Improving sperm cryopreservation with antifreeze proteins: Effect on gilthead seabream (Sparus aurata) plasma membrane lipids

Biology of Reproduction

Volumn 86, Issue 2, 2012, Pages

  Beirão, José ^a   Zilli, Loredana ^b   Vilella, Sebastiano ^b   Cabrita, Elsa ^c   Schiavone, Roberta ^b   Herráez, Maria Paz ^a,b  

^a UNIVERSITY OF LEÓN   (Spain)

^b UNIVERSITY OF SALENTO   (Italy)

^c INSTITUTO DE CIENCIAS MARINAS DE ANDALUCÍA   (Spain)

Author keywords

Antifreeze protein; Cryopreservation; Flagella; Gamete biology; Head plasma membrane; Sparus aurata; Sperm

Indexed keywords

ANTIFREEZE PROTEIN; ANTIFREEZE PROTEIN I; ANTIFREEZE PROTEIN III; CHOLESTEROL; DIMETHYL SULFOXIDE; MEMBRANE LIPID; PHOSPHATIDYLSERINE; PHOSPHOLIPID; POLYUNSATURATED FATTY ACID; SATURATED FATTY ACID; UNCLASSIFIED DRUG; CRYOPROTECTIVE AGENT; FATTY ACID; UNSATURATED FATTY ACID;

ACROSOME; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CELL VIABILITY; CONTROLLED STUDY; CORRELATION ANALYSIS; CRYOPRESERVATION; FLAGELLUM; FREEZING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIPID COMPOSITION; MALE; NONHUMAN; PRIORITY JOURNAL; SPARUS AURATA; SPERM PRESERVATION; SPERMATOZOON MEMBRANE; TELEOST; THAWING; ANIMAL; CELL SURVIVAL; DRUG EFFECT; METABOLISM; METHODOLOGY; PERCIFORMES; SPERMATOZOON; SPERMATOZOON TAIL; ULTRASTRUCTURE;

SPARUS AURATA; TELEOSTEI;

ANIMALS; ANTIFREEZE PROTEINS; CELL MEMBRANE; CELL SURVIVAL; CRYOPRESERVATION; CRYOPROTECTIVE AGENTS; DIMETHYL SULFOXIDE; FATTY ACIDS; FATTY ACIDS, UNSATURATED; MALE; MEMBRANE LIPIDS; PERCIFORMES; SEMEN PRESERVATION; SPERM HEAD; SPERM TAIL;

EID: 84860233847     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.093401     Document Type: Article

References (49)

1. Ladha S. Lipid heterogeneity and membrane fluidity in a highly polarized cell, the mammalian spermatozoon. J Membr Biol 1998; 165:1-10.
2. Wassall SR, Stillwell W. Polyunsaturated fatty acid-cholesterol interactions: domain formation in membranes. Biochim Biophys Acta 2009; 1788:24-32.
3. Miller RR, Sheffer CJ, Cornett CL, McClean R, MacCallum C, Johnston SD. Sperm membrane fatty acid composition in the Eastern grey kangaroo (Macropus giganteus), koala (Phascolarctos cinereus), and common wombat (Vombatus ursinus) and its relationship to cold shock injury and cryopreservation success. Cryobiology 2004; 49:137-148.
4. Am-In N, Kirkwood RN, Techakumphu M, Tantasuparuk W. Lipid profiles of sperm and seminal plasma from boars having normal or low sperm motility. Theriogenology 2011; 75:897-903.
5. Aksoy Y, Aksoy H, Altinkaynak K, Aydin HR, Ozkan A. Sperm fatty acid composition in subfertile men. Prostaglandins Leukot Essent Fatty Acids 2006; 75:75-79.
6. Waterhouse KE, Hofmo PO, Tverdal A, Miller RR. Within and between breed differences in freezing tolerance and plasma membrane fatty acid composition of boar sperm. Reproduction 2006; 131:887-894.
7. Pustowka C, McNiven MA, Richardson GF, Lall SP. Source of dietary lipid affects sperm plasma membrane integrity and fertility in rainbow trout Oncorhynchus mykiss (Walbaum) after cryopreservation. Aquacult Res 2000; 31:297-305.
8. Bongalhardo DC, Leeson S, Buhr MM. Dietary lipids differentially affect membranes from different areas of rooster sperm. Poult Sci 2009; 88:1060-1069.
9. LabbéC, Maisse G. Influence of rainbow trout thermal acclimation on sperm cryopreservation: relation to change in the lipid composition of the plasma membrane. Aquaculture 1996; 145:281-294.
10. Chakrabarty J, Banerjee D, Pal D, De J, Ghosh A, Majumder GC. Shedding off specific lipid constituents from sperm cell membrane during cryopreservation. Cryobiology 2007; 54:27-35.
11. Muller K, Muller P, Pincemy G, Kurz A, LabbéC. Characterization of sperm plasma membrane properties after cholesterol modification: consequences for cryopreservation of rainbow trout spermatozoal. Biol Reprod 2008; 78:390-399.
12. Visconti PE, Galantino-Homer H, Ning X, Moore GD, Valenzuela JP, Jorgez CJ, Alvarez JG, Kopf GS. Cholesterol efflux-mediated signal transduction in mammalian sperm: b-cyclodextrins initiate transmembrane signaling leading to an increase in protein tyrosine phosphorylation and capacitation. J Biol Chem 1999; 274:3235-3242.
13. Bell MV, Dick JR, Buda C. Molecular speciation of fish sperm phospholipids: large amounts of dipolyunsaturated phosphatidylserine. Lipids 1997; 32:1085-1091.
14. Bobe J, LabbéC. Egg and sperm quality in fish. Gen Comp Endocrinol 2010; 165:535-548.
15. Tomczak MM, Hincha DK, Estrada SD, Wolkers WF, Crowe LM, Feeney RE, Tablin F, Crowe JH. A mechanism for stabilization of membranes at low temperatures by an antifreeze protein. Biophys J 2002; 82:874-881.
16. Venketesh S, Dayananda C. Properties, potentials, and prospects of antifreeze proteins. Crit Rev Biotechnol 2008; 28:57-82.
17. Inglis SR, Turner JJ, Harding MM. Applications of type I antifreeze proteins: studies with model membranes & cryoprotectant properties. Curr Protein Pept Sci 2006; 7:509-522.
18. Le Francois NR, Lamarre SG, Tveiten H, Blier PU, Bailey J. Sperm cryoconservation in Anarhichas sp., endangered cold-water aquaculture species with internal fertilization. Aquacult Int 2008; 16:273-279.
19. Karanova MV, Tsvetkova LI. Cryoprotective properties of antifreeze glycoproteins upon freezing of fish sperm. Izv Akad Nauk Ser Biol 1994; 5:818-827.
20. Karanova MV, Zsvetkova LI, Petropavlov NN. Effect of antifreeze glycoproteins on quality of cryoconserved carp sperm. Biofizika 1997; 42:725-728.
21. Younis AI, Rooks B, Khan S, Gould KG. The effects of antifreeze peptide III (AFP) and insulin transferrin selenium (ITS) on cryopreservation of chimpanzee (Pan troglodytes) spermatozoa. J Androl 1998; 19:207-214.
22. Prathalingam NS, Holt WV, Revell SG, Mirczuk S, Fleck RA, Watson PF. Impact of antifreeze proteins and antifreeze glycoproteins on bovine sperm during freeze-thaw. Theriogenology 2006; 66:1894-1900.
23. Fabbrocini A, Lavadera SL, Rispoli S, Sansone G. Cryopreservation of seabream (Sparus aurata) spermatozoa. Cryobiology 2000; 40:46-53.
24. Cabrita E, Robles V, Cuñado S, Wallace JC, Sarasquete C, Herráez MP. Evaluation of gilthead sea bream, Sparus aurata, sperm quality after cryopreservation in 5ml macrotubes. Cryobiology 2005; 50:273-284.
25. Beiraõ J, Pérez-Cerezales S, Martínez-Páramo S, Herráez MP. Detection of early damage of sperm cell membrane in gilthead seabream (Sparus aurata) with the nuclear stain YO-PRO 1. J Appl Ichthyol 2010; 26:794-796.
26. Beiraõ J, Cabrita E, Pérez-Cerezales S, Martínez-Páramo S, Herráez MP. Effect of cryopreservation on fish sperm subpopulations. Cryobiology 2011; 62:22-31.
27. Zilli L, Schiavone R, Storelli C, Vilella S. Molecular mechanisms determining sperm motility initiation in two sparids (Sparus aurata and Lithognathus mormyrus). Biol Reprod 2008; 79:356-366.
28. Folch J, Lees M, Stanley GHS. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 1957; 226:497-509.
29. Rouser G, Fleischer S, Yamamoto A. 2 dimensional thin layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids 1970; 5:494-496.
30. Berry JF, Cevallos WH, Wade RR. Lipid class and fatty acid composition of intact peripheral nerve and during wallerian degeneration. J Am Oil Chem Soc 1965; 42:492-500.
31. Connor WE, Lin DS, Wolf DP, Alexander M. Uneven distribution of desmosterol and docosahexaenoic acid in the heads and tails of monkey sperm. J Lipid Res 1998; 39:1404-1411.
32. Buffone MG, Doncel GF, Calamera JC, Verstraeten SV. Capacitationassociated changes in membrane fluidity in asthenozoospermic human spermatozoa. Int J Androl 2009; 32:360-375.
33. Drokin SI. Phospholipids and fatty-acids of phospholipids of sperm from several fresh-water and marine species of fish. Comp Biochem Physiol B Comp Mol Biol 1993; 104:423-428.
34. Buhr MM, Curtis EF, Kakuda NS. Composition and behavior of head membrane-lipids of fresh and cryopreserved boar sperm. Cryobiology 1994; 31:224-238.
35. LabbéC, Maisse G, Muller K, Zachowski A, Kaushik S, Loir M. Thermalacclimation and dietary lipids alter the composition, but not fluidity, of trout sperm plasma-membrane. Lipids 1995; 30:23-33.
36. Surai PF, Brillard JP, Speake BK, Blesbois E, Seigneurin F, Sparks NHC. Phospholipid fatty acid composition, vitamin E content and susceptibility to lipid peroxidation of duck spermatozoa. Theriogenology 2000; 53:1025-1039.
37. Cosson J, Croison AL, Suquet M, Fauvel C, Dreanno C, Billard R. Marine fish spermatozoa: racing ephemeral swimmers. Reproduction 2008; 136:277-294.
38. Babiak I, Bolla S, Ottensen O. Suitable methods for cryopreservation of semen from Atlantic halibut, Hippoglossus hippoglossus L. Aquacult Int 2008; 16:561-572.
39. Peñaranda DS, Pérez L, Gallego V, Jover M, Asturiano JF. Improvement of European eel sperm cryopreservation method by preventing spermatozoa movement activation caused by cryoprotectants. Cryobiology 2009; 59:119-126.
40. Milani C, Fontbonne A, Sellem E, Stelletta C, Gérard O, Romagnoli S. Effect of post-thaw dilution with caffeine, pentoxifylline, 2'-deoxyadenosine and prostatic fluid on motility of frozen-thawed dog semen. Theriogenology 2010; 74:153-164.
41. Cosson J. Frenetic activation of fish spermatozoa flagella entails shortterm motility, portending their precocious decadence. J Fish Biol 2010; 76:240-279.
42. Kaupp UB, Kashikar ND, Weyand I. Mechanisms of sperm chemotaxis. Annu Rev Physiol 2008; 70:93-117.
43. Kinukawa M, Nagata M, Aoki F. Changes in flagellar bending during the course of hyperactivation in hamster spermatozoa. Reproduction 2003; 125:43-51.
44. Chang H, Suarez SS. Rethinking the relationship between hyperactivation and chemotaxis in mammalian sperm. Biol Reprod 2010; 83:507-513.
45. Payne SR, Oliver JE, Upreti GC. Effect of antifreeze proteins on the motility of ram spermatozoa. Cryobiology 1994; 31:180-184.
46. Koshimoto C, Mazur P. Effects of warming rate, temperature, and antifreeze proteins on the survival of mouse spermatozoa frozen at an optimal rate. Cryobiology 2002; 45:49-59.
47. Blesbois E, Grasseau I, Seigneurin F. Membrane fluidity and the ability of domestic bird spermatozoa to survive cryopreservation. Reproduction 2005; 129:371-378.
48. Cerolini S, Maldjian A, Pizzi F, Gliozzi TM. Changes in sperm quality and lipid composition during cryopreservation of boar semen. Reproduction 2001; 121:395-401.
49. Tomczak MM, Vigh L, Meyer JD, Manning MC, Hincha DK, Crowe JH. Lipid unsaturation determines the interaction of AFP type I with model membranes during thermotropic phase transitions. Cryobiology 2002; 45:135-142.