette and multiple band polypeptides Mol. Reprod. Dev. 28 1991 380 393
44. S.K. Mahadevaiah, J.M. Turner, F. Baudat, E.P. Rogakou, P. de Boer, J. Blanco-Rodriguez, M. Jasin, S. Keeney, W.M. Bonner, and P.S. Burgoyne Recombinational DNA double-strand breaks in mice precede synapsis Nat. Genet. 27 2001 271 276
45. G. Manandhar, P. Sutovsky, H.C. Joshi, T. Stearns, and G. Schatten Centrosome reduction during mouse spermiogenesis Dev. Biol. 203 1998 424 434
46. G. Manandhar, C. Simerly, J.L. Salisbury, and G. Schatten Centriole and centrin degeneration during mouse spermiogenesis Cell Motil. Cytoskeleton 43 1999 137 144
47. G. Manandhar, C. Simerly, and G. Schatten Highly degenerated distal centrioles in rhesus and human spermatozoa Hum. Reprod. 15 2000 256 263
48. M.J. Matunis, J. Wu, and G. Blobel SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex J. Cell Biol. 140 1998 499 509
49. M.L. Meistrich, W.R. Bruce, and Y. Clermont Cellular composition of fractions of mouse testis cells following velocity sedimentation separation Exp. Cell Res. 79 1973 213 227
50. M.L. Meistrich, P.K. Trostle-Weige, and J.E. Womack Mapping of the azh locus to mouse chromosome 4 J. Hered. 83 1992 56 61
51. K. Mochida, L.L. Tres, and A.L. Kierszenbaum Isolation of the rat spermatid manchette and its perinuclear ring Dev. Biol. 200 1998 46 56
52. D. Motzkus, P.B. Singh, and S. Hoyer-Fender M31, a murine homolog of Drosophila HP1, is concentrated in the XY body during spermatogenesis Cytogenet. Cell Genet. 86 1999 83 88
53. S. Muller, A. Ledl, and D. Schmidt SUMO: a regulator of gene expression and genome integrity Oncogene 23 2004 1998 2008
54. R. Oko, and D. Maravei Distribution and possible role of perinuclear theca proteins during bovine spermiogenesis Microsc. Res. Tech. 32 1995 520 532
55. A. Pichler, and F. Melchior Ubiquitin-related modifier SUMO1 and nucleocytoplasmic transport Traffic 3 2002 381 387
56. H. Poukka, P. Aarnisalo, H. Santti, O.A. Janne, and J.J. Palvimo Coregulator small nuclear RING finger protein (SNURF) enhances Sp1- and steroid receptor-mediated transcription by different mechanisms J. Biol. Chem. 275 2000 571 579
57. H. Poukka, U. Karvonen, O.A. Janne, and J.J. Palvimo Covalent modification of the androgen receptor by small ubiquitin-like modifier 1 (SUMO-1) Proc. Natl. Acad. Sci. U. S. A. 97 2000 14145 14150
58. H. Poukka, U. Karvonen, N. Yoshikawa, H. Tanaka, J.J. Palvimo, and O.A. Janne The RING finger protein SNURF modulates nuclear trafficking of the androgen receptor J. Cell Sci. 113 2000 2991 3001
59. J.B. Rattner, and G. Olson Observations on the fine structure of the nuclear ring of the mammalian spermatid J. Ultrastruct. Res. 43 1973 438 444
60. R.S. Rogers, A. Inselman, M.A. Handel, and M.J. Matunis SUMO modified proteins localize to the XY body of pachytene spermatocytes Chromosoma 113 2004 233 243
61. G. Rosas-Acosta, W.K. Russell, A. Deyrieux, D.H. Russell, and V.G. Wilson A universal strategy for proteomic studies of SUMO and other ubiquitin-like modifiers Mol. Cell Proteomics 4 2005 56 72
62. L. Russell, R. Ettlin, A. Sinha Hikim, and E. Clegg Histological and Histopathological Evaluation of the Testis 1990 Cache River Press Florida
63. L.D. Russell, J.A. Russell, G.R. MacGregor, and M.L. Meistrich Linkage of manchette microtubules to the nuclear envelope and observations of the role of the manchette in nuclear shaping during spermiogenesis in rodents Am. J. Anat. 192 1991 97 120
64. H. Santti, L. Mikkonen, S. Hirvonen-Santti, J. Toppari, O.A. Janne, and J.J. Palvimo Identification of a short PIASx gene promoter that directs male germ cell-specific transcription in vivo Biochem. Biophys. Res. Commun. 308 2003 139 147
65. D.C. Schwartz, and M. Hochstrasser A superfamily of protein tags: ubiquitin, SUMO and related modifiers Trends Biochem. Sci. 28 2003 321 328
66. J.S. Seeler, and A. Dejean Nuclear and unclear functions of SUMO Nat. Rev., Mol. Cell Biol. 4 2003 690 699
67. R. Shao, F.P. Zhang, E. Rung, J.J. Palvimo, I. Huhtaniemi, and H. Billig 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 145 2004 384 392
68. Y. Shiio, and R.N. Eisenman Histone sumoylation is associated with transcriptional repression Proc. Natl. Acad. Sci. U. S. A. 100 2003 13225 13230
69. A. Smith, and R. Benavente Meiosis-specific protein selectively associated with sex chromosomes of rat pachytene spermatocytes Proc. Natl. Acad. Sci. U. S. A. 89 1992 6938 6942
70. A. Smith, and R. Benavente An Mr 51,000 protein of mammalian spermatogenic cells that is common to the whole XY body and centromeric heterochromatin of autosomes Chromosoma 103 1995 591 596
71. O.W. Smrzka, N. Delgehyr, and M. Bornens Tissue-specific expression and subcellular localisation of mammalian delta-tubulin Curr. Biol. 10 2000 413 416
72. A.J. Solari The spatial relationship of the X and Y chromosomes during meiotic prophase in mouse spermatocytes Chromosoma 29 1970 217 236
73. P. Sutovsky Ubiquitin-dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: killing three birds with one stone Microsc. Res. Tech. 61 2003 88 102
74. J. Tan, S.H. Hall, K.G. Hamil, G. Grossman, P. Petrusz, J. Liao, K. Shuai, and F.S. French Protein inhibitor of activated STAT-1 (signal transducer and activator of transcription-1) is a nuclear receptor coregulator expressed in human testis Mol. Endocrinol. 14 2000 14 26
75. M. Tarsounas, R.E. Pearlman, and P.B. Moens CLIP-50 immunolocalization during mouse spermiogenesis suggests a role in shaping the sperm nucleus Dev. Biol. 236 2001 400 410
76. J.M. Turner, S.K. Mahadevaiah, R. Benavente, H.H. Offenberg, C. Heyting, and P.S. Burgoyne Analysis of male meiotic "sex body" proteins during XY female meiosis provides new insights into their functions Chromosoma 109 2000 426 432
77. J.M. Turner, S.K. Mahadevaiah, O. Fernandez-Capetillo, A. Nussenzweig, X. Xu, C.X. Deng, and P.S. Burgoyne Silencing of unsynapsed meiotic chromosomes in the mouse Nat. Genet. 37 2005 41 47
78. A. Verger, J. Perdomo, and M. Crossley Modification with SUMO. A role in transcriptional regulation EMBO Rep. 4 2003 137 142
79. M. Vigodner, L.M. Lewin, T. Glaser, L. Shochat, L. Mittelman, and R. Golan Use of confocal microscopy for the study of spermatogenesis Methods Cell Sci. 24 2002 169 180
80. C. Wiese, and Y. Zheng Gamma-tubulin complexes and their interaction with microtubule-organizing centers Curr. Opin. Struct. Biol. 9 1999 250 259
81. S. Wormald, and D.J. Hilton Inhibitors of cytokine signal transduction J. Biol. Chem. 279 2004 821 824
82. W. Yan, H. Santti, O.A. Janne, J.J. Palvimo, and J. Toppari Expression of the E3 SUMO-1 ligases PIASx and PIAS1 during spermatogenesis in the rat Gene Expr. Patterns 3 2003 301 308
83. H. Zhang, H. Saitoh, and M.J. Matunis Enzymes of the SUMO modification pathway localize to filaments of the nuclear pore complex Mol. Cell. Biol. 22 2002 6498 6508