Role of Ubiquitin-Proteasome in Spermatogenesis Process

Document Type : Review Article

Authors

1 Department of Reproductive Biotechnology at Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, The Academic Center for Education, Culture and Research (ACECR), Isfahan, Iran

2 PhD Student, Faculty Member, Department of Reproductive Biotechnology at Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, The Academic Center for Education, Culture and Research (ACECR), Isfahan, Iran

3 Professor, Department of Reproductive Biotechnology, Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, The Academic Center for Education, Culture and Research (ACECR) AND Isfahan Fertility and Infertility Center, Isfahan, Iran

Abstract

Background: Ubiquitin first time was known at 1975, as an 8.5 KDa protein, existing in the cell. Ubiquitin protein has been highly preserved and it has 96% homology gene sequencing between human and yeast. This peptide has been identified as an index of cell mark for removing it via “proteasome”. But, other functions such as participating in the apoptosis, differentiation and etc. have been considered for ubiquitination. In the present study, we tried to concentrate on role of ubiquitin-proteasome system in spermatogenesis process.Methods: Literature search in Entrez PubMed database, as well as other data sources related to ISI Web of Knowledge.Findings: Ubiquitin is secreted through epithelial cells of epididymis during sperm maturation, and placed on surface of abnormal sperm that is deleted. It is possible that some of this sperms escape from deletion in epididymis and appear in ejaculate.Conclusion: Some researches indicated that ubiquitination may increase as a physiological phenomenon during the sperm capacitation which is a positive marker to confirm sperm quality. Therefore, addition to role of ubiquitination in removing abnormal sperm, it can be involved in sperm capacitation process.

Keywords


  1. Xu P, Peng J. Characterization of polyubiquitin chain structure by middle-down mass spectrometry. Anal Chem 2008; 80(9): 3438-44.
  2. Jesenberger V, Jentsch S. Deadly encounter: ubiquitin meets apoptosis. Nat Rev Mol Cell Biol 2002; 3(2): 112-21.
  3. Wojcik C, Benchaib M, Lornage J, Czyba JC, Guerin JF. Proteasomes in human spermatozoa. Int J Androl 2000; 23(3): 169-77.
  4. Glickman MH, Ciechanover A. The ubiquitin--proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 2002; 82(2): 373-428.
  5. Hendil KB. The 19 S multicatalytic "prosome" proteinase is a constitutive enzyme in HeLa cells. Biochem Int 1988; 17(3): 471-7.
  6. Husnjak K, Elsasser S, Zhang N, Chen X, Randles L, Shi Y, et al. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 2008; 453(7194): 481-8.
  7. Yao T, Cohen RE. A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 2002; 419(6905): 403-7.
  8. Guterman A, Glickman MH. Deubiquitinating enzymes are IN/(trinsic to proteasome function). Curr Protein Pept Sci 2004; 5(3): 201-11.
  9. Tulsiani DR, Abou-Haila A. Mammalian sperm molecules that are potentially important in interaction with female genital tract and egg vestments. Zygote 2001; 9(1): 51-69.
  10. Welchman RL, Gordon C, Mayer RJ. Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat Rev Mol Cell Biol 2005; 6(8): 599-609.
  11. Grabbe C, Dikic I. Functional roles of ubiquitin-like domain (ULD) and ubiquitin-binding domain (UBD) containing proteins. Chem Rev 2009; 109(4): 1481-94.
  12. Ubiquitin proteasome pathway [Online]. [cited 2014]; Available from: URL: http://www.bostonbiochem.com/about/ubiquitin-proteasome-pathway-upp
  13. Thrower JS, Hoffman L, Rechsteiner M, Pickart CM. Recognition of the polyubiquitin proteolytic signal. EMBO J 2000; 19(1): 94-102.
  14. Williams PL, Bannister LH, Berry MM, Collins P, Dyson M, Dussek JE, et al. Gray's anatomy. 38th ed. New York, NY: Churchill Livingstone; 1995. p. 125-7.
  15. Fawcett DW, Anderson WA, Phillips DM. Morphogenetic factors influencing the shape of the sperm head. Dev Biol 1971; 26(2): 220-51.
  16. Kay GF, Ashworth A, Penny GD, Dunlop M, Swift S, Brockdorff N, et al. A candidate spermatogenesis gene on the mouse Y chromosome is homologous to ubiquitin-activating enzyme E1. Nature 1991; 354(6353): 486-9.
  17. Wing SS, Jain P. Molecular cloning, expression and characterization of a ubiquitin conjugation enzyme (E2(17)kB) highly expressed in rat testis. Biochem J 1995; 305 ( Pt 1): 125-32.
  18. Rajapurohitam V, Morales CR, El-Alfy M, Lefrancois S, Bedard N, Wing SS. Activation of a UBC4-dependent pathway of ubiquitin conjugation during postnatal development of the rat testis. Dev Biol 1999; 212(1): 217-28.
  19. Kon Y, Endoh D, Iwanaga T. Expression of protein gene product 9.5, a neuronal ubiquitin C-terminal hydrolase, and its developing change in sertoli cells of mouse testis. Mol Reprod Dev 1999; 54(4): 333-41.
  20. Fraile B, Martin R, De Miguel MP, Arenas MI, Bethencourt FR, Peinado F, et al. Light and electron microscopic immunohistochemical localization of protein gene product 9.5 and ubiquitin immunoreactivities in the human epididymis and vas deferens. Biol Reprod 1996; 55(2): 291-7.
  21. Baarends WM, Hoogerbrugge JW, Roest HP, Ooms M, Vreeburg J, Hoeijmakers JH, et al. Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev Biol 1999; 207(2): 322-33.
  22. Chen HY, Sun JM, Zhang Y, Davie JR, Meistrich ML. Ubiquitination of histone H3 in elongating spermatids of rat testes. J Biol Chem 1998; 273(21): 13165-9.
  23. Loir M, Dupressoir T, Lanneau M, Le GF, Sautiere P. High mobility group proteins in ram spermatids. Exp Cell Res 1986; 165(2): 441-9.
  24. Sutovsky P, Ramalho-Santos J, Moreno RD, Oko R, Hewitson L, Schatten G. On-stage selection of single round spermatids using a vital, mitochondrion-specific fluorescent probe MitoTracker(TM) and high resolution differential interference contrast microscopy. Hum Reprod 1999; 14(9): 2301-12.
  25. Baarends WM, van der Laan R, Grootegoed JA. Specific aspects of the ubiquitin system in spermatogenesis. J Endocrinol Invest 2000; 23(9): 597-604.
  26. Bedford JM. Evolution of the sperm maturation and sperm storage functions of the epididymis. In: Fawcett DW, Bedford JM, editors. The spermatozoon. Munich, Germany: Urban and Schwarzenberg; 1979. p. 7–21.
  27. Cooper TG. Epididymis. In: Knobil E, Neil JD, editors. Encyclopedia of reproduction. San Diego, CA: Academic Press; 1998. P. 602–9.
  28. Hermo L, Dworkin J, Oko R. Role of epithelial clear cells of the rat epididymis in the disposal of the contents of cytoplasmic droplets detached from spermatozoa. Am J Anat 1988; 183(2): 107-24.
  29. Rao AR, Bane A, Gustafsson BK. Changes in the morphology of spermatozoa during their passage through the genital tract in dairy bulls with normal and impaired spermat ogenesis. Theriogenology 1980; 14(1): 1-12.
  30. Roussel JD, Stallcup OT, Austin CR. Selective phagocytosis of spermatozoa in the epididymis of bulls, rabbits, and monkeys. Fertil Steril 1967; 18(4): 509-16.
  31. Lippert TH, Seeger H, Schieferstein G, Voelter W. Immunoreactive ubiquitin in human seminal plasma. J Androl 1993; 14(2): 130-1.
  32. Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, Schatten G. Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol Reprod 2000; 63(2): 582-90.
  33. Yeung CH, Schroter S, Wagenfeld A, Kirchhoff C, Kliesch S, Poser D, et al. Interaction of the human epididymal protein CD52 (HE5) with epididymal spermatozoa from men and cynomolgus monkeys. Mol Reprod Dev 1997; 48(2): 267-75.
  34. Kirchhoff C. Molecular characterization of epididymal proteins. Rev Reprod 1998; 3(2): 86-95.
  35. Yeung CH, Cooper TG, Nieschlag E. Human epididymal secreted protein CD52 on ejaculated spermatozoa: correlations with semen characteristics and the effect of its antibody. Mol Hum Reprod 1997; 3(12): 1045-51.
  36. Sinha Hikim AP, Swerdloff RS. Hormonal and genetic control of germ cell apoptosis in the testis. Rev Reprod 1999; 4(1): 38-47.
  37. 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(Pt 9): 1665-75.
  38. Ibrahim NM, Gilbert GR, Loseth KJ, Crabo BG. Correlation between clusterin-positive spermatozoa determined by flow cytometry in bull semen and fertility. J Androl 2000; 21(6): 887-94.
  39. NagDas SK, Winfrey VP, Olson GE. Identification of a hamster epididymal region-specific secretory glycoprotein that binds nonviable spermatozoa. Biol Reprod 2000; 63(5): 1428-36.
  40. Thompson WE, Ramalho-Santos J, Sutovsky P. Ubiquitination of prohibitin in mammalian sperm mitochondria: possible roles in the regulation of mitochondrial inheritance and sperm quality control. Biol Reprod 2003; 69(1): 254-60.
  41. Arnold I, Langer T. Membrane protein degradation by AAA proteases in mitochondria. Biochim Biophys Acta 2002; 1592(1): 89-96.
  42. Honda A, Siruntawineti J, Baba T. Role of acrosomal matrix proteases in sperm-zona pellucida interactions. Hum Reprod Update 2002; 8(5): 405-12.
  43. Buffone MG, Foster JA, Gerton GL. The role of the acrosomal matrix in fertilization. Int J Dev Biol 2008; 52(5-6): 511-22.
  44. Arcelay E, Salicioni AM, Wertheimer E, Visconti PE. Identification of proteins undergoing tyrosine phosphorylation during mouse sperm capacitation. Int J Dev Biol 2008; 52(5-6): 463-72.
  45. Choi YJ, Uhm SJ, Song SJ, Song H, Park JK, Kim T, et al. Cytochrome c upregulation during capacitation and spontaneous acrosome reaction determines the fate of pig sperm cells: linking proteome analysis. J Reprod Dev 2008; 54(1): 68-83.
  46. Kong M, Diaz ES, Morales P. Participation of the human sperm proteasome in the capacitation process and its regulation by protein kinase A and tyrosine kinase. Biol Reprod 2009; 80(5): 1026-35.
  47. Kim KS, Gerton GL. Differential release of soluble and matrix components: evidence for intermediate states of secretion during spontaneous acrosomal exocytosis in mouse sperm. Dev Biol 2003; 264(1): 141-52.
  48. Morales P, Pizarro E, Kong M, Jara M. Extracellular localization of proteasomes in human sperm. Mol Reprod Dev 2004; 68(1): 115-24.
  49. Sutovsky P, Manandhar G, McCauley TC, Caamano JN, Sutovsky M, Thompson WE, et al. Proteasomal interference prevents zona pellucida penetration and fertilization in mammals. Biol Reprod 2004; 71(5): 1625-37.
  50. Sawada H, Sakai N, Abe Y, Tanaka E, Takahashi Y, Fujino J, et al. Extracellular ubiquitination and proteasome-mediated degradation of the ascidian sperm receptor. Proc Natl Acad Sci U S A 2002; 99(3): 1223-8.
  51. Sakai N, Sawada H, Yokosawa H. Extracellular ubiquitin system implicated in fertilization of the ascidian, Halocynthia roretzi: isolation and characterization. Dev Biol 2003; 264(1):
  52. -307.
  53. Sun QY, Fuchimoto D, Nagai T. Regulatory roles of ubiquitin-proteasome pathway in pig oocyte meiotic maturation and fertilization. Theriogenology 2004; 62(1-2): 245-55.
  54. Morales P, Kong M, Pizarro E, Pasten C. Participation of the sperm proteasome in human fertilization. Hum Reprod 2003; 18(5): 1010-7.
  55. Cardullo RA, Thaler CD. Function of the egg's extracellular matrix. In: Hardy DM ,editor. Fertilization. San Diego, CA: Academic Press; 2002. p. 119–52.
  56. Zarei-Kheirabadi M, Shayegan NE, Tavalaee M, Deemeh MR, Arabi M, Forouzanfar M, et al. Evaluation of ubiquitin and annexin V in sperm population selected based on density gradient centrifugation and zeta potential (DGC-Zeta). J Assist Reprod Genet 2012; 29(4): 365-71.
  57. Eskandari-Shahraki M, Tavalaee M, Deemeh MR, Jelodar GA, Nasr-Esfahani MH. Proper ubiquitination effect on the fertilisation outcome post-ICSI. Andrologia 2013; 45(3): 204-10.
  58. Sutovsky P, Schatten G. Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol Reprod 1997; 56(6): 1503-12.
  59. Perry AC, Wakayama T, Cooke IM, Yanagimachi R. Mammalian oocyte activation by the synergistic action of discrete sperm head components: induction of calcium transients and involvement of proteolysis. Dev Biol 2000; 217(2): 386-93.
  60. Bose R, Manku G, Culty M, Wing SS. Ubiquitin-proteasome system in spermatogenesis. Adv Exp Med Biol 2014; 759: 181-213.
  61. Mochida K, Tres LL, Kierszenbaum AL. Structural features of the 26S proteasome complex isolated from rat testis and sperm tail. Mol Reprod Dev 2000; 57(2): 176-84.
  62. Josefsberg LB, Kaufman O, Galiani D, Kovo M, Dekel N. Inactivation of M-phase promoting factor at exit from first embryonic mitosis in the rat is independent of cyclin B1 degradation. Biol Reprod 2001; 64(3): 871-8.
  63. Hwang SY, Oh B, Knowles BB, Solter D, Lee JS. Expression of genes involved in mammalian meiosis during the transition from egg to embryo. Mol Reprod Dev 2001; 59(2): 144-58.
  64. Amann RP. Can the fertility potential of a seminal sample be predicted accurately? J Androl 1989; 10(2): 89-98.
  65. Boue F, Sullivan R. Cases of human infertility are associated with the absence of P34H an epididymal sperm antigen. Biol Reprod 1996; 54(5): 1018-24.
  66. Rawe VY, Olmedo SB, Benmusa A, Shiigi SM, Chemes HE, Sutovsky P. Sperm ubiquitination in patients with dysplasia of the fibrous sheath. Hum Reprod 2002; 17(8): 2119-27.
  67. Bronson RA. Antisperm antibodies: a critical evaluation and clinical guidelines. J Reprod Immunol 1999; 45(2): 159-83.
  68. Primakoff P, Lathrop W, Bronson R. Identification of human sperm surface glycoproteins recognized by autoantisera from immune infertile men, women, and vasectomized men. Biol Reprod 1990; 42(5-6): 929-42.
  69. Sutovsky P, Terada Y, Schatten G. Ubiquitin-based sperm assay for the diagnosis of male factor infertility. Hum Reprod 2001; 16(2): 250-8.