Developmental expression of p97/VCP (Valosin-containing protein) and Jab1/CSN5 in the rat testis and epididymis

Reproductive Biology and Endocrinology

Volumn 9, Issue , 2011, Pages

  Cayli, Sevil ^a   Ocakli, Seda ^a   Erdemir, Fikret ^a   Tas, Ufuk ^a   Aslan, Huseyin ^a   Yener, Tamer ^a   Karaca, Zafer ^a  

^a GAZIOSMANPASA UNIVERSITY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CSN5 PROTEIN; JAB1 PROTEIN; PROTEIN P97; UNCLASSIFIED DRUG; VALOSIN CONTAINING PROTEIN; ADENOSINE TRIPHOSPHATASE; CDC48 PROTEIN; CELL CYCLE PROTEIN; GPS1 PROTEIN, RAT; PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPIDIDYMIS; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SERTOLI CELL; SPERMATID; SPERMATOCYTE; SPERMATOGONIUM; TESTIS DEVELOPMENT; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; TESTIS; WISTAR RAT;

RATTUS;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CELL CYCLE PROTEINS; EPIDIDYMIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; PROTEINS; RATS; RATS, WISTAR; TESTIS;

EID: 80051791585     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-9-117     Document Type: Article

References (49)

1. de Kretser DM. Clinical male infertility. I. Prevalence of and progress in understanding male infertility. Reprod Fertil Dev 1994, 6:3-8. 10.1071/RD9940003, 8066219.
2. Kierszenbaum AL. Mammalian spermatogenesis in vivo and in vitro: a partnership of spermatogenic and somatic cell lineages. Endocr Rev 1994, 15:116-134.
3. Clermont Y, Perey B. Quantitative study of the cell population of the seminiferous tubules in immature rats. Am J Anat 1957, 100:241-267. 10.1002/aja.1001000205, 13435229.
4. Cooper TG. Interactions between epididymal secretions and spermatozoa. J Reprod Fertil Suppl 1998, 53:119-136.
5. Orgebin-Crist MC. Studies on the function of the epididymis. Biol Reprod 1969, 1(Suppl 1):155-175.
6. Hinton BT, Palladino MA, Rudolph D, Labus JC. The epididymis as protector of maturing spermatozoa. Reprod Fertil Dev 1995, 7:731-745. 10.1071/RD9950731, 8711210.
7. Sutovsky P, Moreno R, Ramalho-Santos J, Dominko T, Thompson WE, Schatten G. A putative, ubiquitin-dependent mechanism for the recognition and elimination of defective spermatozoa in the mammalian epididymis. J Cell Sci 2001, 114:1665-1675.
8. Sutovsky P. Ubiquitin-dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: killing three birds with one stone. Microsc Res Tech 2003, 61:88-102. 10.1002/jemt.10319, 12672125.
9. Glickman MH, Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 2002, 82:373-428.
10. Bedard N, Hingamp P, Pang Z, Karaplis A, Morales C, Trasler J, Cyr D, Gagnon C, Wing SS. Mice lacking the UBC4-testis gene have a delay in postnatal testis development but normal spermatogenesis and fertility. Mol Cell Biol 2005, 25:6346-6354. 10.1128/MCB.25.15.6346-6354.2005, 1190331, 16024774.
11. Liu Z, Oughtred R, Wing SS. Characterization of E3Histone, a novel testis ubiquitin protein ligase which ubiquitinates histones. Mol Cell Biol 2005, 25:2819-2831. 10.1128/MCB.25.7.2819-2831.2005, 1061639, 15767685.
12. Wing SS. Deubiquitinating enzymes--the importance of driving in reverse along the ubiquitin-proteasome pathway. Int J Biochem Cell Biol 2003, 35:590-605. 10.1016/S1357-2725(02)00392-8, 12672452.
13. Roest HP, van Klaveren J, de Wit J, van Gurp CG, Koken MH, Vermey M, van Roijen JH, Hoogerbrugge JW, Vreeburg JT, Baarends WM, et al. Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes male sterility associated with chromatin modification. Cell 1996, 86:799-810. 10.1016/S0092-8674(00)80154-3, 8797826.
14. Kwon J, Mochida K, Wang YL, Sekiguchi S, Sankai T, Aoki S, Ogura A, Yoshikawa Y, Wada K. 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 2005, 73:29-35. 10.1095/biolreprod.104.037077, 15744022.
15. Baarends WM, Roest HP, Grootegoed JA. The ubiquitin system in gametogenesis. Mol Cell Endocrinol 1999, 151:5-16. 10.1016/S0303-7207(99)00060-X, 10411315.
16. Baska KM, Manandhar G, Feng D, Agca Y, Tengowski MW, Sutovsky M, Yi YJ, Sutovsky P. Mechanism of extracellular ubiquitination in the mammalian epididymis. J Cell Physiol 2008, 215:684-696. 10.1002/jcp.21349, 18064599.
17. Hochstrasser M. Ubiquitin, proteasomes, and the regulation of intracellular protein degradation. Curr Opin Cell Biol 1995, 7:215-223. 10.1016/0955-0674(95)80031-X, 7612274.
18. Kondo H, Rabouille C, Newman R, Levine TP, Pappin D, Freemont P, Warren G. p47 is a cofactor for p97-mediated membrane fusion. Nature 1997, 388:75-78. 10.1038/40411, 9214505.
19. Hirabayashi M, Inoue K, Tanaka K, Nakadate K, Ohsawa Y, Kamei Y, Popiel AH, Sinohara A, Iwamatsu A, Kimura Y, et al. VCP/p97 in abnormal protein aggregates, cytoplasmic vacuoles, and cell death, phenotypes relevant to neurodegeneration. Cell Death Differ 2001, 8:977-984. 10.1038/sj.cdd.4400907, 11598795.
20. Rabinovich E, Kerem A, Frohlich KU, Diamant N, Bar-Nun S. AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol Cell Biol 2002, 22:626-634. 10.1128/MCB.22.2.626-634.2002, 139744, 11756557.
21. Meyer HH, Shorter JG, Seemann J, Pappin D, Warren G. A complex of mammalian ufd1 and npl4 links the AAA-ATPase, p97, to ubiquitin and nuclear transport pathways. Embo J 2000, 19:2181-2192. 10.1093/emboj/19.10.2181, 384367, 10811609.
22. Hetzer M, Meyer HH, Walther TC, Bilbao-Cortes D, Warren G, Mattaj IW. Distinct AAA-ATPase p97 complexes function in discrete steps of nuclear assembly. Nat Cell Biol 2001, 3:1086-1091. 10.1038/ncb1201-1086, 11781570.
23. Ficarro S, Chertihin O, Westbrook VA, White F, Jayes F, Kalab P, Marto JA, Shabanowitz J, Herr JC, Hunt DF, Visconti PE. Phosphoproteome analysis of capacitated human sperm. Evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation. J Biol Chem 2003, 278:11579-11589. 10.1074/jbc.M202325200, 12509440.
24. Krick R, Bremer S, Welter E, Schlotterhose P, Muehe Y, Eskelinen EL, Thumm M. Cdc48/p97 and Shp1/p47 regulate autophagosome biogenesis in concert with ubiquitin-like Atg8. J Cell Biol 2010, 190:965-973. 10.1083/jcb.201002075, 3101598, 20855502.
25. Tresse E, Salomons FA, Vesa J, Bott LC, Kimonis V, Yao TP, Dantuma NP, Taylor JP. VCP/p97 is essential for maturation of ubiquitin-containing autophagosomes and this function is impaired by mutations that cause IBMPFD. Autophagy 2010, 6:217-227. 10.4161/auto.6.2.11014, 2929010, 20104022.
26. Dai RM, Li CC. Valosin-containing protein is a multi-ubiquitin chain-targeting factor required in ubiquitin-proteasome degradation. Nat Cell Biol 2001, 3:740-744. 10.1038/35087056, 11483959.
27. Meusser B, Hirsch C, Jarosch E, Sommer T. ERAD: the long road to destruction. Nat Cell Biol 2005, 7:766-772. 10.1038/ncb0805-766, 16056268.
28. Klein JB, Barati MT, Wu R, Gozal D, Sachleben LR, Kausar H, Trent JO, Gozal E, Rane MJ. Akt-mediated valosin-containing protein 97 phosphorylation regulates its association with ubiquitinated proteins. J Biol Chem 2005, 280:31870-31881. 10.1074/jbc.M501802200, 16027165.
29. Cayli S, Klug J, Chapiro J, Froehlich S, Krasteva G, Orel L, Meinhardt A. The COP9 signalosome interacts ATP-dependently with p97/VCP and controls the ubiquitination status of proteins bound to p97/VCP. J Biol Chem 2009, 284:34944-34953. 10.1074/jbc.M109.037952, 2787357, 19826004.
30. Berse M, Bounpheng M, Huang X, Christy B, Pollmann C, Dubiel W. Ubiquitin-dependent degradation of Id1 and Id3 is mediated by the COP9 signalosome. J Mol Biol 2004, 343:361-370. 10.1016/j.jmb.2004.08.043, 15451666.
31. Yun J, Tomida A, Andoh T, Tsuruo T. Interaction between glucose-regulated destruction domain of DNA topoisomerase IIalpha and MPN domain of Jab1/CSN5. J Biol Chem 2004, 279:31296-31303. 10.1074/jbc.M401411200, 15126503.
32. Callige M, Kieffer I, Richard-Foy H. CSN5/Jab1 is involved in ligand-dependent degradation of estrogen receptor {alpha} by the proteasome. Mol Cell Biol 2005, 25:4349-4358. 10.1128/MCB.25.11.4349-4358.2005, 1140630, 15899841.
33. Li S, Liu X, Ascoli M. p38JAB1 binds to the intracellular precursor of the lutropin/choriogonadotropin receptor and promotes its degradation. J Biol Chem 2000, 275:13386-13393. 10.1074/jbc.275.18.13386, 10788448.
34. Kim BC, Lee HJ, Park SH, Lee SR, Karpova TS, McNally JG, Felici A, Lee DK, Kim SJ. Jab1/CSN5, a component of the COP9 signalosome, regulates transforming growth factor beta signaling by binding to Smad7 and promoting its degradation. Mol Cell Biol 2004, 24:2251-2262. 10.1128/MCB.24.6.2251-2262.2004, 355855, 14993265.
35. Wan M, Cao X, Wu Y, Bai S, Wu L, Shi X, Wang N. Jab1 antagonizes TGF-beta signaling by inducing Smad4 degradation. EMBO Rep 2002, 3:171-176. 10.1093/embo-reports/kvf024, 1083965, 11818334.
36. Cope GA, Suh GS, Aravind L, Schwarz SE, Zipursky SL, Koonin EV, Deshaies RJ. Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cul1. Science 2002, 298:608-611. 10.1126/science.1075901, 12183637.
37. Shackleford TJ, Claret FX. JAB1/CSN5: a new player in cell cycle control and cancer. Cell Div 2010, 5:26. 10.1186/1747-1028-5-26, 2976740, 20955608.
38. Leblond CP, Clermont Y. Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann N Y Acad Sci 1952, 55:548-573. 10.1111/j.1749-6632.1952.tb26576.x, 13139144.
39. Malkov M, Fisher Y, Don J. Developmental schedule of the postnatal rat testis determined by flow cytometry. Biol Reprod 1998, 59:84-92. 10.1095/biolreprod59.1.84, 9674997.
40. Parvinen M. Regulation of the seminiferous epithelium. Endocr Rev 1982, 3:404-417. 10.1210/edrv-3-4-404, 6295753.
41. Griswold MD. Interactions between germ cells and Sertoli cells in the testis. Biol Reprod 1995, 52:211-216. 10.1095/biolreprod52.2.211, 7711190.
42. Cheng CY, Mruk DD. The biology of spermatogenesis: the past, present and future. Philos Trans R Soc Lond B Biol Sci 2010, 365:1459-1463. 10.1098/rstb.2010.0024, 2871927, 20403863.
43. Hutchison GR, Scott HM, Walker M, McKinnell C, Ferrara D, Mahood IK, Sharpe RM. Sertoli cell development and function in an animal model of testicular dysgenesis syndrome. Biol Reprod 2008, 78:352-360. 10.1095/biolreprod.107.064006, 17928633.
44. Sharpe RM, McKinnell C, Kivlin C, Fisher JS. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 2003, 125:769-784. 10.1530/rep.0.1250769, 12773099.
45. Kayisli UA, Cayli S, Seval Y, Tertemiz F, Huppertz B, Demir R. Spatial and temporal distribution of Tie-1 and Tie-2 during very early development of the human placenta. Placenta 2006, 27:648-659. 10.1016/j.placenta.2005.05.013, 16026828.
46. Bounpheng MA, Melnikova IN, Dodds SG, Chen H, Copeland NG, Gilbert DJ, Jenkins NA, Christy BA. Characterization of the mouse JAB1 cDNA and protein. Gene 2000, 242:41-50. 10.1016/S0378-1119(99)00525-9, 10721695.
47. Sakai Y, Nakamoto T, Yamashina S. Dynamic changes in Sertoli cell processes invading spermatid cytoplasm during mouse spermiogenesis. Anat Rec 1988, 220:51-57. 10.1002/ar.1092200107, 2964797.
48. Russell LD, Tallon-Doran M, Weber JE, Wong V, Peterson RN. Three-dimensional reconstruction of a rat stage V Sertoli cell: III. A study of specific cellular relationships. Am J Anat 1983, 167:181-192. 10.1002/aja.1001670204, 6613903.
49. Tengowski MW, Feng D, Sutovsky M, Sutovsky P. 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 2007, 76:149-163. 10.1095/biolreprod.106.053173, 16988215.