Mechanism of extracellular ubiquitination in the mammalian epididymis

Journal of Cellular Physiology

Volumn 215, Issue 3, 2008, Pages 684-696

  Baska, Kathleen M ^a   Manandhar, Gaurishankar ^a   Feng, Dawn ^a   Agca, Yuksel ^a,b   Tengowski, Mark W ^c   Sutovsky, Miriam ^a   Yi, Young Joo ^a,d   Sutovsky, Peter ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c PFIZER INC   (United States)

^d Chungnam National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; PROTEASOME; THIOESTER; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN THIOLESTERASE; ENHANCED GREEN FLUORESCENT PROTEIN; FLUORESCENT DYE; LYSOZYME; PROTEINASE; THIOL DERIVATIVE; UBIQUITIN C;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; COW; ENZYME ACTIVITY; ENZYME SUBSTRATE; EPIDIDYMIS; EPITHELIUM CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SECRETION; TRANSGENIC MOUSE; TRANSGENIC RAT; UBIQUITINATION; WESTERN BLOTTING; ANIMAL; BIOTINYLATION; BODY FLUID; CATTLE; CELL CULTURE; CELL SEPARATION; CULTURE MEDIUM; CYTOLOGY; CYTOPLASM; ENZYMOLOGY; EXTRACELLULAR SPACE; GENETICS; MAMMAL; METABOLISM; PROMOTER REGION; RAT; TRANSGENIC ANIMAL;

BOVINAE; MAMMALIA; MUS MUSCULUS; RATTUS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BIOTINYLATION; BODY FLUIDS; CATTLE; CELL SEPARATION; CELLS, CULTURED; CULTURE MEDIA; CYTOPLASMIC STRUCTURES; ENDOPEPTIDASES; EPIDIDYMIS; EPITHELIAL CELLS; EXTRACELLULAR SPACE; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; MALE; MAMMALS; MURAMIDASE; PROMOTER REGIONS (GENETICS); PROTEASOME ENDOPEPTIDASE COMPLEX; RATS; SULFHYDRYL COMPOUNDS; UBIQUITIN C; UBIQUITIN-PROTEIN LIGASE COMPLEXES; UBIQUITINATION;

EID: 42949112102     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21349     Document Type: Article

References (40)

1. Andonian S, Jarvi K, Zini A, Hermo L. 2002. Ultrastructural features of the vas deferens from patients undergoing vasectomy and vasectomy reversal. J Androl 23:691-701.
2. Aumuller G, Wilhelm B, Seitz J. 1999. Apocrine secretion - Fact or artifact? Ann Anat 181:437-446.
3. Axner E. 2006. Sperm maturation in the domestic cat. Theriogenology 66:14-24.
4. Barratt CL, Cohen J. 1987. Quantitation of sperm disposal and phagocytic cells in the tract of short- and long-term vasectomized mice. J Reprod Fertil 81:377-384.
5. Baska KM, Sutovsky P. 2005. Protein modification by ubiquitination and is consequences for spermatogenesis, sperm maturation, fertilization and pre-implantation embryonic development. In: Tokumoto T, editor. New impact on protein modifications in the regulation of reproductive system. Kerala: Research Signpost. pp 83-114.
6. Bryda EC, Pearson M, Agca Y, Bauer BA. 2006. Method for detection and identification of multiple chromosomal integration sites in transgenic animals created with lentivirus. Biotechniques 41:715-719.
7. Chen ZJ, Niles EG, Pickart CM. 1991. Isolation of a cDNA encoding a mammalian multiubiquitinating enzyme (E225K) and overexpression of the functional enzyme in Escherichia coli. J Biol Chem 266:15698-15704.
8. Chenoweth PJ, Chase CC, Jr., Risco CA, Larsen RE. 2000. Characterization of gossypol-induced sperm abnormalities in bulls. Theriogenology 53:1193-1203.
9. Einspanier R, Schuster H, Schams D. 1993. A comparison of hormone levels in follide-lutein-cysts and in normal bovine ovarian follicles. Theriogenology 40:181-188.
10. Flickinger CJ. 1982. The fate of sperm after vasectomy in the hamster. Anat Rec 202:231-239.
11. Follenzi A, Ailles LE, Bakovic S, Geuna M, Naldini L. 2000. Gene transfer by lentiviral vectors is limited by nuclear translocation and rescued by HIV-1 pol sequences. Nat Genet 25:217-222.
12. Fraile B, Martin R, De Miguel MP, Arenas MI, Bethencourt FR, Peinado F, Paniagua R, Santamaria L. 1996. Light and electron microscopic immunohistochemical localization of protein gene product 9.5 and ubiquitin immunoreactivities in the human epididymis and vas deferens. Biol Reprod 55:291-297.
13. Francavilla S, Moscardelli S, Properzi G, De Matteis MA, Scorza Barcellona P, Natali PG, De Martino C. 1987. Postnatal development of epididymis and ductus deferens in the rat A correlation between the ultra structure of the epithelium and tubule wall, and the fluorescence-microscopic distribution of actin, myosin, fibronectin, and basement membrane. Cell Tissue Res 249:257-265.
14. Frenette G, Sullivan R. 2001. Prostasome-like particles are involved in the transfer of P25b from the bovine epididymal fluid to the sperm surface. Mol Reprod Dev 59:115-121.
15. Frenette G, Lessard C, Sullivan R. 2002. Selected proteins of "prostasome-like particles" from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol Reprod 67:308-313.
16. Glickman MH, Ciechanover A. 2002. The ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction. Physiol Rev 82:373-428.
17. Hermo L, Jacks D. 2002. Nature's ingenuity: Bypassing the classical secretory route via apocrine secretion. Mol Reprod Dev 63:394-410.
18. Jones R. 2004. Sperm survival versus degradation in the Mammalian epididymis: A hypothesis. Biol Reprod 71:1405-1411.
19. Kwon J, Mochida K, Wang YL, Sekiguchi S, Sankai T, Aoki S, Ogura A, Yoshikawa Y, Wada K. 2005. Ubiquitin C-terminal hydrolase L-1 is essential for the early apoptotic wave of germinal cells and for sperm quality control during spermatogenesis. Biol Reprod 73:29-35.
20. Kwon J, Sekiguchi S, Wang YL, Setsuie R, Yoshikawa Y, Wada K. 2006. The region-specific functions of two ubiquitin C-terminal hydrolase isozymes along the epididymis. Exp Anim 55:35-43.
21. Laney JD, Hochstrasser M. 1999. Substrate targeting in the ubiquitin system. Cell 97:427-430.
22. Lippert TH, Seeger H, Schieferstein G, Voelter W. 1993. Immunoreactive ubiquitin in human seminal plasma. J Androl 14:130-131.
23. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D. 2002. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295:868-872.
24. Olson GE, Winfrey VP, NagDas SK, Meiner MH. 2004. Region-specific expression and secretion of the fibrinogen-related protein, fgl2, by epithelial cells of the hamster epididymis and its role in disposal of defective spermatozoa. J Biol Chem 279:51266-51274.
25. Pfeifer A, Ikawa M, Dayn Y, Verma IM. 2002. Transgenesis by lentiviral vectors: Lack of gene silencing in mammalian embryonic stem cells and preimplantation embryos. Proc Natl Acad Sci USA 99:2140-2145.
26. Rao AR, Bane A, Gustafsson BK. 1980. Changes in the morphology of spermatozoa during their passage through the genital tract in dairy bulls with normal and impaired spermat ogenesis. Theriogenology 14:1-12.
27. Sakai N, Sawada MT, Sawada H. 2004. Non-traditional roles of ubiquitin-proteasome system in fertilization and gametogenesis. Int J Biochem Cell Biol 36:776-784.
28. Santamaria L, Martin R, Paniagua R, Fraile B, Nistal M, Terenghi G, Polak JM. 1993. Protein gene product 9.5 and ubiquitin immunoreactivities in rat epididymis epithelium. Histochemistry 100:131-138.
29. Sawada H, Sakai N, Abe Y, Tanaka E, Takahashi Y, Fujino J, Kodama E, Takizawa S, Yokosawa H. 2002. Extracellular ubiquitination and proteasome-mediated degradation of the ascidian sperm receptor. Proc Natl Acad Sci USA 99:1223-1228.
30. Schaefer BC, Schaefer ML, Kappler JW, Marrack P, Kedl RM. 2001. Observation of antigen-dependent CD8+ T-cell/ dendritic cell interactions in vivo. Cell Immunol 214:110-122.
31. Shaman JA, Prisztoka R, Ward WS. 2006. Topoisomerase IIb and an extracellular nuclease interact to digest sperm DNA in an apoptotic-like manner. Biol Reprod 75:741-748.
32. Sinha Hikim AP, Swerdloff RS. 1999. Hormonal and genetic control of germ cell apoptosis in the testis. Rev Reprod 4:38-47.
33. Sixt SU, Beiderlinden M, Jennissen HP, Peters J. 2007. Extracellular proteasome in the human alveolar space: A new housekeeping enzyme? Am J Physiol Lung Cell Mol Physiol 292:L1280-1288.
34. Sullivan R, Saez F, Girouard J, Frenette G. 2005. Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood Cells Mol Dis 35:1-10.
35. Sutovsky P. 2003. Ubiquitin-dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: Killing three birds with one stone. Microsc Res Tech 61:88-102.
36. Sutovsky P, Moreno R, Ramalho-Santos J, Dominko T, Thompson WE, Schatten G. 2001. A putative, ubiquitin-dependent mechanism for the recognition and elimination of defective spermatozoa in the mammalian epididymis. J Cell Sci 114:1665-1675.
37. Takagi M, Yamauchi M, Takada K, Ohkawa K. 2002. Serum ubiquitin-protein conjugates in normal subjects and patients with alcoholic liver diseases: Immunoaffinity isolation and electrophoretic mobility. Alcohol Clin Exp Res 26:1692-1696.
38. Tengowski MW, Sutovsky P, Hedlund LW, Guyot DJ, Burkhardt JE, Thompson WE, Sutovsky M, Johnson GA. 2005. Reproductive cytotoxicity is predicted by magnetic resonance microscopy and confirmed by ubiquitin-proteasome immunohistochemistry in a theophylline-induced model of rat testicular and epididymal toxicity. Microsc Microanal 11:300-312.
39. Tengowski MW, Feng D, Sutovsky M, Sutovsky P. 2007. Differential expression of genes encoding constitutive and inducible 20S proteasomal core subunits in the testis and epididymis of theophylline- or 1,3-dinitrobenzene- exposed rats. Biol Reprod 76:149-163.
40. Zufferey R, Donello JE, Trono D, Hope TJ. 1999. Woodchuck hepatitis virus posttranscriptional regulatory element enhances expression of transgenes delivered by retroviral vectors. J Virol 73:2886-2892.