Immunocytochemical and ultrastructural analyses of the function of the ubiquitin-proteasome system during spermiogenesis with the use of the inhibitors of proteasome proteolytic activity in the alga, Chara vulgaris

Biology of Reproduction

Volumn 78, Issue 4, 2008, Pages 577-585

  Wojtczak, Agnieszka ^a   Kwiatkowska, Maria ^a  

^a UNIVERSITY OF LODZ   (Poland)

Author keywords

Aggresomes; Chara vulgaris; Epoxomicin; Gamete biology; MG 132; Proteasomes; Sperm maturation; Spermiogenesis; Ubiquitin

Indexed keywords

12 HYDROXY 13 HYDROXYMETHYL 3,5,7 TRIMETHYLTETRADECA 2,4 DIENEDIOIC ACID 12,14 LACTONE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; EPOXOMICIN; HISTONE; LACTACYSTIN; PROTEASOME; PROTEASOME INHIBITOR; UBIQUITIN;

ALGA; ARTICLE; CELL NUCLEUS; CELL VOLUME; CHROMATIN CONDENSATION; CONTROLLED STUDY; CYTOPLASM; DEVELOPMENTAL STAGE; FLAGELLUM; IMMUNOCYTOCHEMISTRY; MEIOSIS; METABOLISM; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; SPERMATID; SPERMATOGENESIS; UBIQUITINATION; ULTRASTRUCTURE;

CELL NUCLEUS; CHARA; CYTOPLASM; HISTONES; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON; PROTEASOME ENDOPEPTIDASE COMPLEX; SPERMATOGENESIS; UBIQUITIN;

ALGAE; ANIMALIA; CHARA VULGARIS;

EID: 41549155216     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.107.062901     Document Type: Article

References (66)

1. Pogany GC, Corzett M, Feston S, Balhorn R. DNA and protein content of mouse sperm. Implications regarding sperm chromatin structure. Exp Cell Res 1981; 136:127-136.
2. Ward WS, Coffey DS. DNA packing and organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod 1991; 44:569-574.
3. Caron C, Govin J, Rousseaux S, Khochbin S. How to pack the genome for a safe trip. In: Jeanteur P (ed.), Progress in Molecular and Subcellular Biology. Epigenetics and Chromatin. Springer-Verlag Berlin Heidelberg; 2005:65-89.
4. Vierstra RD. Proteolysis in plants: mechanisms and functions. Plant Mol Biol 1996; 32:275-302.
5. Munro P, Flatau G, Lemichez E. Bacteria and the ubiquitin pathway. Curr Opin Microbiol 2007; 10:39-46.
6. Tanaka K. Proteasomes: structure and biology. J Biochem 1998; 123:195-204.
7. Baumeister W, Walz J, Zühl F, Seemüller E. The proteasome: paradigm of self-compartmentalizing protease. Cell 1998; 92:367-380.
8. Rechsteiner M, Hill CP. Mobilizing the proteolytic machine: cell biological roles of proteasome activators and inhibitors. Trends Cell Biol 2005; 15:27-33.
9. Nickell S, Mihalache O, Beck F, Hegerl R, Korinek A, Baumeister W. Structural analysis of the 26S proteasome by cryolectron tomography. Biochem Biophys Res Commun 2007; 353:115-120.
10. Agell N, Chiva M, Mezquita C. Changes in nuclear content of protein conjugate histone H2A-ubiquitin during rooster spermatogenesis. FEBS Lett 1983; 155:209-212.
11. Agell N, Mezquita C. Cellular content of ubiquitin and formation of ubiquitin conjugates during chicken spermatogenesis. Biochem J 1988; 250:883-889.
12. Baarends WM, Hoogerbrugge JW, Roest HP, Ooms M, Vreeburg J, Hoeijmakers JHJ, Grootegoed JA. Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev Biol 1999a; 207:322-333.
13. Baarends WM, Roest HP, Grootegoed JA. The ubiquitin system in gametogenesis. Mol Cell Endocrinol 1999b; 151:5-16.
14. Chen HY, Sun J-M, Zhang Y, Davie JR, Meistrich ML. Ubiquitination of histone H3 in elongating spermatids of rat testes. J Biol Chem 1998; 273:13165-13169.
15. Koken MHM, Hoogerbrugge JW, Jaspers-Dekker I, de Wit J, Willemsen R, Roest HP, Grootegoed JA, Hoeijmakers JHJ. Expression of the ubiquitin- conjugating DNA repair enzymes HHR6A and B suggests a role in spermatogenesis and chromatin modification. Dev Biol 1996; 173:119-132.
16. Roest HP, van Klaveren J, de Wit J, van Gurp CG, Koken MHM, Vermey M, van Roijen JH, Hoogerbrugge JW, Vreeburg JTM, Baarends WM, Bootsma D, Grootegoed JA, Hoeijmakers JHJ. Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes male sterility associated with chromatin modification. Cell 1996; 86:799-810.
17. Roest HP, Baarends WM, de Wit J, van Klaveren J, Wassenaar E, Hoogerbrugge JW, van Cappellen WA, Hoeijmakers JHJ, Grootegoed JA. The ubiquitin-conjugating DNA repair enzyme HR6A is a maternal factor essential for early embryonic development in mice. Mol Cell Biol 2004; 24:5485-5495.
18. 17kB) highly expressed in rat testis. Biochem J 1995; 305:125-132.
19. Mezquita J, Pau M, Mezquita C. Characterization and expression of two chicken cDNA encoding ubiquitin fused to ribosomal proteins of 52 and 80 amino acids. Gene 1997; 195:313-319.
20. Yang F, Skaletsky H, Wang PJ. Ubl4b, an X-derived retrogene, is specifically expressed in post-meiotic germ cells in mammals. Gene Expr Patterns 2007; 7:131-136.
21. Kim Y-K, Kim Y-S, Yoo K-J, Lee H-J, Lee D-R, Yeo CY, Baek K-H. The expression of Usp42 during embryogenesis and spermatogenesis in mouse. Gene Expr Patterns 2007; 7:143-148.
22. Wang S, Zheng H, Esaki Y, Kelly F, Yan W. Cullin3 is a KLHL10-interacting protein preferentially expressed during late spermiogenesis. Biol Reprod 2006; 74:102-108.
23. Inaba K, Akazone Y, Morisawa M. Purification of proteasomes from salmonid fish sperm and their localization along sperm flagella. J Cell Sci 1993; 104:907-915.
24. Biały ŁP, Ziemba HT, Marianowski P, Fra̧cki S, Bury M, Wójcik C. Localization of a proteasomal antigen in human spermatozoa: immunohistochemical electron microscopic study. Folia Histochem Cytobiol 2001; 39:129-130.
25. Haraguchi CM, Mabuchi T, Hirata S, Shoda T, Tokumoto T, Hoshi K, Yokota S. 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.
26. Sassone-Corsi P. Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science 2002; 296:2176-2178.
27. Kinyamu HK, Chen J, Archer TK. Linking the ubiquitin-proteasome pathway to chromatin remodeling/modification by nuclear receptors. J Mol Endocrinol 2005; 34:281-297.
28. Reynolds WF, Wolfe SL. Changes in basic proteins during sperm maturation in a plant, Marchantia polymorpha. Exp Cell Res 1978; 116:269-273.
29. Reynolds WF, Wolfe SL. Protamines in plant sperm. Exp Cell Res 1984; 152:443-448.
30. Robert D. Le noyau du gaméte mâle chez les végétaux [in French]. Ann Sci Nat Bot Paris 1984; 6:151-164.
31. 3H-arginine incorporation. Folia Histochem Cytobiol 2002; 40:85-97.
32. Popłońska K, Wojtczak A, Kwiatkowska M, Kaźmierczak A. Cytochemical and immunocytochemical studies of the localization of histones and protamine-type proteins in spermatids of Chara vulgaris and Chara tomentosa. Folia Histochem Cytobiol 2007; 45:1-8.
33. Kwiatkowska M, Kaźmierczak A, Popłońska K. Ultrastructural, autoradiographic and electrophoretic examinations of Chara tomentosa spermiogenesis. Acta Soc Bot Pol 2002; 71:201-209.
34. Kwiatkowska M, Wojtczak A, Popłońska K, Gosek A. Occurence of ubiquitin during spermiogenesis in Chara vulgaris. Folia Histochem Cytobiol 2001; 39:135-136.
35. Kwiatkowska M, Wojtczak A, Popłońska K, Teodorczyk M. The influence of epoxomicin, inhibitor of proteasomal proteolytic activity, on spermiogenesis in Chara vulgaris. Folia Histochem Cytobiol 2003; 41:51-54.
36. Popłońska K, Kwiatkowska M, Stȩpiński D, Gosek A, Wojtczak A. Immunocytochemical localization of ubiquitin and proteasomes in spermatids during spermiogenesis of Chara vulgaris (Charophyceae). Eur J Phycol 2004; 39:309-315.
37. Kaźmierczak A. Electrophoretic analysis of qualitative and quantitative changes of basic proteins during spermiogenesis of Chara. Acta Biol Cracov Ser Botanica 2000; 42(suppl 1):45.
38. Popłońska K. Cytochemical studies on histone-type and protamine-type proteins during spermiogenesis in Chara vulgaris and Chara tomentosa. Folia Histochem Cytobiol 2002; 40:233-234.
39. Heinemeyer W, Fischer M, Krimmer T, Stachon U, Wolf DH. The active sites of the eukaryotic 20 S proteasome and their involvement in subunit procursor processing. J Biol Chem 1997; 272:25200-25209.
40. Meng L, Mohan R, Kwok BHB, Elofsson M, Sin N, Crews CM. Epoxomicin, a potent and selective proteasome inhibitor, exhibits in vivo antiinflammatory activity. Proc Natl Acad Sci 1999; 96:10403-10408.
41. Kisselev AF, Goldberg AL. Proteasome inhibitors: from research tools to drug candidates. Chem Biol 2001; 8:739-758.
42. Verkest A, de O, Manes C-L, Vercruysse S, Maes S, Van Der Schueren E, Beeckman T, Genschik P, Kuiper M, Inze D, De Veylder L. The cyclin-dependent kinase KRP2 controls theonset of the endoreduplication cycle during Arabidopsis leaf development through inhibition of mitotic CDKA;1 kinase complexes. Plant Cell 2005; 17:1723-1736.
43. Planchais S, Glab N, Inzé D, Bergounioux C. Chemical inhibitors: a tool for plant cell cycle studies. FEBS Lett 2000; 476:78-83.
44. Reynolds ES. The use of lead citrate of high pH as an electronopaque stain in electron microscopy. J Cell Biol 1963; 17:208-212.
45. Alfert M, Geschwind I. A selecive staining method for the basic proteins of cell nuclei. Proc Natl Acad Sci 1953; 39:991-998.
46. Myśliwski A. Histochemia histonów [in Polish]. In: Krygier-Stojałowska A, Godlewski H (eds.), Topochemiczne Metody Badań Komórek i Tkanek. PWN, Warszawa; 1982:361-376.
47. Kwiatkowska M. Plasmodesmal changes are related to different developmental stages of antheridia of Chara species. Protoplasma 2003; 222:1-11.
48. Olszewska MJ, Godlewski M. An autoradiographic study of the synthesis of nucleic acids and protein during the cell cycle of synchronously dividing antheridial filaments in Chara vulgaris L. Folia Histochem Cytochem 1972; 10:245-256.
49. Kwiatkowska M, Maszewski J. Cell sizes and DNA level in antheridial filaments in relation to the initiation of spermatozoid differentiation in Chara vulgaris L. Folia Histochem Cytobiol 1987; 24:79-90.
50. Godlewski M, Kwiatkowska M. Effect of gibberellic acid on the formation and development of antheridia and oogonia in Chara vulgaris L. Acta Soc Bot Pol 1980; 49:459-469.
51. Olszewska MJ, Godlewski M. A cytochemical study of spermatogenesis in Chara vulgaris L. Folia Histochem Cytochem 1973; 11:9-20.
52. Olszewska MJ, Gernand D, Godlewski M, Kunachowicz A. DNA methylation during antheridial filament development and spermiogenesis in Chara vulgaris (Charophyceae) analysed by in situ nick-translation driven by methylation-sensitive restriction enzymes. Eur J Phycol 1997; 32:287-291.
53. del Mazo J, Prantera G, Torres M, Ferraro M. DNA metylation changes during mouse spermatogenesis. Chromosome Res 1994; 2:147-152.
54. Tanaka H, Baba T. Gene expression in spermiogenesis. Cell Mol Life Sci 2005; 62:344-354.
55. DeJong J. Basic mechanisms for the control of germ cell gene expression. Gene 2006; 366:39-50.
56. Chan W-Y, Lee T-L, Wu S-M, Ruszczyk L, Alba D, Baxendale V, Rennert OM. Transcriptome analyses of male germ cells with serial analysis of gene expression (SAGE). Mol Cell Endocrinol 2006; 250:8-19.
57. Kwiatkowska M. Changes in ultrastructure of cytoplasm and nucleus during spermiogenesis in Chara vulgaris. Folia Histochem Cytobiol 1996; 34:41-56.
58. Ward WS. The structure of the sleeping genome: implications of sperm DNA organization for somatic cells. J Cell Biochem 1994; 55:77-82.
59. Wójcik C, Schroeter D, Wilk S, Lamprecht J, Paweletz N. Ubiquitin-mediated proteolysis centers in HeLa cells: indication from studies of an inhibitor of the chymotrypsin-like activity of the proteasome. Eur J Cell Biol 1996; 71:311-318.
60. Johnston JA, Ward CL, Kopito RR. Aggresomes: a cellular response to misfolded proteins. J Cell Biol 1998; 143:1883-1898.
61. García-Mata R, Bebök Z, Sorscher EJ, Sztul ES. Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J Cell Biol 1999; 146:1239-1254.
62. Kopito RR. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 2000; 10:524-530.
63. Wójcik C, DeMartino GN. Intracellular localization of proteasomes. Int J Biochem Cell Biol 2003; 35:579-589.
64. Bardag-Gorce F, Riley NE, Nan L, Montgomery RO, Li J, French BA, Lue YH, French SW. The proteasome inhibitor, PS-341, causes cytokeratin aggresome formation. Exp Mol Pathol 2004; 76:9-16.
65. Meiners S, Heyken D, Weller A, Ludwig A, Stangl K, Kloetzel P-M, Krüger E. Inhibition of proteasome activity induces concerted expression of proteasome genes and de novo formation of mammalian proteasomes. J Biol Chem 2003; 278:21517-21525.
66. Lundgren J, Masson P, Mirzaei Z, Young P. Identification and characterization of a Drosophila proteasome regulatory network. Mol Cell Biol 2005; 25:4662-4675.