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Research Article

volume 53 issue 9 (september 2019) : 1167-1171,   Doi: 10.18805/ijar.B-3665

Effects of prostasomes on functional parameters of fresh and cryopreserved-thawed spermatozoa of crossbred Karan Fries (KF) bulls

A
Amit Kumar
S
Sujata Pandita
N
N. Anand Laxmi
M
Mukesh Bhakat
T
T.K. Mohanty
1<div style="text-align: justify;">Department of Animal Physiology, National Dairy Research Institute, Karnal-132001, Haryana, India.</div>
Cite article:- Kumar Amit, Pandita Sujata, Laxmi Anand N., Bhakat Mukesh, Mohanty T.K. (2018). Effects of prostasomes on functional parameters of fresh and cryopreserved-thawed spermatozoa of crossbred Karan Fries (KF) bulls. Indian Journal of Animal Research. 53(9): 1167-1171. doi: 10.18805/ijar.B-3665.

ABSTRACT

Prostasomes are extracellular vesicles that fuse with sperms thereby improving its functional parameters. Present study aimed to isolate and characterise prostasomes from semen of KF bulls, and to investigate prostasomes effects on functional parameters of KF bull spermatozoa. Isolated prostasomes were characterized with respect to the binding of FITC-conjugated CD 26 antibodies, as well as protein, cholesterol and phospholipids content. Subsequently, effects of prostasomes supplementation (1mg/ml) were investigated on ROS production, Ca2+ signalling, mitochondrial membrane potential and acrosome integrity of fresh and cryopreserved-thawed spermatozoa. Isolated prostasomes were immunostained positively. Prostasomes showed higher proportion of both protein and cholesterol as compared to phospholipids. When sperm samples were supplemented with prostasomes, ROS production decreased, while all other functional parameters improved.

REFERENCES

  1. Alvarez, J.G. and Storey, B.T. (1989). Role of glutathione peroxidase in protecting mammalian spermatozoa from loss of motility caused by spontaneous lipid peroxidation. Gamete Res., 23:77–90.
  2. Burden, H.P., Holmes, C.H., Persad, R., Whittington, K. (2006). Prostasomes—their effects on human male reproduction and fertility. Hum. Reprod. Update, 12: 283–292.
  3. Carlsson, L., Ronquist, G., Eliasson, R., Egberg, N., Larsson, A. (2006). Flow cytometric technique for determination of prostasomal quantity, size and expression of CD10, CD13, CD26 and CD59 in human seminal plasma. Int. J. Androl., 29: 331–338. 
  4. Chowdhury, S., Das, S., Gupta, T., Sana, D., Bose, S. (2014). Evaluation of frozen semen by acrosomal integrity and sperm concentration -two vital quality parameters of male fertility in bovines. Explor. Anim. Med. Res., 4(1): 101-107. 
  5. Cross, N.L. and Mahasreshti, P. (1997). Prostasome fraction of human seminal plasma prevents sperm from becoming acrosomally responsive to the agonist progesterone. Arch. Androl., 39: 39–44.
  6. Ek, P., Malm, J., Lilja, H., Carlsson, L., Ronquist, G. (2002). 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. 
  7. Fisher, H.M. and Aitken, R.J. (1997). Comparative analysis of the ability of precursor germ cells and epididymal spermatozoa to generate reactive oxygen metabolites. J. Exp. Zool., 277: 390–400.
  8. González-Cuevas, J., Navarro-Partida, J., Marquez-Aguirre, A.L., Bueno-Topete, M.R., Beas-Zarate, C., Armendáriz-Borunda, J. (2011). Ethylenediaminetetraacetic acid induces antioxidant and anti-inflammatory activities in experimental liver fibrosis. Redox Report, 16(2): 62-70.
  9. Kadirve, G., Kumar, S.,Ghosh, S.K., Perumal, P. (2014). Activity of antioxidative enzymes in fresh and frozen thawed buffalo (Bubalus bubalis) spermatozoa in relation to lipid peroxidation and semen quality. Asian Pac. J. Reprod., 3(3): 210-217. 
  10. Kim, S., Lee, Y.J., Kim, Y.J. (2011). Changes in sperm membrane and ROS following cryopreservation of liquid boar semen stored at 15 °C. Anim. Reprod. Sci., 124(1-2):118-124.
  11. Kravets, F.G., Lee, J., Singh, B., Trocchia, A., Pentyala, S.N., Khan, S.A. (2000). Prostasomes: current concepts. Prostate, 43:169–174. 
  12. Laurell, C.B., Weiber, H., Ohlsson K., Rannevik, G. (1982). A zinc-dependent peptidase in prostatic organelles present in seminal plasma. Clin. Chim. Acta, 126: 161-170.
  13. Mann, T. and Lutwak-Mann, C. (1981). Male reproductive function and semen. In: Physiology, Biochemistry and Investigative Andrology. Springer-Verlag; Berlin, Germany: 495.
  14. Maxwell, W.M.C., de Graaf, S.P., Ghaoui, RE-H., Evans, G. (2007). Seminal plasma effects on sperm handling and female fertility. Soc. Reprod. Fertil. Suppl., 64:13–38.
  15. Minelli, A., Moroni, M., Mart´ýnez, E., Mezzasoma, I., Ronquist, G. (1998). Occurrence of prostasome-like membrane vesicles in equine seminal plasma. J. Reprod. Fertil., 114: 237–243. 
  16. Palmerini, C.A., Carlini, E., Nicolucci, A., Arienti, G. (1999). Increase of human spermatozoa intracellular Ca2+ concentration after fusion with prostasomes. Cell Calcium, 25: 291–296. 
  17. Piehl, L.L., Cisale, H., Torres, N., Capani, F., Sterin-Speziale, N., Hager, A. (2006). Biochemical characterization and membrane fluidity of membranous vesicles isolated from boar seminal plasma. Anim. Reprod. Sci., 92: 401-410. 
  18. Pons-Rejraji, H., Artonne, C., Sion, B., Brugnon, F., Canis, M., Janny, L., Grizard, G. (2011). Prostasomes: inhibitors of capacitation and modulators of cellular signalling in human sperm. Int. J. Androl., 34: 568-580.
  19. Rajoriya, J.S., Prasad, J.K., Ghosh, S.K., Perumal, P., Kumar, A., Kaushal, S., Singh, M. (2013). Effects of seasons on enzymatic changes and cholesterol efflux in relation to freezability in Tharparkar bull semen. Asian Pac. J. Reprod., 2(4): 280 -288.
  20. Ronquist, G. and Brody, I. (1985). The prostasome: its secretion and function in man. Biochim. Biophys. Acta, 822: 203–218.
  21. Ronquist, G. and Hedström, M. (1977). Restoration of detergent-inactivated adenosine triphosphatase activity of human prostatic fluid with concanavalin A. Biochim. Biophys. Acta, 483: 483-486.
  22. Ronquist, K. G., Ek, B., Morrell, J., Stavreus-Evers, A., Holst, B.S., Humblot, P., Ronquist, G., Larsson, A. (2013). Prostasomes from four different species are able to produce extracellular adenosine triphosphate (ATP). Biochim. Biophys. Acta, 1830: 4604–4610. 
  23. Saez, F., Motta, C., Boucher, D., Grizard, G. (1998). Antioxidant capacity of prostasomes in human semen. Mol. Human Rep., 4: 667–672. 
  24. Siciliano, L., Marcianò, V., Carpino, A. (2008). Prostasome-like vesicles stimulate acrosome reaction of pig spermatozoa. Reprod. Biol. Endocrinol., 6: 5.
  25. Suarez, S.S. (2008). Control of hyperactivation in sperm. Hum. Reprod. Update, 14: 647–657.
  26. Wang, J., Lundqvist, M., Carlsson, L., Nilsson, O., Lundkvist, O., Ronquist, G. (2001). Prostasome-like granules from the PC-3 prostate cancer cell line increase the motility of washed human spermatozoa and adhere to the sperm. Eur. J. Obstet. Gynecol. Reprod. Biol., 96(1): 88-97.
  27. White, I.G., Gol, P., Voglmayr, J.K. (1987). Effect of male reproductive tract fluids and proteins on the metabolism and motility of ram spermatozoa. Arch. Androl., 19:115–125. 
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Indian Journal of Animal Research
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    Research Article

    volume 53 issue 9 (september 2019) : 1167-1171,   Doi: 10.18805/ijar.B-3665

    Effects of prostasomes on functional parameters of fresh and cryopreserved-thawed spermatozoa of crossbred Karan Fries (KF) bulls

    A
    Amit Kumar
    S
    Sujata Pandita
    N
    N. Anand Laxmi
    M
    Mukesh Bhakat
    T
    T.K. Mohanty
    1<div style="text-align: justify;">Department of Animal Physiology, National Dairy Research Institute, Karnal-132001, Haryana, India.</div>
    Cite article:- Kumar Amit, Pandita Sujata, Laxmi Anand N., Bhakat Mukesh, Mohanty T.K. (2018). Effects of prostasomes on functional parameters of fresh and cryopreserved-thawed spermatozoa of crossbred Karan Fries (KF) bulls. Indian Journal of Animal Research. 53(9): 1167-1171. doi: 10.18805/ijar.B-3665.

    ABSTRACT

    Prostasomes are extracellular vesicles that fuse with sperms thereby improving its functional parameters. Present study aimed to isolate and characterise prostasomes from semen of KF bulls, and to investigate prostasomes effects on functional parameters of KF bull spermatozoa. Isolated prostasomes were characterized with respect to the binding of FITC-conjugated CD 26 antibodies, as well as protein, cholesterol and phospholipids content. Subsequently, effects of prostasomes supplementation (1mg/ml) were investigated on ROS production, Ca2+ signalling, mitochondrial membrane potential and acrosome integrity of fresh and cryopreserved-thawed spermatozoa. Isolated prostasomes were immunostained positively. Prostasomes showed higher proportion of both protein and cholesterol as compared to phospholipids. When sperm samples were supplemented with prostasomes, ROS production decreased, while all other functional parameters improved.

    REFERENCES

    1. Alvarez, J.G. and Storey, B.T. (1989). Role of glutathione peroxidase in protecting mammalian spermatozoa from loss of motility caused by spontaneous lipid peroxidation. Gamete Res., 23:77–90.
    2. Burden, H.P., Holmes, C.H., Persad, R., Whittington, K. (2006). Prostasomes—their effects on human male reproduction and fertility. Hum. Reprod. Update, 12: 283–292.
    3. Carlsson, L., Ronquist, G., Eliasson, R., Egberg, N., Larsson, A. (2006). Flow cytometric technique for determination of prostasomal quantity, size and expression of CD10, CD13, CD26 and CD59 in human seminal plasma. Int. J. Androl., 29: 331–338. 
    4. Chowdhury, S., Das, S., Gupta, T., Sana, D., Bose, S. (2014). Evaluation of frozen semen by acrosomal integrity and sperm concentration -two vital quality parameters of male fertility in bovines. Explor. Anim. Med. Res., 4(1): 101-107. 
    5. Cross, N.L. and Mahasreshti, P. (1997). Prostasome fraction of human seminal plasma prevents sperm from becoming acrosomally responsive to the agonist progesterone. Arch. Androl., 39: 39–44.
    6. Ek, P., Malm, J., Lilja, H., Carlsson, L., Ronquist, G. (2002). 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. 
    7. Fisher, H.M. and Aitken, R.J. (1997). Comparative analysis of the ability of precursor germ cells and epididymal spermatozoa to generate reactive oxygen metabolites. J. Exp. Zool., 277: 390–400.
    8. González-Cuevas, J., Navarro-Partida, J., Marquez-Aguirre, A.L., Bueno-Topete, M.R., Beas-Zarate, C., Armendáriz-Borunda, J. (2011). Ethylenediaminetetraacetic acid induces antioxidant and anti-inflammatory activities in experimental liver fibrosis. Redox Report, 16(2): 62-70.
    9. Kadirve, G., Kumar, S.,Ghosh, S.K., Perumal, P. (2014). Activity of antioxidative enzymes in fresh and frozen thawed buffalo (Bubalus bubalis) spermatozoa in relation to lipid peroxidation and semen quality. Asian Pac. J. Reprod., 3(3): 210-217. 
    10. Kim, S., Lee, Y.J., Kim, Y.J. (2011). Changes in sperm membrane and ROS following cryopreservation of liquid boar semen stored at 15 °C. Anim. Reprod. Sci., 124(1-2):118-124.
    11. Kravets, F.G., Lee, J., Singh, B., Trocchia, A., Pentyala, S.N., Khan, S.A. (2000). Prostasomes: current concepts. Prostate, 43:169–174. 
    12. Laurell, C.B., Weiber, H., Ohlsson K., Rannevik, G. (1982). A zinc-dependent peptidase in prostatic organelles present in seminal plasma. Clin. Chim. Acta, 126: 161-170.
    13. Mann, T. and Lutwak-Mann, C. (1981). Male reproductive function and semen. In: Physiology, Biochemistry and Investigative Andrology. Springer-Verlag; Berlin, Germany: 495.
    14. Maxwell, W.M.C., de Graaf, S.P., Ghaoui, RE-H., Evans, G. (2007). Seminal plasma effects on sperm handling and female fertility. Soc. Reprod. Fertil. Suppl., 64:13–38.
    15. Minelli, A., Moroni, M., Mart´ýnez, E., Mezzasoma, I., Ronquist, G. (1998). Occurrence of prostasome-like membrane vesicles in equine seminal plasma. J. Reprod. Fertil., 114: 237–243. 
    16. Palmerini, C.A., Carlini, E., Nicolucci, A., Arienti, G. (1999). Increase of human spermatozoa intracellular Ca2+ concentration after fusion with prostasomes. Cell Calcium, 25: 291–296. 
    17. Piehl, L.L., Cisale, H., Torres, N., Capani, F., Sterin-Speziale, N., Hager, A. (2006). Biochemical characterization and membrane fluidity of membranous vesicles isolated from boar seminal plasma. Anim. Reprod. Sci., 92: 401-410. 
    18. Pons-Rejraji, H., Artonne, C., Sion, B., Brugnon, F., Canis, M., Janny, L., Grizard, G. (2011). Prostasomes: inhibitors of capacitation and modulators of cellular signalling in human sperm. Int. J. Androl., 34: 568-580.
    19. Rajoriya, J.S., Prasad, J.K., Ghosh, S.K., Perumal, P., Kumar, A., Kaushal, S., Singh, M. (2013). Effects of seasons on enzymatic changes and cholesterol efflux in relation to freezability in Tharparkar bull semen. Asian Pac. J. Reprod., 2(4): 280 -288.
    20. Ronquist, G. and Brody, I. (1985). The prostasome: its secretion and function in man. Biochim. Biophys. Acta, 822: 203–218.
    21. Ronquist, G. and Hedström, M. (1977). Restoration of detergent-inactivated adenosine triphosphatase activity of human prostatic fluid with concanavalin A. Biochim. Biophys. Acta, 483: 483-486.
    22. Ronquist, K. G., Ek, B., Morrell, J., Stavreus-Evers, A., Holst, B.S., Humblot, P., Ronquist, G., Larsson, A. (2013). Prostasomes from four different species are able to produce extracellular adenosine triphosphate (ATP). Biochim. Biophys. Acta, 1830: 4604–4610. 
    23. Saez, F., Motta, C., Boucher, D., Grizard, G. (1998). Antioxidant capacity of prostasomes in human semen. Mol. Human Rep., 4: 667–672. 
    24. Siciliano, L., Marcianò, V., Carpino, A. (2008). Prostasome-like vesicles stimulate acrosome reaction of pig spermatozoa. Reprod. Biol. Endocrinol., 6: 5.
    25. Suarez, S.S. (2008). Control of hyperactivation in sperm. Hum. Reprod. Update, 14: 647–657.
    26. Wang, J., Lundqvist, M., Carlsson, L., Nilsson, O., Lundkvist, O., Ronquist, G. (2001). Prostasome-like granules from the PC-3 prostate cancer cell line increase the motility of washed human spermatozoa and adhere to the sperm. Eur. J. Obstet. Gynecol. Reprod. Biol., 96(1): 88-97.
    27. White, I.G., Gol, P., Voglmayr, J.K. (1987). Effect of male reproductive tract fluids and proteins on the metabolism and motility of ram spermatozoa. Arch. Androl., 19:115–125. 
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