Skip to main content
PMC home page
Journal of Cellular and Molecular Medicine logoLink to Journal of Cellular and Molecular Medicine
. 2007 May 1;8(1):77–84. doi: 10.1111/j.1582-4934.2004.tb00261.x

Role of human prostasomes in the activation of spermatozoa

G Arienti 1,✉, E Carlini 1, C Saccardi 2, C A Palmerini 2,✉
PMCID: PMC6740304  PMID: 15090262

Abstract

Prostasomes are small vesicles of prostatic origin contained in human semen. Their composition is peculiar under many aspects. Cholesterol is abundant and many proteins are endowed with enzymatic or other activities. The function of prostasomes has been amply debated and several hypotheses have been put forward. The liquefaction of semen, spermatozoa motility, antibacterial activity and immunological functions have been related to prostasomes. Under certain aspects, prostasomes resemble synaptosomes. The fusion of prostasomes to spermatozoa enriches spermatozoa with cholesterol and causes bursts of cytoplasmic sperm calcium. The interaction of spermatozoa and prostasomes should be limited to vagina since prostasomes are immobile and do not follow spermatozoa in the superior female genital tract. Calcium bursts would increase spermatozoa motility, where cholesterol would decapacitate spermatozoa, so preventing untimely activation. Since spermatozoa receive many different molecules from prostasomes, additional effects are also possible. Prostasomes makes spermatozoa more apt to be activated by progesterone in the proximity of the ovum. Therefore, the fusion between spermatozoa and prostasomes would influence spermatozoa behaviour under many aspects and might be relevant for fecundation. The richness of molecular species in prostasomes is amazing and these small vesicles are expected to lead to many more discoveries in the field of human reproduction.

Keywords: acrosomal reaction, cytosolic calcium, membrane fusion, prostasomes, semen, spermatozoa

References

  • 1. Ronquist G., Brody I., The prostasome: its secretion and function in man, Biochim. Biophys. Acta, 822: 203–218, 1985. [DOI] [PubMed] [Google Scholar]
  • 2. Brody I., Ronquist G., Gottfries A., Ultrastructural localization of the prostas, Ups. J. Med. Sci., 88: 63–80, 1983. [DOI] [PubMed] [Google Scholar]
  • 3. Carlsson L., Nilsson O., Larsson A., Stridsberg M., Sahlen G., Ronquist G., Characteristics of human prostasomes isolated from three different sources, Prostate, 54: 322–330, 2003. [DOI] [PubMed] [Google Scholar]
  • 4. Nilsson B.O., Egevad L., Jin M., Ronquist G., Busch C., Distribution of prostasomes in neoplastic epithelial prostate cells, Prostate, 39: 36–40, 1999. [DOI] [PubMed] [Google Scholar]
  • 5. Nilsson B.O., Jin M Ronquist G., Immunolocalization of prostasomes in the human prostate, Ups. J. Med. Sci., 101: 149–157, 1996. [DOI] [PubMed] [Google Scholar]
  • 6. Sahlen G.E., Egevad L., Ahlander A., Norlen B.J., Ronquist G., Nilsson B.O., Ultrastructure of the secretion of prostasomes from benign and malignant epithelial cells in the prostate, Prostate, 53: 192–199, 2002. [DOI] [PubMed] [Google Scholar]
  • 7. Stridsberg M., Fabiani R., Lukinius A., Ronquist G., Prostasomes are neuroendocrine‐like vesicles in human semen, Prostate, 29: 287–295, 1996. [DOI] [PubMed] [Google Scholar]
  • 8. Arienti G., Carlini E., De Cosmo A.M., Di Profio P., Palmerini C.A., Prostasome‐like particles in stallion semen, Biol. Reprod., 59: 309–313, 1998. [DOI] [PubMed] [Google Scholar]
  • 9. Minelli A., Moroni M., Martinez E., Mezzasoma I., Ronquist G., Occurrence of prostasome‐like membrane vesicles in equine seminal plasma, J. Reprod. Fertil., 114: 237–243, 1998. [DOI] [PubMed] [Google Scholar]
  • 10. Frenette G., Lessard C., Sullivan R., Selected proteins of “prostasome‐like particles” from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull, Biol. Reprod., 67: 308–313, 2002. [DOI] [PubMed] [Google Scholar]
  • 11. Arvidson G., Ronquist G., Wikander G., Ojteg A.C., Human prostasome membranes exhibit very high cholesterol/phospholipid ratios yielding high molecular ordering, Biochim. Biophys. Acta, 984: 167–173, 1989. [DOI] [PubMed] [Google Scholar]
  • 12. Arienti G., Carlini E., Polci A., Cosmi E.V., Palmerini C.A., Fatty acid pattern of human prostasome lipid, Arch. Biochem. Biophys., 358: 391–395, 1998. [DOI] [PubMed] [Google Scholar]
  • 13. Bordi F., Cametti C., De Luca F., Carlini E., Palmerini C.A., Arienti G., Hydrodynamic radii and lipid transfer in prostasome self‐fusion, Arch. Biochem. Biophys., 396: 10–15, 2001. [DOI] [PubMed] [Google Scholar]
  • 14. Mack S.R., Everingham J., Zaneveld L.J.D., Isolation and partial characterization of the plasma membrane from human spermatozoa, J. Expt. Zool., 240: 127–136, 1986. [DOI] [PubMed] [Google Scholar]
  • 15. Carlini E., Palmerini C.A., Cosmi E.V., Arienti G., Fusion of sperm with prostasomes: effects on membrane fluidity, Arch. Biochem. Biophys., 343: 6–12, 1997. [DOI] [PubMed] [Google Scholar]
  • 16. Poulos A., White I.G., The phospholipid composition of human spermatozoa and seminal plasma, J. Reprod. Fertil., 53: 265–272, 1973. [DOI] [PubMed] [Google Scholar]
  • 17. Benoff S., Preliminaries to fertilization. The role of cholesterol during capacitation of human spermatozoa, Hum. Reprod., 8: 2001–2008, 1993. [DOI] [PubMed] [Google Scholar]
  • 18. Fabiani R., Functional and biochemical characteristics of human prostasomes. Minireview based on a doctoral, Ups. J. Med. Sci., 99: 73–111, 1994. [DOI] [PubMed] [Google Scholar]
  • 19. Ronquist G., Frithz G.G., Prostasomes in human semen contain ADP and GDP, Acta Eur. Fertil., 17: 273–276, 1986. [PubMed] [Google Scholar]
  • 20. Ek P., Malm J., Lilja H., Carlsson L., Ronquist G., Exogenous protein kinases A and C, but not endogenous prostasome‐associated protein kinase, phosphorylate semenogelins I and II from human semen, J. Androl., 23: 806–814, 2002. [PubMed] [Google Scholar]
  • 21. Fabiani R., Ronquist G., Association of some hydrolytic enzymes with the prostasome membrane and their differential responses to detergent and PIPLC treatment, Prostate, 27: 95–101, 1995. [DOI] [PubMed] [Google Scholar]
  • 22. Minelli A., Allegrucci C., Mezzasoma I., Ronquist G., Lluis C., Franco R., CD26 and adenosine deaminase interaction: its role in the fusion between horse membrane vesicles and spermatozoa, Biol. Reprod., 61: 802–808, 1999. [DOI] [PubMed] [Google Scholar]
  • 23. Olsson I., Ronquist G., Isoenzyme pattern of lactate dehydrogenase associated with human prostasomes, Urol. Int., 45: 346–349, 1990. [DOI] [PubMed] [Google Scholar]
  • 24. Utleg A.G., Yi E.C., Xie T., Shannon P., White J.T., Goodlett D.R., Hood L., Lin B., Proteomic analysis of human prostasomes, Prostate, 56: 150–161, 2003. [DOI] [PubMed] [Google Scholar]
  • 25. Stegmayr B., Ronquist G., Promotive effect on human sperm progressive motility by prostasomes, Urol. Res., 10: 253–257, 1982. [DOI] [PubMed] [Google Scholar]
  • 26. Lilja H., Laurel C.B., Liquefaction of coagulated human semen, Scand. J. Clin. Lab. Invest., 44: 447–452, 1984. [DOI] [PubMed] [Google Scholar]
  • 27. Kelly R.W., Holland P., Skibinski G., Harrison C., McMillan L., Hargreave T., James K., Extracellular organelles (prostasomes) are immunosuppressive components of human semen, Clin. Exp. Immunol., 86: 550–556, 1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28. Skibinski G., Kelly R.W., Harkiss D., James K., Immunosuppression by human seminal plasma‐extracellular organelles (prostasomes) modulate activity of phagocytic cells, Am. J. Reprod. Immunol., 28: 97–103, 1992. [DOI] [PubMed] [Google Scholar]
  • 29. Kelly R.W., Immunosuppressive mechanisms in semen: implications for contraception, Hum. Reprod., 10: 1686–1693, 1995. [DOI] [PubMed] [Google Scholar]
  • 30. Lazarevic M., Skibinski G., Kelly R.W., James K., Immunomodulatory effects of extracellular secretory vesicles isolated from bovine semen, Vet. Immunol. Immunopathol., 44: 237–250, 1995. [DOI] [PubMed] [Google Scholar]
  • 31. Babiker A.A., Ronquist G., Nilsson U.R., Nilsson B., Transfer of prostasomal CD59 to CD59‐deficient red blood cells results in protection against complement‐mediated hemolysis, Am. J. Reprod. Immunol., 47: 183–192, 2002. [DOI] [PubMed] [Google Scholar]
  • 32. Carlsson L., Ronquist G., Stridsberg M., Johansson L., Motility stimulant effects of prostasome inclusion in swim‐up medium on cryopreserved human spermatozoa, Arch. Androl., 38: 215–221, 1997. [DOI] [PubMed] [Google Scholar]
  • 33. Fabiani R., Johansson L., Lundkvist O., Ronquist G., Prolongation and improvement of prostasome promotive effect on sperm forward motility, Eur. J. Obstet. Gynecol. Reprod. Biol., 58: 191–198, 1995. [DOI] [PubMed] [Google Scholar]
  • 34. Fabiani R., Johansson L., Lundkvist O., Ulmsten U., Ronquist G., Promotive effect by prostasomes on normal human spermatozoa exhibiting no forward motility due to buffer washings, Eur. J. Obstet. Gynecol. Reprod. Biol., 57: 181–188, 1994. [DOI] [PubMed] [Google Scholar]
  • 35. Fabiani R., Johansson L., Lundkvist O., Ronquist G., Enhanced recruitment of motile spermatozoa by prostasome inclusion in swim‐up medium, Hum. Reprod., 9: 1485–1489, 1994. [DOI] [PubMed] [Google Scholar]
  • 36. Ronquist G., Stegmayr B., Brody I., Gottfries A., Prostasomes‐a newly discovered organelle that increases sperm motility, Lakartidningen, 80: 810–813, 1983. [PubMed] [Google Scholar]
  • 37. Arienti G., Carlini E., Nicolucci A., Cosmi E.V., Santi F., Palmerini C.A., The motility of human spermatozoa as influenced by prostasomes at various pH levels, Biol. Cell, 91: 51–54, 1999. [PubMed] [Google Scholar]
  • 38. Carlsson L., Pahlson C., Bergquist M., Ronquist G., Stridsberg M., Antibacterial activity of human prostasomes, Prostate, 44: 279–286, 2000. [DOI] [PubMed] [Google Scholar]
  • 39. Andersson E., Sorensen O.E., Frohm B., Borregaard N., Egesten A., Malm J., Isolation of human cationic antimicrobial protein‐18 from seminal plasma and its association with prostasomes, Hum. Reprod., 17: 2529–2534, 2002. [DOI] [PubMed] [Google Scholar]
  • 40. Saez F., Motta C., Boucher D., Grizard G., Antioxidant capacity of prostasomes in human semen, Mol. Hum. Reprod., 4: 667–672, 1998. [DOI] [PubMed] [Google Scholar]
  • 41. Ronquist G., Nilsson B.O., Hjerten S., Interaction between prostasomes and spermatozoa from human semen, Arch. Androl., 24: 147–157, 1990. [DOI] [PubMed] [Google Scholar]
  • 42. Arienti G., Carlini E., Palmerini C.A., Fusion of human sperm to prostasomes at acidic pH, J. Membr. Biol., 155: 89–94, 1997. [DOI] [PubMed] [Google Scholar]
  • 43. Hoekstra D., De Boer T., Klappe K., Wilschut J., Fluorescent method for measuring the kinetic of fusion between biological membranes, Biochemistry, 23: 5675–5681, 1984. [DOI] [PubMed] [Google Scholar]
  • 44. Corazzi L., Pistolesi R., Arienti G., The fusion of liposomes to rat brain microsomal membranes regulates phosphatidylserine synthesis, J. Neurochem., 56: 207–212, 1991. [DOI] [PubMed] [Google Scholar]
  • 45. Raboch J., Skaková J., The pH of human ejaculates, Fertil. Steril., 16: 252–256, 1965. [DOI] [PubMed] [Google Scholar]
  • 46. Meinertz H., Antisperm antibodies in split ejaculates, Am. J. Reprod. Immunol. 26: 110–113, 1991. [DOI] [PubMed] [Google Scholar]
  • 47. Arienti G., Carlini E., Verdacchi R., Cosmi E.V., Palmerini C.A., Prostasome to sperm transfer of CD13/aminopeptidase N (EC 3.4.11.2), Biochim. Biophys. Acta 1336: 533–538, 1997. [DOI] [PubMed] [Google Scholar]
  • 48. Arienti G., Carlini E., Verdacchi R., Palmerini C.A., Transfer of aminopeptidase activity from prostasomes to sperm, Biochim. Biophys. Acta 1336: 269–274, 1997. [DOI] [PubMed] [Google Scholar]
  • 49. Arienti G., Polci A., Carlini E., Palmerini C.A., Transfer of CD26/dipeptidyl peptidase IV (E.C. 3.5.4.4) from prostasomes to sperm, FEBS Lett., 410: 343–346, 1997. [DOI] [PubMed] [Google Scholar]
  • 50. Arienti G., Carlini E., Saccardi C., Palmerini C.A., Interactions between prostasomes and leukocytes, Biochim. Biophys. Acta, 1425: 36–40, 1998. [DOI] [PubMed] [Google Scholar]
  • 51. Stegmayr B., Berggren P.O., Ronquist G., Hellman B., Calcium, magnesium and zinc contents in organelles of prostatic origin in human seminal plasma, Scand. J. Urol. Nephrol., 16: 199–203, 1982. [DOI] [PubMed] [Google Scholar]
  • 52. Suarez S.S., Hyperactivated motility in sperm, J. Androl., 17: 331–335, 1996. [PubMed] [Google Scholar]
  • 53. Ahmad K., Bracho G.E., Wolf D.P., Tash J.S., Regulation of human sperm motility and hyperactivation components by calcium, calmodulin and protein phosphatases, Arch. Androl., 35: 187–208, 1995. [DOI] [PubMed] [Google Scholar]
  • 54. Suarez S.S., Dai X., Intracellular calcium reaches different levels of elevation in hyperactivated and acrosome‐reacted hamster sperm, Mol. Reprod. Develop., 42: 325–333, 1995. [DOI] [PubMed] [Google Scholar]
  • 55. Palmerini C.A., Carlini E., Nicolucci A., Arienti G., Increase of human spermatozoa intracellular Ca2+ concentration after fusion with prostasomes. Cell Calcium 25: 291–296, 1999. [DOI] [PubMed] [Google Scholar]
  • 56. Cross N.L., Human seminal plasma prevents sperm from becoming acrosomally reactive to the agonist progesterone: cholesterol is the major inhibitor. Biol. Reprod. 54: 138–145, 1996. [DOI] [PubMed] [Google Scholar]
  • 57. Cross N.L., Mahasreshti P., Prostasome fraction of human seminal plasma prevents sperm from becoming acrosomally responsive to the agonist progesterone. Arch. Androl. 39: 39–44, 1997. [DOI] [PubMed] [Google Scholar]
  • 58. Cross N.L., Razy‐Faulkner P., Control of human sperm intracellular pH by cholesterol and its relationship to the response of the acrosome to progesterone. Biol. Reprod., 56: 1169–1174, 1997. [DOI] [PubMed] [Google Scholar]
  • 59. Cross N.L., Sphingomyelin modulates capacitation of human sperm in vitro. Biol. Reprod. 63: 1129–1134, 2000. [DOI] [PubMed] [Google Scholar]
  • 60. Snell W.J., White J.M., The molecules of mammalian fertilization, Am. J. Reprod. Immunol., 28: 97–103, 1996. [DOI] [PubMed] [Google Scholar]
  • 61. Davis B.K., Timing of fertilization in mammals: sperm cholesterol/phospholipid ratio as a determinant of the capacitation interval, Proc. Natl. Acad. Sci. USA, 78: 7560–7564, 1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62. Osheroff J.E., Visconti P.E., Valenzuela J.P., Travis A.J., Alvarez J., Kopf G.S., Regulation of human sperm capacitation by a cholesterol efflux‐ stimulated signal transduction pathway leading to protein kinase A‐ mediated up‐regulation of protein tyrosine phosphorylation. Mol. Hum. Reprod., 5: 1017–1026, 1999. [DOI] [PubMed] [Google Scholar]
  • 63. Khorasani A.M., Cheung A.P., Lee C.Y., Cholesterol inhibitory effects on human sperm‐induced acrosome reaction. J. Androl., 21: 586–594, 2000. [PubMed] [Google Scholar]
  • 64. Calogero A.E., Burrello N., Barone N., Palermo I., Grasso U., D'Agata R., Effects of progesterone on sperm function: mechanisms of action, Hum. Reprod., 15 Suppl 1: 28–45, 2000. [DOI] [PubMed] [Google Scholar]
  • 65. Baldi E., Luconi M., Bonaccorsi L., Maggi M., Francavilla S., Gabriele A., Properzi G., Forti G., Nongenomic progesterone receptor on human spermatozoa: biochemical aspects and clinical implications, Steroids, 64: 143–148, 1999. [DOI] [PubMed] [Google Scholar]
  • 66. Patrat C., Serres C., Jouannet P., The acrosome reaction in human spermatozoa. Biol. Cell 92: 255–266, 2000. [DOI] [PubMed] [Google Scholar]
  • 67. Kirkman‐Brown J.C., Bray C., Stewart P.M., Barratt C.L.R., Publicover S.J., Biphasic elevation of [Ca2+]i in individual human spermatozoa exposed to progesterone, Develop. Biol., 222: 326–335, 2000. [DOI] [PubMed] [Google Scholar]
  • 68. Kirkman‐Brown J.C., Barratt C.L., Publicover S.J., Nifedipine reveals the existence of two discrete components of the progesterone‐induced [Ca2+]i transient in human spermatozoa, Dev. Biol., 259: 71–82, 2003. [DOI] [PubMed] [Google Scholar]
  • 69. Arienti G., Nicolucci A., Santi F., Carlini E., Palmerini C.A., Progesterone‐induced increase of sperm cytosolic calcium is enhanced by previous fusion of spermatozoa to prostasomes, Cell Calcium, 30: 222–227, 2001. [DOI] [PubMed] [Google Scholar]
  • 70. Palmerini C.A., Saccardi C., Carlini E., Fabiani R., Arienti G., Fusion of prostasomes to human spermatozoa stimulates the acrosome reaction, Fertil. Steril., 80: in press, 2003. [DOI] [PubMed] [Google Scholar]
  • 71. Sirivaidyapong S., Bevers M.M., Gadella B.M., Colenbrander B., Induction of the acrosome reaction in dog sperm cells is dependent on epidymal maturation: the generation of a functional progesterone receptor is involved, Mol. Reprod. Dev., 58: 451–459, 2001. [DOI] [PubMed] [Google Scholar]
  • 72. Kuroda Y., Kaneko S., Yoshimura Y., Nozawa S., Mikoshiba K., Influence of progesterone and GABAA receptors on calcium mobilization during human sperm acrosome reaction. Arch. Androl., 42: 185–191, 1999. [DOI] [PubMed] [Google Scholar]
  • 73. Mendoza C., Carreras A., Moos J., Tesarik J., Distinction between true acrosomal reaction and degenerative acrosome loss by one‐step staining method using pisum sativum agglutinin, J. Reprod. Fertil., 95: 763, 1992. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Cellular and Molecular Medicine are provided here courtesy of Blackwell Publishing

RESOURCES