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Archives of Andrology
Journal of Reproductive Systems
Volume 53, 2007 - Issue 4
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REVIEW AND HYPOTHESIS

Role(s) of the Serine/Threonine Protein Phosphatase 1 on Mammalian Sperm Motility

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Pages 169-177 | Received 31 Dec 2006, Accepted 26 Feb 2007, Published online: 09 Jul 2009

REFERENCES

  • Achanzar, W. E. and Ward, S. (1997) A nematode gene required for sperm vesicle fusion. J. of Cell Sci 110:1073–1081.
  • Aitken, A., Collinge, D. B., van Heusden, B. P., Isobe, T., Roseboom, P. H., Rosenfeld, G. and Soll, J. (1992) 14-3-3 proteins: A highly conserved, widespread family of eukaryotic proteins. Treads Biochem Sci 17:498–501.
  • Amann, R. P., Hay, S. R. and Hammerstedt, R. H. (1982) Yield, characteristics, motility and cAMP content of sperm isolated from seven regions of ram epididymis. Biol Reprod 27:723–733.
  • Andreassen, P. R., Lacroix, F. B., Villa-Moruzzi, E. and Margolis, R. L. (1998) Differential subcellular localization of protein phosphatase-1 alpha, gamma1, and delta isoforms during both interphase and mitosis in mammalian cells. J Cell Biol 141:1207–1215.
  • Armstrong, V. L., Clulow, J., Murdoch, R. N. and Jones, R. C. (1994) Intracellular signal transduction mechanisms of rat epididymal spermatozoa and their relationship to motility and metabolism. Mol Reprod Dev 38:77–84.
  • Ashizawa, K., Wishart, G. J., Tomonaga, H., Nishinakama, K. and Tsuzuki, Y. (1994) Presence of protein phosphatase type 1 and its involvement in temperature-dependent flagellar movement of fowl spermatozoa. FEBS Letters 350:130–134.
  • Ayllon, C., Cayla, X., Garcia, A., Fleischer, A. and Rebollo, A. (2002) The antiapoptotic molecules Bcl-xL and Bcl-w target protein phosphatase 1 alpha to Bad. Eur J Immunol 32:1847–1855.
  • Barua, M., Bhattacharyya, U. and Majumder, G. C. (1985) Occurrence of an ecto-phosphoprotein phosphatase in goat epididymal spermatozoa. Biochem Int 10:733–741.
  • Bedford, J. M. and Hoskins, D. D. (1990) The mammalian spermatozoa. In: Marshall's physiology of reproduction. Edinburgh: Churchill Livingstone, , UK.
  • Bollen, M. and Stalmans, W. (1992) The structure, role and regulation of type 1 protein phosphatase. Critical reviews in Biochemistry and molecular biology 27:227–281.
  • Bollen, M. (2001) Combinatorial control of protein phosphatase-1. Trends In Biochemical Sciences 26:426–431.
  • Bradshaw, J. M., Kubota, Y., Meyer, T. and Schulman, H. (2002) An ultrasensitive Ca2 + /calmodulin-dependent protein kinase II-protein phosphatase 1 switch facilitates specificity in postsynaptic calcium signaling. Proc Natl Acad Sci USA 100:10512–10517.
  • Brandt, H. and Hoskins, D. D. (1980) A cAMP-dependent phosphorylated motility protein in bovine epididymal sperm. J Biol Chem 255:982–987.
  • Brokaw, C. J. (1987) Regulation of sperm flagellar motility by calcium and cAMP-dependent phosphorylation. J Cell Biochem 35:175–184.
  • Browne, G. J., Fardilha, M., Oxenham, S. K., Wu, W., Helps, N. R., da Cruz, E., Silva, O. A., Cohen, P. T. W., da Cruz, E. and Silva, E. F. (2007) SARP, a new alternatively spliced protein phosphatase 1 and DNA interacting protein. Biochem J 402:187–196.
  • Cardone, L., de Cristofaro, T., Affaitati, A., Garbi, C., Ginsberg, M. D., Saviano, M., Varrone, S., Rubin, C. S., Gottesman, M. E., Avvedimento, E. V. and Feliciello, A. (2002) A-Kinase anchor protein 84/121 are targeted to mitochondria and mitotic spindles by overlapping amino-terminal motifs. J of Mol Biol 320:663–675.
  • Ceulemans, H., Vulsteke, V., De Maeyer, M., Tatchell, K., Stalmans, W. and Bollen, M. (2002) Binding of the concave surface of the Sds22 superhelix to the alpha 4/alpha 5/alpha 6-triangle of protein phosphatase-1. J of Biological Chemistry 277:47331–47337.
  • Ceulemans, H. and Bollen, M. (2004) Functional diversity of protein phosphatase-1, a cellular economizer and reset button. Physiological Review 84:1–39.
  • Chaudhry, P. S., Creagh, S., Yu, N. and Brokaw, C. J. (1995) Multiple protein kinase activities required for activation of sperm flagellar motility. Cell Motility and the Cytoskeleton 32:65–79.
  • Cohen, P. (1989) The structure and regulation of protein phosphatases. Annu Rev Biochem. 58:453–508.
  • Cohen, P. T. (2002) Protein phosphatase 1-targeted in many directions. J of Cell Science 15:241–256.
  • Cooper, T. G. (1986). The epididymis, sperm maturation and fertilization, Berlin, Germany: Heidelberg Springer-Verlag.
  • Dohadwala, M., da Cruz E Silva, E. F., Hall, F. L., Williams, R. T., Carbonaro-Hall, D. A., Nairn, A. C., Greengard, P. and Berndt, N. (1994) Phosphorylation and inactivation of protein phosphatase 1 by cyclin-dependent kinases. Proc Natl Acad Sci USA 91:6408–6412.
  • Ecroyd, H., Jones, R. C. and Aitken, R. J. (2003) Tyrosine phosphorylation of HSP-90 during mammalian sperm capacitation. Biol Reprod 69:1801–1807.
  • Garcia-Gimeno, M. A., Munoz, I., Arino, J. and Sanz, P. (2003) Molecular characterization of Ypi1, a novel saccharomyces cerevisiae type 1 protein phosphatase inhibitor. J Biol Chem 278:47744–47752.
  • Habermacher, G. and Sale, W. S. (1996) Regulation of flagellar dynein by an axonemal type-1 phosphatase in Chlamydomonas. J Cell Sci 109:1899–1907.
  • Hagaman, J. R., Moyer, U. S., Bachman, E. S., Sibony, M., Magyar, P. L., Welch, J. E., Smithies, O., Krege, J. H. and O'Brien, D. A. (1998) Angiotensin-converting enzyme and male fertility. Proc Natl Acad Sci USA 95:2552–2557.
  • Han, Y., Feng, H., Cheung, C. K., Lam, P. M., Wang, C. C. and Haines, C. J. (2007) Expression of a novel T-complex testis expressed 5 (Tctex5) in mouse testis, epididymis and spermatozoa. Molecular Reproduction and Development 74:1132–1140.
  • Hemmings, B. A., Rensnik, T. J. and Cohen, P. (1982) Reconstitution of a Mg-ATP-dependent protein phosphatase and its activation through a phosphorylation mechanism. FEBD Letters 150:319–324.
  • Hrabchak, C. and Varmuza, S. (2004) Identification of the spermatogenic zip protein Spz1 as a putative protein phosphatase-1 (PP1) regulatory protein that specifically binds the PP1cgamm2 splice variant in mouse testis. J Biol Chem 279:37079–37086.
  • Hsu, S. H., Hsieh-Li, H. M. and Li, H. (2004) Dysfunctional spermatogenesis in transgenic mice overexpressing bHLH-Zip transcription factor, Spz1. Exp Cell Res 294:185–198.
  • Huang, B., Ramanis, Z. and Luck, D. J. (1982) Suppressor mutations in Chlamydomonas reveal a regulatory mechanism for Flagellar function. Cell 28:115–124.
  • Huang, H. S., Pozarowski, P., Gao, Y., Darzynkiewicz, Z. and Lee, E. Y. C. (2005a) Protein phosphatase-inhibitor-3 colocalized to the nucleoli and centrosomes with PP1γ1 and PP1α, respectively. Arch Biochem and Biophy 443:33–44.
  • Huang, Z., Khatra, B., Bollen, M., Carr, D. W. and Vijayaraghavan, S. (2002) Sperm PP1gamma2 is regulated by a homologue of the yeast protein phosphatase binding protein sds22. Biol Reprod 67:1936–1942.
  • Huang, Z., Myers, K., Khatra, B. and Vijayaraghavan, S. (2004a) Protein 14-3-3zetta binds to protein phosphatase PP1gamma2 in bovine epididymal spermatozoa. Biol Reprod 71:177–184.
  • Huang, Z. and Vijayaraghavan, S. (2004b) Increased phosphorylation of a distinct subcellular pool of protein phosphatase, PP1gamma2, during epididymal sperm maturation. Biol Reprod 70:439–447.
  • Huang, Z., Somanath, P. R., Chakrabarti, R., Eddy, E. M. and Vijayaraghavan, S. (2005b) Changes in intracellular distribution and activity of protein phosphatase PP1gamma2 and its regulating proteins in spermatozoa lacking AKAP4. Biol Reprod 72:384–392.
  • Inaba, K. (2003) Molecular architecture of the sperm flagella: Molecules for motility and signaling. Zoological Science 20:1043–1056.
  • Jurisicova, A., Lopes, S., Meriano, J., Oppedisano, L., Casper, R. F. and Varmuza, S. (1999) DNA damage in round spermatids of mice with a targeted disruption of the PP1cgamma gene and in testicular biopsies of patients with non-obstructive azoospermia. Mol Human Reprod 5:323–330.
  • Kessler, S. P., Rowe, T. M., Gomos, J. B., Kessler, P. M. and Sen, G. C. (2000) Physiological non-equivalence of the two isoforms of anti-tension-converting enzyme. J Biol Chem 275:26259–26264.
  • Kitagawa, Y., Sasaki, K., Shima, H., Shibuya, M., Sugimura, T. and Nagao, M. (1990) Protein phosphatases possibly involved in rat spermatogenesis. Biochem Biophy Res Commun 171:230–235.
  • Krege, J. H., John, S. W., Langenbach, L. L., Hodgin, J. B., Hagaman, J. R., Vaqchman, E. S., Jennette, J. C., O'Brien, D. A. and Smithies, O. (1995) Male-female differences in fertility and blood pressure in ACE-deficient mice. Nature 375:146–148.
  • Kwon, Y. G., Huang, H. B., Desdouits, F., Girault, J. A., Greengard, P. and Nairn, A. C. (1997) Cell cycle-dependent phosphorylation of mammalian protein phosphatase 1 by cdc2 kinase. Proc Natl Acad Sci USA 94:3536–3541.
  • Lesage, B., Beullens, M., Nuytten, M., Van Eynde, A., Keppens, S., Himpens, B. and Bollen, M. (2004) Interactor-mediated nuclear translocation and retention of protein phosphatase-1. J Biol Chem 279:55978–55984.
  • Liu, C. W., Wang, R. H., Rohadwala, M., Schonthal, A. H., Cilla-Moruzzi, E. and Berndt, N. (1999) Inhibitory phosphoryalation of PP1alpha catalytic subunit during the G(1)/S transition. Journal of Biological Chemistry 274:29470–29475.
  • Mann, T. and Lutwak-Mann, C. (1981). Male reproductive function and semen: Themes and trends in physiology, biochemistry and investigative andrology. Berlin, Germany: Springer-Verlag.
  • Miki, K. and Eddy, E. M. (1998) Identification of tethering domains for protein kinase A type I alpha regulatory subunits on sperm fibrous sheath protein FSC1. J Biol Chem 273:34384–34390.
  • Miki, K., Willis, W. D., Brown, P. R., Goulding, E. H., Fulcher, K. D. and Eddy, E. M. (2002) Targeted disruption of the Akap4 gene causes defects in sperm flagellum and motility. Dev Biol 248:331–342.
  • Miki, K., Qu, W., Goulding, E. H., Eillis, W. D., Bunch, D. O., Strader, L. F., Perreault, S. D., Eddy, E. M. and O'Brien, D. A. (2004) Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proc Natl Acad Sci USA 101:16501–16506.
  • Mishra, S., Somanath, P. R., Huang, Z. and Vijayaraghavan, S. (2003) Binding and inactivation of the germ cell-specific protein phosphatase PP1gamma2 by sds22 during epididymal sperm maturation. Biol Reprod 69:1572–1579.
  • Mohri, H. and Yanagimachi, R. (1980) Characteristics of motor apparatus in testicular, epididymal and ejaculated spermatozoa. Exp Cell Res 127:191–196.
  • Morton, B., Harrigan-Lum, L., Albagli, L. and Joose, T. (1974) The activation of motility in quiescent hamster sperm from the epididymis by calcium and cyclic nucleotides. Biochem Biophys Res Commun 56:372–379.
  • Nolan, M. A., Babcock, D. F., Wennemuth, G., Brown, W., Burton, K. A. and McKnight, G. S. (2004) Sperm-specific protein kinase A catalytic subunit Calpha2 orchestrates cAMP signaling for male fertility. Proc Natl Acad Sci USA. 101:13483–13488.
  • Nomura, M., Yoshida, M. and Morisawa, M. (2004) Calmodulin/calmodulin-dependent protein kinase II mediates SAAD-induced motility activation of ascidian sperm. Cell Motil Cytoskeleton 59:28–37.
  • Oppedisano-Wells, L., Haines, G., Hrabchak, C., Fimia, G., Elliott, R., Sassone-Corsi, P., Varmuza, S. (2002) The rate of aneuploidy is altered in spermatids from infertile mice. Human Reprod 17:710–717.
  • Oppedisano-Wells, L. and Varmuza, S. (2003) Protein phosphatase 1cgamma is required in germ cells in murine testis. Mol Reprod and Dev 65:157–166.
  • Pauls, K., Metzger, R., Steger, K., Knonisch, T., Danilov, S. and Franke, F. E. (2003) Isoforms of angiotension I-converting enzyme is the development and differentiation of human testis and epididymis. Andrologia 35:32–43.
  • Piperno, G., Mead, K. and Shestak, W. (1992) The inner dynein arms I2 interact with a “dynein regulatory complex” in Chlamydomonas flagella. J Cell Biol 118:1455–1463.
  • Piperno, G., Mead, K., LeDizet, M. and Moscatelli, A. (1994) Mutations in the “dynein regulatory complex” alter the ATP-insensitive binding sites for inner arm dyneins in Chlamydomonas axonemes. J Cell Biol 125:1109–1117.
  • Porter, M. E., Power, J. and Dutcher, S. K. (1992) Extragenic suppressors of paralyzed flagellar mutations in Chlamydomonas reinhardtii identify loci that alter the inner dynein arms. J Cell Biol 118:1163–1176.
  • Richter, K. and Buchner, J. (2001) Hsp90: Chaperoning signal transduction. J Cell Physiol 1883:281–290.
  • San Agustin, J. T. and Witman, G. B. (1994) Role of cAMP in the reactivation of demembranated ram spermatozoa. Cell Motility and the Cytoskeleton 27:206–218.
  • Satir, P., Barkalow, K. and Hamasaki, T. (1993) The control of ciliary beat frequency. Trends in Cell Biol 3:409–412.
  • Schulh, S. M., Calson, A. E., McKnight, S., Conti, M., Hille, B. and Babcock, D. F. (2006) Signaling pathways for modulation of mouse sperm motility by adenosine and catecholamine agonists. Biol Reprod 74:492–500.
  • Shenolikar, C. and Nairn, A. C. (1991) Protein phosphatase: Recent progress. Adv Second Messenger Phosphoprotein Res 23:1–121.
  • Shima, H., Haneji, T., Hatano, Y., Kasugai, I., Sugimura, T. and Nagao, M. (1993) Protein phosphatase 1 gamma 2 is associated with nuclei of meiotic cells in rat testis. Biochem Biophy Res Commun 194:930–937.
  • Si, Y., and Okuno, M. (1995) Activation of mammalian sperm motility by regulation of microtubule sliding via cyclic adenosine 5′-monophosphate-dependent phosphorylation. Biol Reprod 53:1081–1087.
  • Smith, G. D., Wolf, D. P., Trautman, K. C., Sila, E. F., Greengard, P. and Vijayaraghavan, S. (1996) Primate sperm contain protein phosphatase 1, a biochemical mediator of motility. Biol Reprod 54:719–727.
  • Smith, G. D., Wolf, D. P., Trautman, K. C. and Vijayaraghavan, S. (1999) Motility of macaque epididymal sperm: The role of protein phosphatase and glycogen synthase kinase-3 activities. J Androl 20:47–53.
  • Somanath, P. R., Jack, S. L. and Vijayaraghavan, S. (2004) Changes in sperm glycogen synthase kinase-3 serine phosphorylation and activity accompany motility initiation and stimulation. J Androl 25:605–617.
  • Swarup, D. and Garbers, D. L. (1992) Phosphoprotein phosphatase activity of sea urchin spermatozoa. Biol Reprod 26:953–960.
  • Tang, F. Y. and Hoskins, D. D. (1975) Phosphoprotein phosphatase of bovine epididymal sperm. Biochem Biophys Res Commun 62:328–335.
  • Tash, J. S. and Bracho, G. E. (1994) Regulation of sperm motility: Emerging evidence for a major role for protein phosphatase. J Androl 15:505–509.
  • Tash, J. S., Krinks, M., Patel, J., Means, R. L., Klee, C. B. and Means, A. R. (1988) Identification, characterization, and functional correlation of calmodulin-dependent protein phosphatase in sperm. J Cell Biol 106:1625–1633.
  • Toshima, J., Toshima, J. Y., Takeuchi, K., Mori, R. and Mizuno, K. (2001) Cofilin phosphorylation and actin reorganization activities of testicular protein kinase 2 and its predominant expression in testicular Sertoli cells. J Biol Chem 276:31449–31458.
  • Trinkle-Mulcahy, L., Sleeman, J. E. and Lamond, A. I. (2001) Dynamic targeting of protein phosphatase 1 within the nuclei of living mammalian cells. J cell Sci 114:1207–1215.
  • Trinkle-Mulcahy, L., Andrews, P. D., Wickramasinghe, S., Sleeman, J., Prescott, A., Lam, Y. W., Lyon, C., Swedlow, J. R. and Lamond, A. I. (2003) Time-lapse imaging reveals dynamic re-localization of PP1γ throughout the mammalian cell cycle. Mol Biol Cell 14:107–117.
  • Trinkle-Mulcahy, L., Anderson, J., Lam, Y. W., Moorhead, G., Mann, M. and Lamonel, A. I. (2006) Repo-Man recruits PP1γ to chromatin and is essential for cell viability. J Cell Biol 172:679–692.
  • Tzivion, G. and Avruch, J. (2002) 14-3-3 proteins: Active cofactors in cellular regulation by serine/threonine phosphorylation. J Biol Chem 277:3061–3064.
  • Varmuza, S., Jurisicova, A., Okano, K., Hudson, J., Boekelheide, K. and Shipp, E. B. (1999) Spermiogenesis is impaired in mice bearing a targeted mutation in the protein phosphatase 1cgamma gene. Del Biol 205:98–110.
  • Vijayaraghavan, S., Stephens, D. T., Trautman, K., Smith, G. D., Khatra, B., da Cruz e Silva, E. F., Greengard, P. (1996) Sperm motility development in the epididymis is associated with decreased glycogen synthase kinase-3 and protein phosphatase 1 activity. Biol Reprod 54:709–718.
  • Wade, M. A., Jones, R. C., Murdoch, R. N. and Aitken, R. J. (2003) Motility activation and second messenger signaling in spermatozoa from rat cauda epididymidis. Reprod 125:175–183.
  • Yaffe, M. B. and Elia, A. E. (2001) Phosphoserine/threonine-binding domains. Curr Opin Cell Biol 13:131–138.
  • Yang, P., Fox, L., Colbran, R. J. and Sale, W. S. (2000) Protein phosphatases PP1 and PP2A are located in distinct positions in the Chlamydomonas flagellar axoneme. J Cell Sci 113:91–102.
  • Yeung, C. H. (1984) Effects of cyclic AMP on the motility of mature and immature hamster epididymal spermatozoa studied by reactivation of the demembraned cells. Gamete Res 9:99–114.
  • Yoshimura, M. and Shingyoji, C. (1999) Effects of the central pair apparatus on microtubule sliding velocity in sea urchin sperm flagella. Cell Structure and Function 24:43–54.
  • Zhang, J., Zhang, L., Zhao, S. and Lee, E. Y. C. (1998) Identification and characterization of the human HCG V gene product as a novel inhibitor of protein phosphatase-1. Biochem 37:16728–16734.

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