A novel testis-specific GTPase serves as a link to proteasome biogenesis: Functional characterization of RhoS/RSA-14-44 in spermatogenesis

Molecular Biology of the Cell

Volumn 21, Issue 24, 2010, Pages 4312-4324

  Zhang, Ning ^a,b   Liang, Junbo ^a   Tian, Yongqiang ^a   Yuan, Ligang ^a   Wu, Lan ^a   Miao, Shiying ^a   Zong, Shudong ^b   Wang, Linfang ^a  

^a TSINGHUA UNIVERSITY   (China)

^b NATIONAL RESEARCH INSTITUTE FOR FAMILY PLANNING   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE PSMB5; PROTEASOME; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN RSA 14 44; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BIOGENESIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME STABILITY; ENZYME SUBUNIT; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN STRUCTURE; SPERMATOGENESIS; TESTIS;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MALE; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STABILITY; RATS; RATS, SPRAGUE-DAWLEY; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOZOA; TESTIS;

MAMMALIA;

EID: 78650503825     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-04-0310     Document Type: Article

References (83)

1. Adams, J. (2003). The proteasome: Structure, function, and role in the cell. Cancer Treat. Rev. 29(Suppl 1), 3-9.
2. Adly, M. A., and Hussein, M. R. (2010). Immunohistological profile of the Ras homologous B protein (RhoB) in human testes showing normal spermatogenesis, spermatogenic arrest and Sertoli cell only syndrome. Pathol. Oncol. Res. 16, 427-433.
3. Aki, M., Shimbara, N., Takashina, M., Akiyama, K., Kagawa, S., Tamura, T., Tanahashi, N., Yoshimura, T., Tanaka, K., and Ichihara, A. (1994). Interferongamma induces different subunit organizations and functional diversity of proteasomes. J. Biochem. 115, 257-269.
4. Badr, G., Saad, H., Waly, H., Hassan, K., Abdel-Tawab, H., Alhazza, I. M., and Ahmed, E. A. (2010). Type I interferon (IFN-alpha/beta) rescues B-lymphocytes from apoptosis via PI3Kdelta/Akt, Rho-A, NFkappaB and Bcl-2/ Bcl(XL). Cell Immunol. 263, 31-40.
5. Belote, J. M., and Zhong, L. (2009). Duplicated proteasome subunit genes in Drosophila and their roles in spermatogenesis. Heredity 103, 23-31.
6. Benetka, W., Koranda, M., Maurer-Stroh, S., Pittner, F., and Eisenhaber, F. (2006). Farnesylation or geranylgeranylation? Efficient assays for testing protein prenylation in vitro and in vivo. BMC Biochem. 7, 6.
7. Berruti, G., and Martegani, E. (2005). The deubiquitinating enzyme mUBPy interacts with the sperm-specific molecular chaperone MSJ-1, the relation with the proteasome, acrosome, and centrosome in mouse male germ cells. Biol. Reprod. 72, 14-21.
8. Bishop, A. L., and Hall, A. (2000). Rho GTPases and their effector proteins. Biochem. J. 348(Pt 2), 241-255.
9. Boureux, A., Vignal, E., Faure, S., and Fort, P. (2007). Evolution of the Rho family of ras-like GTPases in eukaryotes. Mol. Biol. Evol. 24, 203-216.
10. Bourne, H. R., Sanders, D. A., and McCormick, F. (1991). The GTPase superfamily: Conserved structure and molecular mechanism. Nature 349, 117-127.
11. Bryan, B. A., and D'Amore, P. A. (2007). What tangled webs they weave: Rho-GTPase control of angiogenesis. Cell Mol. Life Sci. 64, 2053-2065.
12. Bustelo, X. R., Sauzeau, V., and Berenjeno, I. M. (2007). GTP-binding proteins of the Rho/Rac family: Regulation, effectors and functions in vivo. Bioessays 29, 356-370.
13. Chen, P., and Hochstrasser, M. (1996). Autocatalytic subunit processing couples active site formation in the 20S proteasome to completion of assembly. Cell 86, 961-972.
14. Chen, X., Hu, T., Liang, G., Yang, M., Zong, S., Miao, S., Koide, S. S., and Wang, L. (2008). A novel testis protein, RSB-66, interacting with INCA1 (inhibitor of Cdk interacting with cyclin A1). Biochem. Cell Biol. 86, 345-351.
15. Cheng, Y. (2009). Toward an atomic model of the 26S proteasome. Curr. Opin. Struct. Biol. 19, 203-208.
16. Dahlmann, B., Ruppert, T., Kuehn, L., Merforth, S., and Kloetzel, P. M. (2000). Different proteasome subtypes in a single tissue exhibit different enzymatic properties. J. Mol. Biol. 303, 643-653.
17. de Kretser, D. M., Loveland, K. L., Meinhardt, A., Simorangkir, D., and Wreford, N. (1998). Spermatogenesis. Hum. Reprod. 13(Suppl 1), 1-8.
18. Dong, J., Chen, W., Welford, A., and Wandinger-Ness, A. (2004). The proteasome alpha-subunit XAPC7 interacts specifically with Rab7 and late endosomes. J. Biol. Chem. 279, 21334-21342.
19. Ducummon, C. C., and Berger, T. (2006). Localization of the Rho GTPases and some Rho effector proteins in the sperm of several mammalian species. Zygote 14, 249-257.
20. Eddy, E. M. (2002). Male germ cell gene expression. Recent Prog. Horm. Res. 57, 103-128.
21. Erschbamer, M. K., Hofstetter, C. P., and Olson, L. (2005). RhoA, RhoB, RhoC, Rac1, Cdc42, and Tc10 mRNA levels in spinal cord, sensory ganglia, and corticospinal tract neurons and long-lasting specific changes following spinal cord injury. J. Comp. Neurol. 484, 224-233.
22. Etienne-Manneville, S., and Hall, A. (2002). Rho GTPases in cell biology. Nature 420, 629-635.
23. Freeman, E. A., Jani, P., and Millette, C. E. (2002). Expression and potential function of Rho family small G proteins in cells of the mammalian seminiferous epithelium. Cell Commun. Adhes. 9, 189-204.
24. Fricke, B., Heink, S., Steffen, J., Kloetzel, P. M., and Kruger, E. (2007). The proteasome maturation protein POMP facilitates major steps of 20S proteasome formation at the endoplasmic reticulum. EMBO Rep. 8, 1170-1175.
25. Groll, M., Nazif, T., Huber, R., and Bogyo, M. (2002). Probing structural determinants distal to the site of hydrolysis that control substrate specificity of the 20S proteasome. Chem. Biol. 9, 655-662.
26. Heink, S., Ludwig, D., Kloetzel, P. M., and Kruger, E. (2005). IFN-gammainduced immune adaptation of the proteasome system is an accelerated and transient response. Proc. Natl. Acad. Sci. USA 102, 9241-9246.
27. Hendil, K. B., and Hartmann-Petersen, R. (2004). Proteasomes: A complex story. Curr. Protein Pept. Sci. 5, 135-151.
28. Hirano, Y., Hayashi, H., Iemura, S., Hendil, K. B., Niwa, S., Kishimoto, T., Kasahara, M., Natsume, T., Tanaka, K., and Murata, S. (2006). Cooperation of multiple chaperones required for the assembly of mammalian 20S proteasomes. Mol. Cell 24, 977-984. (Pubitemid 44960093)
29. Hirano, Y., Hendil, K. B., Yashiroda, H., Iemura, S., Nagane, R., Hioki, Y., Natsume, T., Tanaka, K., and Murata, S. (2005). A heterodimeric complex that promotes the assembly of mammalian 20S proteasomes. Nature 437, 1381-1385.
30. Hori, Y., Kikuchi, A., Isomura, M., Katayama, M., Miura, Y., Fujioka, H., Kaibuchi, K., and Takai, Y. (1991). Post-translational modifications of the C-terminal region of the rho protein are important for its interaction with membranes and the stimulatory and inhibitory GDP/GTP exchange proteins. Oncogene 6, 515-522.
31. Ihara, K., Muraguchi, S., Kato, M., Shimizu, T., Shirakawa, M., Kuroda, S., Kaibuchi, K., and Hakoshima, T. (1998). Crystal structure of human RhoA in a dominantly active form complexed with a GTP analogue. J. Biol. Chem. 273, 9656-9666.
32. Khor, B., et al. (2006). Proteasome activator PA200 is required for normal spermatogenesis. Mol. Cell. Biol. 26, 2999-3007.
33. Kierszenbaum, A. L. (1994). Mammalian spermatogenesis in vivo and in vitro: A partnership of spermatogenic and somatic cell lineages. Endocr. Rev. 15, 116-134.
34. Kleijnen, M. F., Shih, A. H., Zhou, P., Kumar, S., Soccio, R. E., Kedersha, N. L., Gill, G., and Howley, P. M. (2000). The hPLIC proteins may provide a link between the ubiquitination machinery and the proteasome. Mol. Cell 6, 409-419.
35. Knaus, U. G., Bamberg, A., and Bokoch, G. M. (2007). Rac and Rap GTPase activation assays. Methods Mol. Biol. 412, 59-67.
36. Liang, G., Zhang, X. D., Wang, L. J., Sha, Y. S., Zhang, J. C., Miao, S. Y., Zong, S. D., Wang, L. F., and Koide, S. S. (2004). Identification of differentially expressed genes of primary spermatocyte against round spermatid isolated from human testis using the laser capture microdissection technique. Cell Res. 14, 507-512.
37. Liu, A. X., Rane, N., Liu, J. P., and Prendergast, G. C. (2001). RhoB is dispensable for mouse development, but it modifies susceptibility to tumor formation as well as cell adhesion and growth factor signaling in transformed cells. Mol. Cell. Biol. 21, 6906-6912.
38. Liu, X., Huang, W., Li, C., Li, P., Yuan, J., Li, X., Qiu, X. B., Ma, Q., and Cao, C. (2006). Interaction between c-Abl and Arg tyrosine kinases and proteasome subunit PSMA7 regulates proteasome degradation. Mol. Cell 22, 317-327.
39. Lui, W. Y., and Cheng, C. Y. (2008). Transcription regulation in spermatogenesis. Adv. Exp. Med. Biol. 636, 115-132.
40. Lui, W. Y., Mruk, D. D., and Cheng, C. Y. (2005). Interactions among IQGAP1, Cdc42, and the cadherin/catenin protein complex regulate Sertoli-germ cell adherens junction dynamics in the testis. J. Cell. Physiol. 202, 49-66.
41. Mackay, D. J., and Hall, A. (1998). Rho GTPases. J. Biol. Chem. 273, 20685-20688.
42. Matias, A. C., Ramos, P. C., and Dohmen, R. J. (2010). Chaperone-assisted assembly of the proteasome core particle. Biochem. Soc. Trans. 38, 29-33.
43. Merforth, S., Kuehn, L., Osmers, A., and Dahlmann, B. (2003). Alteration of 20S proteasome-subtypes and proteasome activator PA28 in skeletal muscle of rat after induction of diabetes mellitus. Int. J. Biochem. Cell Biol. 35, 740-748.
44. Michaelson, D., Silletti, J., Murphy, G., D'Eustachio, P., Rush, M., and Philips, M. R. (2001). Differential localization of Rho GTPases in live cells: Regulation by hypervariable regions and RhoGDI binding. J. Cell Biol. 152, 111-126.
45. Mitchell, D. C., Bryan, B. A., Liu, J. P., Liu, W. B., Zhang, L., Qu, J., Zhou, X., Liu, M., and Li, D. W. (2007). Developmental expression of three small GTPases in the mouse eye. Mol. Vis. 13, 1144-1153.
46. Murata, S., Sasaki, K., Kishimoto, T., Niwa, S., Hayashi, H., Takahama, Y., and Tanaka, K. (2007). Regulation of CD8+ T cell development by thymus-specific proteasomes. Science 316, 1349-1353.
47. Naud, N., Toure, A., Liu, J., Pineau, C., Morin, L., Dorseuil, O., Escalier, D., Chardin, P., and Gacon, G. (2003). Rho family GTPase Rnd2 interacts and co-localizes with MgcRacGAP in male germ cells. Biochem. J. 372, 105-112.
48. Okazaki, Y., et al. (2002). Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 420, 563-573.
49. Ostrowska, H., Kruszewski, K., and Kasacka, I. (2006). Immuno-proteasome subunit LMP7 is up-regulated in the ischemic kidney in an experimental model of renovascular hypertension. Int. J. Biochem. Cell Biol. 38, 1778-1785.
50. Qiao, Y., Yang, J. X., Zhang, X. D., Liu, Y., Zhang, J. C., Zong, S. D., Miao, S. Y., Wang, L. F., and Koide, S. S. (2004). Characterization of rtSH3p13 gene encoding a development protein involved in vesicular traffic in spermiogenesis. Cell Res. 14, 197-207.
51. Qiu, X. B., Ouyang, S. Y., Li, C. J., Miao, S., Wang, L., and Goldberg, A. L. (2006). hRpn13/ADRM1/GP110 is a novel proteasome subunit that binds the deubiquitinating enzyme, UCH37. EMBO J, 25, 5742-5753.
52. Ramos, P. C., Hockendorff, J., Johnson, E. S., Varshavsky, A., and Dohmen, R. J. (1998). Ump1p is required for proper maturation of the 20S proteasome and becomes its substrate upon completion of the assembly. Cell 92, 489-499.
53. Ridley, A. J. (2001). Rho family proteins: Coordinating cell responses. Trends Cell Biol. 11, 471-477.
54. Rivett, A. J. (1993). Proteasomes: Multicatalytic proteinase complexes. Biochem. J. 291(Pt 1), 1-10.
55. Rivkin, E., Kierszenbaum, A. L., Gil, M., and Tres, L. L. (2009). Rnf19a, a ubiquitin protein ligase, and Psmc3, a component of the 26S proteasome, tether to the acrosome membranes and the head-tail coupling apparatus during rat spermatid development. Dev. Dyn. 238, 1851-1861.
56. Rolland, A. D., Jegou, B., and Pineau, C. (2008). Testicular development and spermatogenesis: Harvesting the postgenomics bounty. Adv. Exp. Med. Biol. 636, 16-41.
57. Rottinger, E., Croce, J., Lhomond, G., Besnardeau, L., Gache, C., and Lepage, T. (2006). Nemo-like kinase (NLK) acts downstream of Notch/Delta signalling to downregulate TCF during mesoderm induction in the sea urchin embryo. Development 133, 4341-4353.
58. Sarkar, A., Parikh, N., Hearn, S. A., Fuller, M. T., Tazuke, S. I., and Schulz, C. (2007). Antagonistic roles of Rac and Rho in organizing the germ cell microenvironment. Curr. Biol. 17, 1253-1258.
59. Schmidt, F., Dahlmann, B., Janek, K., Kloss, A., Wacker, M., Ackermann, R., Thiede, B., and Jungblut, P. R. (2006). Comprehensive quantitative proteome analysis of 20S proteasome subtypes from rat liver by isotope coded affinity tag and 2-D gel-based approaches. Proteomics 6, 4622-4632.
60. Schultz, N., Hamra, F. K., and Garbers, D. L. (2003). A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets. Proc. Natl. Acad. Sci. USA 100, 12201-12206.
61. Sha, J., Zhou, Z., Li, J., Yin, L., Yang, H., Hu, G., Luo, M., Chan, H. C., and Zhou, K. (2002). Identification of testis development and spermatogenesisrelated genes in human and mouse testes using cDNA arrays. Mol. Hum. Reprod. 8, 511-517.
62. Solski, P. A., Helms, W., Keely, P. J., Su, L., and Der, C. J. (2002). RhoA biological activity is dependent on prenylation but independent of specific isoprenoid modification. Cell Growth Differ. 13, 363-373.
63. Su, A. I., et al. (2004). A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. USA 101, 6062-6067.
64. Takai, Y., Sasaki, T., and Matozaki, T. (2001). Small GTP-binding proteins. Physiol. Rev. 81, 153-208.
65. Tanaka, K. (2009). The proteasome: Overview of structure and functions. Proc. Jpn. Acad. Ser. B. Phys. Biol. Sci. 85, 12-36.
66. Tanaka, K., Tamura, T., Yoshimura, T., and Ichihara, A. (1992). Proteasomes: Protein and gene structures. New Biol. 4, 173-187.
67. Tengowski, M. W., Feng, D., Sutovsky, M., and 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.
68. Tomaru, U., et al. (2009). Exclusive expression of proteasome subunit {beta}5t in the human thymic cortex. Blood 113, 5186-5191.
69. Trasler, J. M. (2009). Epigenetics in spermatogenesis. Mol. Cell. Endocrinol. 306, 33-36.
70. Unno, M., Mizushima, T., Morimoto, Y., Tomisugi, Y., Tanaka, K., Yasuoka, N., and Tsukihara, T. (2002a). Structure determination of the constitutive 20S proteasome from bovine liver at 2.75 A resolution. J. Biochem. 131, 171-173. (Pubitemid 34194350)
71. Unno, M., Mizushima, T., Morimoto, Y., Tomisugi, Y., Tanaka, K., Yasuoka, N., and Tsukihara, T. (2002b). The structure of the mammalian 20S proteasome at 2.75 A resolution. Structure 10, 609-618.
72. Utech, M., Ivanov, A. I., Samarin, S. N., Bruewer, M., Turner, J. R., Mrsny, R. J., Parkos, C. A., and Nusrat, A. (2005). Mechanism of IFN-gamma-induced endocytosis of tight junction proteins: Myosin II-dependent vacuolarization of the apical plasma membrane. Mol. Biol. Cell 16, 5040-5052.
73. Vega, F. M., and Ridley, A. J. (2008). Rho GTPases in cancer cell biology. FEBS Lett. 582, 2093-2101.
74. Voges, D., Zwickl, P., and Baumeister, W. (1999). The 26S proteasome: A molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 68, 1015-1068.
75. Walz, J., Erdmann, A., Kania, M., Typke, D., Koster, A. J., and Baumeister, W. (1998). 26S proteasome structure revealed by three-dimensional electron microscopy. J. Struct. Biol. 121, 19-29.
76. Wheeler, A. P., and Ridley, A. J. (2004). Why three Rho proteins? RhoA, RhoB, RhoC, and cell motility. Exp. Cell Res. 301, 43-49.
77. White-Cooper, H. (2010). Molecular mechanisms of gene regulation during Drosophila spermatogenesis. Reproduction 139, 11-21.
78. Wong, E. W., and Cheng, C. Y. (2009). Polarity proteins and cell-cell interactions in the testis. Int. Rev. Cell. Mol. Biol. 278, 309-353.
79. Zallen, J. A., Peckol, E. L., Tobin, D. M., and Bargmann, C. I. (2000). Neuronal cell shape and neurite initiation are regulated by the Ndr kinase SAX-1, a member of the Orb6/COT-1/warts serine/threonine kinase family. Mol. Biol. Cell 11, 3177-3190.
80. Zhang, B., and Zheng, Y. (1998). Regulation of RhoA GTP hydrolysis by the GTPase-activating proteins p190, p50RhoGAP, Bcr, and 3BP-1. Biochemistry 37, 5249-5257.
81. Zhang, X., Liu, H., Zhang, Y., Qiao, Y., Miao, S., Wang, L., Zhang, J., Zong, S., and Koide, S. S. (2003). A novel gene, RSD-3/HSD-3.1, encodes a meioticrelated protein expressed in rat and human testis. J. Mol. Med. 81, 380-387.
82. Zhong, L., and Belote, J. M. (2007). The testis-specific proteasome subunit Prosalpha6T of D. melanogaster is required for individualization and nuclear maturation during spermatogenesis. Development 134, 3517-3525.
83. Zwickl, P. (2002). The 20S proteasome. Curr. Top. Microbiol. Immunol. 268, 23-41.