Theriogenology
Volume 74, Issue 8 , Pages 1420-1430 , November 2010

Comparison of sperm quality and DNA integrity in mouse sperm exposed to various cooling velocities and osmotic stress

  • Cengiz Yildiz

      Affiliations

    • Physiology and Experimental Medicine Research Program, The Hospital for Sick Children, Toronto, Ontario, Canada M5G 1X8
    • Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada M5G 1X8
    • Department of Reproduction and Artificial Insemination, Faculty of Veterinary Medicine, University of Mustafa Kemal, Hatay, Turkey
    • ,
  • Napoleon Law

      Affiliations

    • Physiology and Experimental Medicine Research Program, The Hospital for Sick Children, Toronto, Ontario, Canada M5G 1X8
    • ,
  • Palma Ottaviani

      Affiliations

    • Physiology and Experimental Medicine Research Program, The Hospital for Sick Children, Toronto, Ontario, Canada M5G 1X8
    • ,
  • Keith Jarvi

      Affiliations

    • Division of Urology, Mount Sinai Hospital, University of Toronto, Toronto, Ontario, Canada M5G 1X6
    • ,
  • Colin McKerlie

      Affiliations

    • Physiology and Experimental Medicine Research Program, The Hospital for Sick Children, Toronto, Ontario, Canada M5G 1X8
    • Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada M5G 1X8
    • Corresponding Author InformationCorresponding author. Tel.: +1 647-837-5840; fax: +1 647-837-5834

Received 16 July 2009 ,Revised 23 April 2010 ,Accepted 10 June 2010.

References 

  1. Schreuders PD, Jetton AE, Baker JL, Critser JK, Mazur P. Mechanical and chill sensitivity of mouse sperm. Cryobiology. 1996;33:676–677
  2. Katkov II, Mazur P. Influence of centrifugation regimens on motility, yield, and cell associations of mouse spermatozoa. J Androl. 1998;19:232–241
  3. Willoughby CE, Mazur P, Peter AT, Critser JK. Osmotic tolerance limits and properties of murine spermatozoa. Biol Reprod. 1996;55:715–727
  4. Alvarez JG, Storey BT. Role of glutathione peroxidase in protecting mammalian spermatozoa from loss of motility caused by spontaneous lipid peroxidation. Gamete Res. 1989;23:77–90
  5. Critser JK, Mobraaten LE. Cryopreservation of murine spermatozoa. Institute for Laboratory Animal Research Journal. 2000;41:4
  6. Hammerstedt RH, Crichton EG, Watson PF. Comparative approach to sperm cryopreservation: Does cell shape and size influence cryosurvival? In: Proceedings, Society for Theriogenology, San Diego, CA, Society for Theriogenology, Hastings, NE 1991. p. 8–11.
  7. Noiles EE, Bailey JL, Storey BT. The temperature dependence in the hydraulic conductivity, Lp, of the mouse sperm plasma membrane shows a discontinuity between 4 and 0 degrees C. Cryobiology. 1995;32:220–238
  8. Noiles EE, Thompson KA, Storey BT. Water permeability, Lp, of the mouse sperm plasma membrane and its activation energy are strongly dependent on interaction of the plasma membrane with the sperm cytoskeleton. Cryobiology. 1997;35:79–92
  9. Parks JE, Graham JK. Effects of cryopreservation procedures on sperm membranes. Theriogenology. 1992;38:209–222
  10. Gilmore JA, Liu J, Woods EJ, Peter AT, Critser JK. Cryoprotective agent and temperature effects on human sperm membrane permeabilites: Convergence of theoretical and empirical approaches for optimal cryopreservation methods. Hum Reprod. 2000;15:335–343
  11. Mazur P, Koshimoto C. Is intracellular ice formation the cause of death of mouse sperm frozen at high cooling rates?. Biol Reprod. 2002;66:1485–1490
  12. Nishizono H, Shioda M, Takeo T, Irie T, Nakagata N. Decrease of fertilizing ability of mouse spermatozoa after freezing and thawing is related to cellular injury. Biol Reprod. 2004;71:973–978
  13. Songsasen N, Leibo SP. Cryopreservation of mouse spermatozoa (II. Relationship between survival after cryopreservation and osmotic tolerance of spermatozoa from three strains of mice). Cryobiology. 1997;35:255–269
  14. Sztein JM, Noble K, Farley JS, Mobraaten LE. Comparison of permeating and nonpermeating cryoprotectants for mouse sperm cryopreservation. Cryobiology. 2001;42:28–39
  15. Byers SL, Payson SJ, Taft RA. Performance of ten inbred mouse strains following assisted reproductive technologies (ARTs). Theriogenology. 2006;65:1716–1726
  16. Ho Y, Wigglesworth K, Eppig JJ, Schultz RM. Preimplantation development of mouse embryos in KSOM: augmentation by amino acids and analysis of gene expression. Mol Reprod Dev. 1995;41:232–238
  17. Sztein JM, Farley JS, Mobraaten LE. In vitro fertilization with cryopreserved inbred mouse sperm. Biol Reprod. 2000;63:1774–1780
  18. Roudebush WE, Duralia DR. Superovulation, fertilization, and in vitro embryo development in BALB/cByJ, BALB/cJ, B6D2F1/J, and CFW mouse strains. Lab Anim Sci. 1996;46:239–240
  19. Scott L, Whittingham DG. Influence of genetic background and media components on the development of mouse embryos in vitro. Mol Reprod Dev. 1996;43:336–346
  20. Agca Y, Gilmore J, Byers M, Woods EJ, Liu J, Critser JK. Osmotic characteristics of mouse spermatozoa in the presence of extenders and sugars. Biol Reprod. 2002;67:1493–1501
  21. Walters EM, Men H, Agca Y, Mullen SF, Critser ES, Critser JK. Osmotic tolerance of mouse spermatozoa from various genetic backgrounds: acrosome integrity, membrane integrity, and maintenance of motility. Cryobiology. 2005;50:193–205
  22. Royere D, Barthelemy C, Hamamah S, Lansac J. Cryopreservation of spermatozoa: a 1996 review. Hum Reprod Update. 1996;2:553–559
  23. Yildiz C, Ottaviani P, Law N, Ayearst R, Liu L, McKerlie C. Effects of cryopreservation on sperm quality, nuclear DNA integrity, in vitro fertilization, and in vitro embryo development in the mouse. Reproduction. 2007;133:585–595
  24. Nakagata N. Cryopreservation of mouse spermatozoa. Mammal Genome. 2000;11:572–576
  25. Songsasen N, Leibo SP. Cryopreservation of mouse spermatozoa (I. Effect of seeding on fertilizing ability of cryopreserved spermatozoa). Cryobiology. 1997;35:240–254
  26. W.H.O. Health Organization. Laboratory manual for the examination of human semen and sperm-cervical mucus interaction. 4th Edition. Cambridge: Cambridge University Press; 1999;
  27. Quinn P, Kerin JF, Warnes GM. Improved pregnancy rate in human in vitro fertilization with the use of a medium based on the composition of human tubal fluid. Fertil Steril. 1985;44:493–498
  28. Larson KL, DeJonge CJ, Barnes AM, Jost LK, Evenson DP. Sperm chromatin structure assay parameters as predictors of failed pregnancy following assisted reproductive techniques. Hum Reprod. 2000;15:1717–1722
  29. Traina ME, Rescia M, Urbani E, Mantovani A, Macri C, Ricciardi C, et al. Long-lasting effects of lindane on mouse spermatogenesis induced by in utero exposure. Reprod Toxicol. 2003;17:25–35
  30. Marschall S, Hrabe de Angelis M. Cryopreservation of mouse spermatozoa: double your mouse space. Trends Genet. 1999;15:128–131
  31. Marschall S, Huffstadt U, Balling R, Hrabĕ de Angelis M. Reliable recovery of inbred mouse lines using cryopreserved spermatozoa. Mammal Genome. 1999;10:773–776
  32. Thornton CE, Brown SD, Glenister PH. Large numbers of mice established by in vitro fertilization with cryopreserved spermatozoa: implications and applications for genetic resource banks, mutagenesis screens, and mouse backcrosses. Mammal Genome. 1999;10:987–992
  33. Nallella KP, Sharma RK, Allamaneni SS, Aziz N, Agarwal A. Cryopreservation of human spermatozoa: comparison of two cryopreservation methods and three cryoprotectants. Fertil Steril. 2004;82:913–918
  34. Stanic P, Tandara M, Sonicki Z, Simunic V, Radakovic B, Suchanek E. Comparison of protective media and freezing techniques for cryopreservation of human semen. Eur J Obstet Gynecol Reprod Biol. 2000;91:65–70
  35. Pena A, Linde-Forsberg C. Effects of Equex, one- or two-step dilution, and two freezing and thawing rates on post-thaw survival of dog spermatozoa. Theriogenology. 2000;54:859–875
  36. Strom B, Rota A, Linde-Forsberg C. In vitro characteristics of canine spermatozoa subjected to two methods of Cryopreservation. Theriogenology. 1997;15:247–256
  37. Foote RH, Kaprotht MT. Large batch freezing of bull semen: effect of time of freezing and fructose on fertility. J Dairy Sci. 2002;85:453–456
  38. Rasul Z, Anzar M, Jalali S, Ahmad N. Effect of buffering systems on post-thaw motion characteristics, plasma membrane integrity, and acrosome morphology of buffalo spermatozoa. Anim Reprod Sci. 2000;59:31–41
  39. Pontbriand D, Howard JG, Schiewe MC, Stuart LD, Wildt DE. Effect of cryoprotective diluent and method of freeze-thawing on survival and acrosomal integrity of ram spermatozoa. Cryobiology. 1989;26:341–354
  40. Hammadeh ME, Szarvasy D, Zeginiadou T, Rosenbaum P, Georg T, Schmidt W. Evaluation of cryoinjury of spermatozoa after slow (programmed biological freezer) or rapid (liquid nitrogen vapor) freeze-thawing techniques. J Assist Reprod Genet. 2001;18:364–370
  41. Koshimoto C, Mazur P. Effects of cooling and warming rate to and from −70 degrees C, and effect of further cooling from −70 to −196 degrees C on the motility of mouse spermatozoa. Biol Reprod. 2002;66:1477–1484
  42. Devireddy RV, Swanlund DJ, Roberts KP, Bischof JC. Subzero water permeability parameters of mouse spermatozoa in the presence of extracellular ice and cryoprotective agents. Biol Reprod. 1999;61:764–775
  43. Nakagata N, Takeshima T. Cryopreservation of mouse spermatozoa from inbred and F1 hybrid strains. Jikken Dobutsu. 1993;42:317–320
  44. An TZ, Iwakiri M, Edashige K, Sakurai T, Kasai M. Factors affecting the survival of frozen-thawed mouse spermatozoa. Cryobiology. 2000;40:237–249
  45. Dewit M, Marley WS, Graham JK. Fertilizing potential of mouse spermatozoa cryopreserved in a medium containing whole eggs. Cryobiology. 2000;40:36–45
  46. Kusakabe H, Szczygiel MA, Whittingham DG, Yanagimachi R. Maintenance of genetic integrity in frozen and freeze-dried mouse spermatozoa. Proc Natl Acad Sci USA. 2001;98:13501–13506
  47. Ward MA, Kaneko T, Kusakabe H, Biggers JD, Whittingham DG, Yanagimachi R. Long-term preservation of mouse spermatozoa after freeze-drying and freezing without cryoprotection. Biol Reprod. 2003;69:2100–2108
  48. Koshimoto C, Mazur P. The effect of the osmolality of sugar-containing media, the type of sugar, and the mass and molar concentration of sugar on the survival of frozen-thawed mouse sperm. Cryobiology. 2002;45:80–90
  49. Mazur P, Katkov II, Katkova N, Critser JK. The enhancement of the ability of mouse sperm to survive freezing and thawing by the use of high concentrations of glycerol and the presence of an Escherichia coli membrane preparation (Oxyrase) to lower the oxygen concentration. Cryobiology. 2000;40:187–209
  50. Alvarez JG, Storey BT. Evidence for increased lipid peroxidative damage and loss of superoxide dismutase activity as a mode of sublethal cryodamage to human sperm during Cryopreservation. J Androl. 1992;13:232–241
  51. Aitken RJ, Clarkson JS, Fishel S. Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biol Reprod. 1989;41:183–197
  52. Aitken RJ, Buckingham D, Harkiss D. Use of a xanthine oxidase free radical generating system to investigate the cytotoxic effects of reactive oxygen species on human spermatozoa. J Reprod Fertil. 1993;97:441–450
  53. Flaherty SP, Payne D, Swann NJ, Mattews CD. A etiology of failed and abnormal fertilization after intracytoplasmic sperm injection. Hum Reprod. 1995;10:2623–2629
  54. Chohan KR, Griffin JT, Carrell DT. Evaluation of chromatin integrity in human sperm using acridine orange staining with different fixatives and after cryopreservation. Andrologia. 2004;36:321–326
  55. Donnelly ET, McClure N, Lewis SE. Cryopreservation of human semen and prepared sperm: effects on motility parameters and DNA integrity. Fertil Steril. 2001;76:892–900
  56. Royere D, Hamamah S, Nicolle JC, Barthelemy C, Lansac J. Freezing and thawing alter chromatin stability of ejaculated human spermatozoa: fluorescence acridine orange staining and Feulgen-DNA cytophotometric studies. Gamete Res. 1988;21:51–57
  57. Royere D, Hamamah S, Nicolle JC, Lansac J. Chromatin alterations induced by freeze-thawing influence the fertilizing ability of human sperm. Int J Androl. 1991;14:328–332
  58. Fraser L, Strzezek J. The use of comet assay to assess DNA integrity of boar spermatozoa following liquid preservation at 5 degrees C and 16 degrees C Folia. Histochem Cytobiol. 2004;42:49–55
  59. Fraser L, Strzezek J. Is there a relationship between the chromatin status and DNA fragmentation of boar spermatozoa following freezing-thawing?. Theriogenology. 2007;15:248–257
  60. Linfor JJ, Mayers SA. Detection of DNA damage in response to cooling injury in equine spermatozoa using single-cell gel electrophoresis. J Androl. 2002;23:107–113
  61. Peris SI, Morrier A, Dufour M, Bailey JL. Cryopreservation of ram semen facilitates sperm DNA damage: relationship between sperm andrological parameters and the sperm chromatin structure assay. J Androl. 2004;25:224–233
  62. Peris SI, Bilodeau JF, Dufour M, Bailey JL. Impact of cryopreservation and reactive oxygen species on DNA integrity, lipid peroxidation, and functional parameters in ram sperm. Mol Reprod Dev. 2007;74:878–892
  63. Koshimoto C, Gamliel E, Mazur P. Effect of osmolality and oxygen tension on the survival of mouse sperm frozen to various temperatures in various concentrations of glycerol and raffinose. Cryobiology. 2000;41:204–231
  64. Gao DY, Liu J, Liu C, McGann LE, Watson PF, Kleinhans FW, et al. Prevention of osmotic injury to human spermatozoa during addition and removal of glycerol. Hum Reprod. 1995;10:1109–1122
  65. Gilmore JA, Liu J, Peter AT, Critser JK. Determination of plasma membrane characteristics of boar spermatozoa and their relevance to cryopreservation. Biol Reprod. 1998;58:28–36

PII: S0093-691X(10)00331-6

doi: 10.1016/j.theriogenology.2010.06.014

Theriogenology
Volume 74, Issue 8 , Pages 1420-1430 , November 2010

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