Storage temperature of boar semen and its relationship to changes in sperm plasma membrane integrity, mitochondrial membrane potential, and oxidoreductive capability

The aim of this study was to analyze changes in sperm plasma membrane integrity, mitochondrial activity, and extracellular environment during storage of boar semen at 5 °C, 16 °C, and 25 °C for 10 days. Progressive sperm motility, plasma membrane integrity (SYBR-14/PI-test and HOS test), aspartate aminotransferase (AAT), and mitochondrial activity (JC-1-test and NADH-dependent NBT assay), as well as pH and osmolality were assessed in nine ejaculates of Polish Landrace boars. The plasma membrane integrity of the semen stored at 5 °C was similar to that of the semen stored at 16 °C and 25 °C; however, an increase in AAT activity of the semen stored at 5 °C revealed sperm membrane disorders as early as day 2. Significant differences in the progressive motility of the semen stored at 5 °C and 16 °C were observed at each of the evaluation times. This reduced motility was consistent with decreased sperm mitochondrial transmembrane potential and oxidoreductive capability. We inferred that the cooling of boar semen to 5 °C increases the permeability of the sperm plasma membrane, which may not be revealed by SYBR-14/PI staining or HOS testing. The loss of boar sperm motility that occurs during hypothermic liquid preservation may be connected with alterations in the plasma membrane stability and disorders of mitochondrial transmembrane potential and oxidoreductive capability.

Storage temperature of boar semen and its relationship to changes in sperm plasma membrane integrity, mitochondrial membrane potential, and oxidoreductive capability

The aim of this study was to analyze changes in sperm plasma membrane integrity, mitochondrial activity, and extracellular environment during storage of boar semen at 5 °C, 16 °C, and 25 °C for 10 days. Progressive sperm motility, plasma membrane integrity (SYBR-14/PI-test and HOS test), aspartate aminotransferase (AAT), and mitochondrial activity (JC-1-test and NADH-dependent NBT assay), as well as pH and osmolality were assessed in nine ejaculates of Polish Landrace boars. The plasma membrane integrity of the semen stored at 5 °C was similar to that of the semen stored at 16 °C and 25 °C; however, an increase in AAT activity of the semen stored at 5 °C revealed sperm membrane disorders as early as day 2. Significant differences in the progressive motility of the semen stored at 5 °C and 16 °C were observed at each of the evaluation times. This reduced motility was consistent with decreased sperm mitochondrial transmembrane potential and oxidoreductive capability. We inferred that the cooling of boar semen to 5 °C increases the permeability of the sperm plasma membrane, which may not be revealed by SYBR-14/PI staining or HOS testing. The loss of boar sperm motility that occurs during hypothermic liquid preservation may be connected with alterations in the plasma membrane stability and disorders of mitochondrial transmembrane potential and oxidoreductive capability.

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  • Aitken RJ (2006). Sperm function tests and fertility. Int J Androl 29: 69–75.
  • Althouse GC, Wilson ME, Kuster C, Parsley M (1998). Characterization of lower temperature storage limitations of fresh-extended porcine semen. Theriogenology 50: 535–543.
  • Amaral A, Lourenço B, Marques M, Ramalho-Santos J (2013). Mitochondria functionality and sperm quality. Reproduction 146: R163–R174.
  • Awda BJ, Mackenzie-Bell M, Buhr MM (2009). Reactive oxygen species and boar sperm function. Biol Reprod 81: 553–561.
  • Bailey JL, Buhr MM (1995). Regulation of internal Ca2+ by chilled bull and boar spermatozoa. Cryobiology 32: 259–269.
  • Bailey JL, Lessard C, Jacques J, Breque C, Dobrinski I, Zeng W, Galantino-Homer HL (2008). Cryopreservation of boar semen and its future importance to the industry. Theriogenology 70: 1251–1259.
  • Brouwers JF, Silva PFN, Gadella BM (2005). New assays for detection and localization of endogenous lipid peroxidation products in living boar sperm after BTS dilution or after freeze-thawing. Theriogenology 63: 458–469.
  • Canvin AT, Buhr MM (1989). Effect of temperature on the fluidity of boar sperm membranes. J Reprod Fertil 85: 553–540.
  • Casas I, Althouse GC (2013). The protective effect of a 17 °C holding time on boar sperm plasma membrane fluidity after exposure to 5 °C. Cryobiology 66: 69–75.
  • Ciereszko A, Glogowski J, Demianowicz W, Strzeżek J (1994). Stimulation of aspartate aminotransferase from farm animal semen by pyridoxal 5’-phosphate. Anim Reprod Sci 34: 327– 341.
  • Costello S, Michelangeli F, Nash K, Lefievre L, Morris J, Machado- Oliveira G, Barratt C, Kirkman-Brown J, Publicover S (2009). Ca2+-stores in sperm: their identities and functions. Reproduction 138: 425–437.
  • Drobnis EZ, Crowe LM, Berger T, Anchordoguy TJ, Overstreet JW, Crowe JH (1993). Cold shock damage is due to lipid phase transitions in cell membranes: a demonstration using sperm as a model. J Exp Zool 265: 432–437.
  • Dziekońska A, Fraser L, Majewska A, Lecewicz M, Zasiadczyk Ł, Kordan W (2013). Effect of commercial long-term extenders on metabolic activity and membrane integrity of boar spermatozoa stored at 17 °C. Pol J Vet Sci 16: 517–525.
  • Dziekońska A, Fraser L, Strzeżek J (2009). Effect of different storage temperatures on the metabolic activity of spermatozoa following liquid storage of boar semen. J Anim Feed Sci 18: 638–649.
  • Dziekońska A, Strzeżek J (2011). Boar variability affects sperm metabolism activity in liquid stored semen at 5 °C. Pol J Vet Sci 14: 21–27.
  • Fantinati P, Zannoni A, Bernardini C, Forni M, Tattini A, Seren E, Bacci ML (2009). Evaluation of swine fertilisation medium (SFM) efficiency in preserving spermatozoa quality during long-term storage in comparison to four commercial swine extenders. Animal 3: 269–274.
  • Flores E, Fernández-Novell JM, Peña A, Rodríguez-Gil JE (2009). The degree of resistance to freezing-thawing is related to specific changes in the structures of motile sperm subpopulations and mitochondrial activity in boar spermatozoa. Theriogenology 72: 784–797.
  • Fraczek M, Piasecka M, Gaczarzewicz D, Szumala-Kakol A, Kazienko A, Lenart S, Laszczynska M, Kurpisz M (2012). Membrane stability and mitochondrial activity of human ejaculated spermatozoa during in vitro experimental infection with Escherichia coli, Staphylococcus haemolyticus and Bacteroides ureolyticus. Andrologia 44: 315–329.
  • Funahashi H, Sano T (2005). Select antioxidants improve the function of extended boar semen stored at 10 °C. Theriogenology 63: 1605–1616.
  • Gączarzewicz D, Piasecka M, Udała J, Błaszczyk B, Laszczyńska M, Kram A (2003). Oxidoreductive capability of boar sperm mitochondria in fresh semen and during their preservation in BTS extender. Reprod Biol 3: 161–172.
  • Gączarzewicz D, Piasecka M, Udała J, Błaszczyk B, Stankiewicz T, Laszczyńska M (2010). Plasma membrane changes during the liquid storage of boar spermatozoa: a comparison of methods. Acta Vet Hung 58: 105–116.
  • Gadella BM, Luna C (2014). Cell biology and functional dynamics of the mammalian sperm surface. Theriogenology 81: 74–84.
  • Garcia JC, Dominguez JC, Pena FJ, Alegre B, Gonzalez R, Castro MJ, Habing GG, Kirkwood RN (2010). Thawing boar semen in the presence of seminal plasma: effects on sperm quality and fertility. Anim Reprod Sci 119: 160–165.
  • Golas A, Malek P, Piasecka M, Styrna J (2010). Sperm mitochondria diaphorase activity: a gene mapping study of recombinant inbred strains of mice. Int J Dev Biol 54: 667–673.
  • Großfeld R, Sieg B, Struckmann C, Frenzel A, Maxwell WMC, Rath D (2008). New aspects of boar semen freezing strategies. Theriogenology 70: 1225–1233.
  • Guthrie HD, Welch GR (2012). Effects of reactive oxygen species on sperm function. Theriogenology 78: 1700–1708.
  • Guthrie HD, Welch GR, Long JA (2008). Mitochondrial function and reactive oxygen species action in relation to boar motility. Theriogenology 70: 1209–1215.
  • Huo LJ, Yue KZ, Yang ZM (2002). Characterization of viability, mitochondrial activity, acrosomal integrity and capacitation status in boar sperm during in vitro storage at different ambient temperatures. Reprod Fert Develop 14: 509–514.
  • Hurtado de Llera A, Martin-Hidalgo D, Gil MC, Garcia-Marin LJ, Bragado MJ (2012). AMP-activated kinase AMPK is expressed in boar spermatozoa and regulates motility. PLoS ONE 7: e38840.
  • Johnson LA, Weitze KF, Fiser P, Maxwell WMC (2000). Storage of boar semen. Anim Reprod Sci 62: 143–172.
  • Kim JC, Li Y, Lee S, Yi YJ, Park CS, Woo SH (2008). Effects of cryopreservation on Ca2+ signals induced by membrane depolarization, caffeine, thapsigargin and progesterone in boar spermatozoa. Mol Cells 26: 558–565.
  • Kim S, Lee YJ, Kim YJ (2011). Changes in sperm membrane and ROS following cryopreservation of liquid boar semen stored at 15 °C. Anim Reprod Sci 124: 118–124.
  • Koppers AJ, De Iuliis GN, Finnie JM, McLaughlin EA, Aitken RJ (2008). Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. J Clin Endocr Metab 93: 3199–3207.
  • Kumaresan A, Kadirvel G, Bujarbaruah KM, Bardoloi RK, Das A, Kumar S, Naskar S (2009). Preservation of boar semen at 18 °C induces lipid peroxidation and apoptosis like changes in spermatozoa. Anim Reprod Sci 110: 162–171.
  • López Rodrigeuz A, Rijsselaere T, Vyt P, Van Soom A, Maes D (2012). Effect of dilution temperature on boar semen quality. Reprod Domest Anim 66: e63–e66.
  • Lydka M, Piasecka M, Gaczarzewicz D, Koziorowski M, Bilinska B (2012). Administration of flutamide alters sperm ultrastructure, sperm plasma membrane integrity and its stability, and sperm mitochondrial oxidative capability in the boar: in vivo and in vitro approach. Reprod Domest Anim 47: 635–643.
  • Martín-Hidalgo D, Barón FJ, Bragado MJ, Carmona P, Robina A, García-Marín LJ, Gil MC (2011). The effect of melatonin on the quality of extended boar semen after long-term storage at 17 °C. Theriogenology 75: 1550–1560.
  • Martín-Hidalgo D, Barón FJ, Robina A, Bragado MJ, Hurtado de Llera A, García-Marín LJ, Gil MC (2013a). Inter- and intra- breed comparative study of sperm motility and viability in Iberian and Duroc boar semen during long-term storage in MR-A and XCell extenders. Anim Reprod Sci 139: 109–114.
  • Martín-Hidalgo D, Hurtado de Llera A, Yeste M, Gil MC, Bragado MJ, García-Marín LJ (2013b). Adenosine monophosphate- activated kinase, AMPK, is involved in the maintenance of the quality of extended boar semen during long-term storage. Theriogenology 80: 285–294.
  • Medrano A, Peña A, Rigau T, Rodríguez-Gil JE (2005). Variations in the proportion of glycolytic/non-glycolytic energy substrates modulate sperm membrane integrity and function in diluted boar samples stored at 15–17 °C. Reprod Domest Anim 40: 448–453.
  • Namula Z, Sato Y, Kodama R, Morinaga K, Luu VV, Taniguchi M, Nakai M, Tanihara F, Kikuchi K, Nagai T, Otoi T (2013). Motility and fertility of boar semen after liquid preservation at 5 °C for more than 2 weeks. Anim Sci J 84: 600–606.
  • Paulenz H, Kommisrud E, Hofmo PO (2000). Effect of long-term storage at different temperatures on the quality of liquid boar semen. Reprod Domest Anim 35: 83–87.
  • Peña FJ, Rodríguez Martínez H, Tapia JA, Ortega Ferrusola C, González Fernández L, Macías García B (2009). Mitochondria in mammalian sperm physiology and pathology: a review. Reprod Domest Anim 44: 345–349.
  • Pérez-Llano B, Enciso M, García-Casado P, Sala R, Gosálvez J (2006). Sperm DNA fragmentation in boars is delayed or abolished by using sperm extenders. Theriogenology 66: 2137–2143.
  • Petrunkina AM, Volker G, Weitze KF, Beyerbach M, Töpfer-Petersen E, Waberski D (2005). Detection of cooling-induced membrane changes in the response of boar sperm to capacitating conditions. Theriogenology 63: 2278–2299.
  • Piasecka M, Wenda-Różewicka L, Ogoński T (2001). Computerized analysis of cytochemical reactions for dehydrogenases and oxygraphic studies as methods to evaluate the function of the mitochondrial sheath in rat spermatozoa. Andrologia 33: 1–12.
  • Piomboni P, Focarelli R, Stendardi A, Ferramosca A, Zara V (2012). The role of mitochondria in energy production for human sperm motility. Int J Androl 35: 109–124.
  • Purdy PH, Tharp N, Stewart T, Spiller SF, Blackburn HD (2010). Implications of the pH and temperature of diluted, cooled boar semen on fresh and frozen-thawed sperm motility characteristics. Theriogenology 74: 1304–1310.
  • Ramió-Lluch L, Fernández-Novell JM, Peña A, Bucci D, Rigau T, Rodríguez-Gil JE (2012). “In vitro” capacitation and subsequent acrosome reaction are related to changes in the expression and location of midpiece actin and mitofusin-2 in boar spermatozoa. Theriogenology 77: 979–988.
  • Rodriguez-Gil JE (2006). Mammalian sperm energy resources management and survival during conservation in refrigeration. Reprod Domest Anim 41: 11–20.
  • Schmid S, Henning H, Oldenhof H, Wolkers WF, Petrunkina AM, Waberski D (2013). The specific response to capacitating stimuli is a sensitive indicator of chilling injury in hypothermically stored boar spermatozoa. Andrology 1: 376–386.
  • Schulze M, Henning H, Rüdiger K, Wallner U, Waberski D (2013). Temperature management during semen processing: Impact on boar sperm quality under laboratory and field conditions. Theriogenology 80: 990–998.
  • Storey BT (2008). Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol 52: 427–437.
  • Strzeżek J (2002). Secretory activity of boar seminal vesicle glands. Reprod Biol 2: 243–266.
  • Trzcińska M, Bryła M, Smorąg Z (2011). Apoptotic-like changes in the spermatozoa of fresh and stored boar semen and the quality of embryos produced in vivo. Anim Reprod Sci 124: 90–97.
  • Vadzyuk O, Kosterin S (2015). Diazoxide attenuates ROS generation and exerts cytoprotection under conditions of ROS overproduction in rat uterus cells. Turk J Biol 39: doi: 10.3906/ biy-1410-75.
  • Vyt P, Maes D, Dejonckheere E, Castryck F, Van Soom A (2004). Comparative study on five different commercial extenders for boar semen. Reprod Domest Anim 39: 8–12.
  • Vyt P, Maes D, Sys SU, Rijsselaere T, Van Soom A (2007). Air contact influences the pH of extended porcine semen. Reprod Domest Anim 42: 218–220.
  • Waberski D, Henning H, Petrunkina AM (2011). Assessment of storage effects in liquid preserved boar semen. Reprod Domest Anim 46: 45–48.
  • Zou CX, Yang ZM (2000). Evaluation on sperm quality of freshly ejaculated boar semen during in vitro storage under different temperatures. Theriogenology 53: 1477–1488.
Turkish Journal of Biology-Cover
  • ISSN: 1300-0152
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK
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