Low Density Lipoprotein - important player in increasing cryoprotective efficiency of soybean lecithin-based bull semen extenders
Šimoník Ondřej, Šichtař Jiří, Beran Jan, Maňásková-Postlerová Pavla, Tůmová Lucie, Martina Doležalová, Folková Petra, Stádník Luděk, Rajmon Radko
Abstract
Currently, considering cryopreservation of bull semen, there is no clear consensus over the comparability of cryoprotective efficacy of extenders with soybean lecithin and those based on egg yolk. The objective of this study was to prove the use of Low Density Lipoprotein (LDL) extracted from hen-egg yolk as an enhancing factor for soybean lecithin-based extenders. In total, 35 ejaculates of (seven bulls x five ejaculates per bull) were collected and cryopreserved at a commercial insemination centre. The effect of the LDL addition to the extenders AndroMed® and Bioxcell® was tested in a 6% (v/v) concentration on spermatozoa after thawing. Modified extender composition effects were assessed on sperm functional parameters motility, plasma membrane, mitochondrial membrane potential and acrosomal integrity after thawing by CASA, flow cytometry and fluorescent microscopy, respectively. Based on kinematic parameters determined from CASA, k-means cluster analysis was used to classify individual spermatozoon into specific subpopulations (fast, medium fast and slow). A subpopulation of fast spermatozoa was increased in the presence of LDL in both selected extenders (P < 0.05). Moreover, the positive effect of LDL on sperm motility was confirmed by decreasing the percentage of sperm in slow subpopulation (P < 0.05). The effect of LDL addition on the incidence of spermatozoa with intact plasma membrane was not demonstrated in any case of extender used (P > 0.05). The percentage of sperm with intact acrosome was improved when LDL was added to Bioxcell® extender (P < 0.05). On the other hand, addition of LDL to AndroMed® extender improved mitochondrial intactness after thawing (P < 0.05). In conclusion, our results showed that adding LDL to selected soybean lecithin-based extenders considerably ameliorated the functional parameters of spermatozoa after thawing and thus this lipoprotein could represent an improving agent for soybean lecithin-based extender for bull semen cryopreservation.
Keywords
References
Aires VA, Hinsch KD, Mueller-Schloesser F, Bogner K, Mueller-Schloesser S, Hinsch E. 2003. In vitro and in vivo comparison of egg yolk-based and soybean lecithin-based extenders for cryopreservation of bovine semen. Theriogenology, 60:269-279.
Alvarez-Rodriguez M, Alvarez M, Anel-Lopez L, Martinez-Rodriguez C, Martinez-Pastor F, Borragan S, Anel L de Paz P. 2013. The antioxidant effects of soybean lecithin- or low-density lipoprotein-based extenders for the cryopreservation of brown-bear (Ursus arctos) spermatozoa. Reprod Fert Dev, 25:1185-1193.
Amaral A, Lourenco B, Marques M, Ramalho-Santos J. 2013. Mitochondria functionality and sperm quality. Reproduction, 146:R163-R174.
Amirat L, Tainturier D, Jeanneau L, Thorin C, Gerard O, Courtens JL, Anton M. 2004. Bull semen in vitro fertility after cryopreservation using egg yolk LDL: a comparison with Optidyl (R), a commercial egg yolk extender. Theriogenology, 61:895-907.
Amirat L, Anton M, Tainturier D, Chatagnon G, Battut I, Courtens JL. 2005. Modifications of bull spermatozoa induced by three extenders: Biociphos, low density lipoprotein and Triladyl, before, during and after freezing and thawing. Reproduction, 129:535-543.
Ansari MS, Rakha BA, Andrabi SMH, Akhter S. 2010. Usefulness of powdered and fresh egg yolk for cryopreservation of Zebu bull spermatozoa. Reprod Biol, 10:235-240.
Anton M, Martinet V, Dalgalarrondo M, Beaurnal V, David-Briand E, Rabesona H. 2003. Chemical and structural characterisation of low-density lipoproteins purified from hen egg yolk. Food Chem, 83:175-183.
Beran J, Simonik O, Stadnik L, Rajmon R, Jaromir D, Krejcarkova A, Dolezalova M, Sichtar J. 2013. Effect of bull, diluter and LDL-cholesterol concentration on spermatozoa resistance against cold shock. Acta Univ Agric Silvic Mendelianae Brun, 61:1575-1581.
Beran J, Simonik O, Rajmon R, Stadnik L, Dolezalova M, Krejcarkova A, Duchacek J, Sichtar J. 2016. Effect of LDL addition into selected bull sperm diluters on resistance of spermatozoa against cold shock. Acta Univ Agric Silvic Mendelianae Brun, 64:395-399.
Bergeron A, Crete MH, Brindle Y, Manjunath P. 2004. Low-density lipoprotein fraction from hen's egg yolk decreases the binding of the major proteins of bovine seminal plasma to sperm and prevents lipid efflux from the sperm membrane. Biol Reprod, 70:708-717.
Bousseau S, Brillard JP, Marquant-Le Guienne B, Guerin B, Camus A, Lechat M. 1998. Theriogenology, 50:699-706.
Breitbart H, Cohen G, Rubinstein S. 2005. Role of actin cytoskeleton in mammalian sperm capacitation and the acrosome reaction. Reproduction, 129:263-268.
Crespilho AM, Sa Filho MF, Dell'Aqua JA Jr, Nichi M, Monteiro GA, Avanzi BR, Martins A, Papa FO. 2012. Comparison of in vitro and in vivo fertilizing potential of bovine semen frozen in egg yolk or new lecithin based extenders. Livestock Sci, 149:1-6.
Faezah SS, Zuraina FM, Farah JH, Khairul O, Hilwani NI, Iswadi MI, Fang CN, Zawawi I, Abas OM, Fatimah SI. 2014. The effects of magnetic separation on cryopreserved bovine spermatozoa motility, viability and cryo-capacitation status. Zygote, 22(3):378-386.
Ferraz M, Morato R, Yeste M, Arcarons N, Pena AI, Tamargo C, Hidalgo CO, Muino R, Mogas T. 2014. Evaluation of sperm subpopulation structure in relation to in vitro sperm-oocyte interaction of frozen-thawed semen from Holstein bulls. Theriogenology, 81:1067-1072.
Ferrusola CO, Fernandez LG, Morrell JM, Sandoval CS, Garcia BM, Rodriguez-Martinez H, Tapia JA, Pena FJ. 2009. Lipid Peroxidation, Assessed with BODIPY-C11, Increases after Cryopreservation of Stallion Spermatozoa, is Stallion-dependent and is Related to Apoptotic-like Changes. Reprod Domest Anim, 44:88-88.
Futino DO, Mendes MCB, Matos WNL, Mondadori RG, Lucci CM. 2010. Glycerol, Methyl-Formamide and Dimethyl-Formamide in Canine Semen Cryopreservation. Reprod Domest Anim, 45:214-220.
Gharagozloo P, Aitken RJ. 2011. The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy. H Reprod, 26:1628-1640.
Gil J, Januskauskas A, Haard MC, Haard MGM, Johanisson A, Soderquist L, Rodriguez-Martinez H. 2000. Functional sperm parameters and fertility of bull semen extended in biociphos-Plus (R) and Triladyl (R). Reprod Domest Anim, 35:69-77.
Hevonoja T, Pentikainen MO, Hyvonen MT, Kovanen PT, Ala-Korpela M. 2000. Structure of low density lipoprotein (LDL) particles: Basis for
understanding molecular changes in modified LDL. Biochimica Et Biophysica Acta-Molecular and Cell Biology of Lipids, 1488:189-210.
Holt WV. 2000. Basic aspects of frozen storage of semen. Anim Reprod Sci, 62:3-22.
Holt WV,Van Look KJW. 2004. Concepts in sperm heterogeneity, sperm selection and sperm competition as biological foundations for laboratory tests of semen quality. Reproduction, 127:527-535.
Horokhovatskyi Y, Sampels S, Cosson J, Linhart O, Rodina M, Fedorov P, Blecha M, Dzyuba B. 2016. Lipid composition in common carp (Cyprinus carpio) sperm possessing different cryoresistance. Cryobiology, 73:282-285.
Hu JH, Li QW, Zan LS, Jiang ZL, An JH, Wang LQ, Jia YH. 2010. The cryoprotective effect of low-density lipoproteins in extenders on bull spermatozoa following freezing-thawing. Anim Reprod Sci, 117:11-17.
Hu JH, Jiang ZL, Lv RK, Li QW, Zhang SS, Zan LS, Li YK, Li X. 2011. The advantages of low-density lipoproteins in the cryopreservation of bull semen. Cryobiology, 62:83-87.
Jankovicova J, Frolikova M, Sebkova N, Simon M, Cupperova P, Lipcseyova D, Michalkova K, Horovska L, Sedlacek R, Stopka P, Antalikova J, Dvorakova-Hortova K. 2016. Characterization of tetraspanin protein CD81 in mouse spermatozoa and bovine gametes. Reproduction, 152:785-793.
Layek SS, Mohanty TK, Kumaresan A, Parks JE. 2016. Cryopreservation of bull semen: Evolution from egg yolk based to soybean based extenders. Anim Reprod Sci, 172:1-9.
Lusignan MF, Bergeron A, Lafleur M, Manjunath P. 2011. The Major Proteins of Bovine Seminal Plasma Interact with Caseins and Whey Proteins of Milk Extender. Biol Reprod, 85:457-464.
Manjunath P, Nauc V, Bergeron A, Menard M. 2002. Major proteins of bovine seminal plasma bind to the low-density lipoprotein fraction of hen's egg yolk. Biol Reprod, 67:1250-1258.
Martinet V, Saulnier P, Beaumal V, Courthaudon JL, Anton M. 2003. Surface properties of hen egg yolk low-density lipoproteins spread at the air-water interface. Coll Surf B-Biointer, 31:185-194.
Martinez-Pastor F, Jorge Tizado E, Julian Garde J, Anel L, de Paz P. 2011. Statistical Series: Opportunities and challenges of sperm motility subpopulation analysis. Theriogenology, 75:783-795.
Morris GJ, Acton E, Murray BJ, Fonseca F. 2012. Freezing injury: The special case of the sperm cell. Cryobiology, 64(2):71-80.
Moussa M, Martinet V, Trimeche A, Tainturier D, Anton M. 2002. Low density lipoproteins extracted from hen egg yolk by an easy method: cryoprotective effect on frozen-thawed bull semen. Theriogenology, 57:1695-1706.
Muino R, Tamargo C, Hidalgo CO, Pena AI. 2008. Identification of sperm subpopulations with defined motility characteristics in ejaculates from Holstein bulls: Effects of cryopreservation and between-bull variation. Anim Reprod Sci, 109:27-39.
Murphy E M, Murphy C, O'Meara C, Dunne G, Eivers B, Lonergan P, Fair S. 2017. A comparison of semen diluents on the in vitro and in vivo fertility of liquid bull semen. J Dairy Sci, 100:1541-1554.
Oldenhof H, Heutelbeck A, Blasse AK, Bollwein H, Martinsson G, Wolkers WF,Sieme H. 2015. Tolerance of spermatozoa to hypotonic stress: role of membrane fluidity and correlation with cryosurvival. Reprod Fert Dev, 27:285-293.
Pace MM, Graham EF. 1974. Components in egg-yolk which protect bovine spermatozoa during freezing. J Anim Sci, 39:1144-1149.
Parrish JJ, Suskoparrish J, Winer MA, First NL. 1988. Capacitation of bovine sperm by heparin. Biol Reprod, 38:1171-1180.
Perumal P, Srivastava SK, Ghosh SK, Baruah KK, Bag S, Rajoria JS, Kumar K, Rajkhowa C, Pande M, Srivastava N. 2016. Effects of low-density lipoproteins as additive on quality parameters and oxidative stress following cryopreservation of mithun (Bos frontalis) spermatozoa. Reprod Domest Anim, 51:708-716.
Petrunkina AM, Waberski D, Bollwein H, Sieme H. 2010. Identifying non-sperm particles during flow cytometric analysis: a simple approach. Reprod Domest Anim, 45:39-39.
Polge C, Rowson LEA. 1952. Fertilizing capacity of bull spermatozoa after freezing at -79 degrees. Nature, 169:626-627.
Roca J, Parrilla I, Gil MA, Cuello C, Martinez EA,Rodriguez-Martinez H. 2016. Non-viable sperm in the ejaculate: Lethal escorts for Contemporary viable sperm. Anim Reprod Sci, 169:24-31.
Sichtar J, Nehasilova A, Simonik O, Bubenickova F. 2017. Effect of Two Freezing Extenders on Characteristic of Fresh and Frozen-Thawed Semen in Endangered Old Kladruber Stallions - A Pilot Study. Czech J Anim Sci, 62:227-233.
Sieme H, Harrison RAP, Petrunkina AM. 2008. Cryobiological determinants of frozen semen quality, with special reference to stallion. Anim Reprod Sci, 107:276-292.
Simonik O, Rajmon R, Stadnik L, Sichtar J, Beran J, Duchacek J, Hodek P,Trefil P. 2016. Effect of low-density lipoprotein addition to soybean lecithin-based extenders on bull spermatozoa following freezing-thawing - preliminary results. Czech J Anim Sci, 61:560-567.
Srivastava N, Jerome A, Srivastava S K, Ghosh S K, Kumar A. 2013. Bovine seminal PDC-109 protein: An overview of biochemical and functional properties. Anim Reprod Sci, 138:1-13.
Srivastava N, Srivastava SK, Ghosh SK, Singh LP, Prasad JK, Kumar A, Perumal P, Jerome A, Thamizharasan A. 2012. Sequestration of PDC-109 protein improves freezability of crossbred bull spermatozoa. Anim Reprod Sci, 131:54-62.
Stadnik L, Rajmon R, Beran J, Simonik O, Dolezalova M, Sichtar J, Stupka R, Folkova P. 2015. Influence of selected factors on bovine spermatozoa cold shock resistance. Acta Vet Brno, 84:125-131.
Stradaioli G, Noro T, Sylla L, Monaci M. 2007. Decrease in glutathione (GSH) content in bovine sperm
after cryopreservation: Comparison between two extenders. Theriogenology, 67:1249-1255.
Sultan SD, Farag AE. 2010. Perspective on plasma membrane cholesterol efflux and spermatozoal function. J Hum Reprod Sci, 3:68-75.
Tapia JA, Macias-Garcia B, Miro-Moran A, Ortega-Ferrusola C, Salido GM, Pena FJ, Aparicio IM. 2012. The Membrane of the Mammalian Spermatozoa: Much More Than an Inert Envelope. Reprod Domest Anim, 47:65-75.
Thun R, Hurtado M, Janett F. 2002. Comparison of Biociphos-Plus (R) and TRIS-egg yolk extender for cryopreservation of bull semen. Theriogenology, 57:1087-1094.
Travis AJ, Kopf GS. 2002. The role of cholesterol efflux in regulating the fertilization potential of mammalian spermatozoa. J Clin Invet, 110:731-736.
van Wagtendonk-de Leeuw AM, Haring RM, Kaal-Lansbergen L, den Daas JHG. 2000. Fertility results using bovine semen cryopreserved with extenders based on egg yolk and soy bean extract. Theriogenology, 54:57-67.
Verstegen J, Iguer-Ouada M, Onclin K. 2002. Computer assisted semen analyzers in andrology research and veterinary practice. Theriogenology, 57:149-179.
Vidal AH, Batista AM, da Silva ECB, Gomes WA, Pelinca MA, Silva SV, Guerra MMP. 2013. Soybean lecithin-based extender as an alternative for goat sperm cryopreservation. Small Ruminant Res, 109:47-51.
Wakamatu T, Sato Y, Saito Y. 1982. Identification of the components responsible for the gelation of egg-yolk during freezing. Agric Biol Chem, 46:1495-1503.
Yeste M. 2016. Sperm cryopreservation update: Cryodamage, markers, and factors affecting the sperm freezability in pigs. Theriogenology, 85:47-64.
Zhang SS, Hu JH, Li QW, Jiang ZL, Zhang XY. 2009. The cryoprotective effects of soybean lecithin on boar spermatozoa quality. Afr J Biotechnol, 8:6476-6480.
Facebook
Google+
Twitter
LinkedIn
Mendeley
StumbleUpon
CiteULike
Reddit
Email