Theriogenology
Volume 73, Issue 1 , Pages 86-96 , 1 January 2010

Cryopreservation of immature porcine testis tissue to maintain its developmental potential after xenografting into recipient mice

  • M. Abrishami

      Affiliations

    • Department of Veterinary Biomedical Sciences, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan, Canada
  • ,
  • M. Anzar

      Affiliations

    • Canadian Animal Genetic Resources Program, Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan, Canada
  • ,
  • Y. Yang

      Affiliations

    • Department of Veterinary Biomedical Sciences, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan, Canada
  • ,
  • A. Honaramooz

      Affiliations

    • Department of Veterinary Biomedical Sciences, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan, Canada
    • Corresponding Author InformationCorresponding author. Tel.: +1 306 966 7355; fax: +1 306 966 7376.

Received 19 March 2009 ,Revised 18 August 2009 ,Accepted 18 August 2009.

References 

  1. Brinster RL, Avarbock MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci U S A. 1994;91:11303–11307
  2. Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A. 1994;91:11298–11302
  3. Honaramooz A, Snedaker A, Boiani M, Scholer H, Dobrinski I, Schlatt S. Sperm from neonatal mammalian testes grafted in mice. Nature. 2002;418:778–781
  4. Avarbock MR, Brinster CJ, Brinster RL. Reconstitution of spermatogenesis from frozen spermatogonial stem cells. Nat Med. 1996;2:693–696
  5. Nagano M, Brinster RL. Spermatogonial transplantation and reconstitution of donor cell spermatogenesis in recipient mice. APMIS. 1998;106:47–55
  6. Brook PF, Radford JA, Shalet SM, Joyce AD, Gosden RG. Isolation of germ cells from human testicular tissue for low temperature storage and autotransplantation. Fertil Steril. 2001;75:269–274
  7. Izadyar F, Matthijs-Rijsenbilt JJ, den Ouden K, Creemers LB, Woelders H, de Rooij DG. Development of a cryopreservation protocol for type A spermatogonia. J Androl. 2002;23:537–545
  8. Tournaye H, Goossens E, Verheyen G, Frederickx V, De Block G, Devroey P, et al. Preserving the reproductive potential of men and boys with cancer: current concepts and future prospects. Hum Reprod Update. 2004;10:525–532
  9. Keros V, Rosenlund B, Hultenby K, Aghajanova L, Levkov L, Hovatta O. Optimizing cryopreservation of human testicular tissue: comparison of protocols with glycerol, propanediol and dimethylsulphoxide as cryoprotectants. Hum Reprod. 2005;20:1676–1687
  10. Kvist K, Thorup J, Byskov AG, Hoyer PE, Mollgard K, Yding Andersen C. Cryopreservation of intact testicular tissue from boys with cryptorchidism. Hum Reprod. 2006;21:484–491
  11. Keros V, Hultenby K, Borgstrom B, Fridstrom M, Jahnukainen K, Hovatta O. Methods of cryopreservation of testicular tissue with viable spermatogonia in pre-pubertal boys undergoing gonadotoxic cancer treatment. Hum Reprod. 2007;22:1384–1395
  12. Pegg DE. Principles of cryopreservation. Methods Mol Biol. 2007;368:39–57
  13. Paulenz H, Söderquist L, Adnøy T, Nordstoga A, Gulbrandsen B, Berg KA. Fertility results after different thawing procedures for ram semen frozen in minitubes and mini straws. Theriogenology. 2004;61:1719–1727
  14. Yavin S, Arav A. Measurement of essential physical properties of vitrification solutions. Theriogenology. 2007;67:81–89
  15. Bellve AR, Cavicchia JC, Millette CF, O’Brien DA, Bhatnagar YM, Dym M. Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J Cell Biol. 1977;74:68–85
  16. Honaramooz A, Megee SO, Dobrinski I. Germ cell transplantation in pigs. Biol Reprod. 2002;66:21–28
  17. Schlatt S, Honaramooz A, Boiani M, Scholer HR, Dobrinski I. Progeny from sperm obtained after ectopic grafting of neonatal mouse testes. Biol Reprod. 2003;68:2331–2335
  18. Schlatt S, Kim SS, Gosden R. Spermatogenesis and steroidogenesis in mouse, hamster and monkey testicular tissue after cryopreservation and heterotopic grafting to castrated hosts. Reproduction. 2002;124:339–346
  19. Honaramooz A, Li MW, Penedo MC, Meyers S, Dobrinski I. Accelerated maturation of primate testis by xenografting into mice. Biol Reprod. 2004;70:1500–1503
  20. Oatley JM, de Avila DM, Reeves JJ, McLean DJ. Spermatogenesis and germ cell transgene expression in xenografted bovine testicular tissue. Biol Reprod. 2004;71:494–501
  21. Snedaker AK, Honaramooz A, Dobrinski I. A game of cat and mouse: xenografting of testis tissue from domestic kittens results in complete cat spermatogenesis in a mouse host. J Androl. 2004;25:926–930
  22. Rathi R, Honaramooz A, Zeng W, Turner R, Dobrinski I. Germ cell development in equine testis tissue xenografted into mice. Reproduction. 2006;131:1091–1098
  23. Arregui L, Rathi R, Megee SO, Honaramooz A, Gomendio M, Roldan ER, et al. Xenografting of sheep testis tissue and isolated cells as a model for preservation of genetic material from endangered ungulates. Reproduction. 2008;136:85–93
  24. Honaramooz A, Cui XS, Kim NH, Dobrinski I. Porcine embryos produced after intracytoplasmic sperm injection using xenogeneic pig sperm from neonatal testis tissue grafted in mice. Reprod Fertil Dev. 2008;20:802–807
  25. Shinohara T, Inoue K, Ogonuki N, Kanatsu-Shinohara M, Miki H, Nakata K, et al. Birth of offspring following transplantation of cryopreserved immature testicular pieces and in-vitro microinsemination. Hum Reprod. 2002;17:3039–3045
  26. Jahnukainen K, Ehmcke J, Schlatt S. Testicular xenografts: a novel approach to study cytotoxic damage in juvenile primate testis. Cancer Res. 2006;66:3813–3818
  27. Wyns C, Curaba M, Martinez-Madrid B, Van Langendonckt A, Francois-Xavier W, Donnez J. Spermatogonial survival after cryopreservation and short-term orthotopic immature human cryptorchid testicular tissue grafting to immunodeficient mice. Hum Reprod. 2007;22:1603–1611
  28. Cohen J, Simons RF, Edwards RG, Fehilly CB, Fishel SB. Pregnancies following the frozen storage of expanding human blastocysts. J In Vitro Fert Embryo Transf. 1985;2:59–64
  29. Milazzo JP, Vaudreuil L, Cauliez B, Gruel E, Masse L, Mousset-Simeon N, et al. Comparison of conditions for cryopreservation of testicular tissue from immature mice. Hum Reprod. 2008;23:17–28
  30. Jezek D, Schulze W, Kalanj-Bognar S, Vukelic Z, Milavec-Puretic V, Krhen I. Effects of various cryopreservation media and freezing-thawing on the morphology of rat testicular biopsies. Andrologia. 2001;33:368–378
  31. Jahnukainen K, Ehmcke J, Hergenrother SD, Schlatt S. Effect of cold storage and cryopreservation of immature non-human primate testicular tissue on spermatogonial stem cell potential in xenografts. Hum Reprod. 2007;22:1060–1067
  32. Goossens E, Frederickx V, Geens M, De Block G, Tournaye H. Cryosurvival and spermatogenesis after allografting prepubertal mouse tissue: comparison of two cryopreservation protocols. Fertil Steril. 2008;89:725–727
  33. Hovatta O, Foudila T, Siegberg R, Johansson K, von Smitten K, Reima I. Pregnancy resulting from intracytoplasmic injection of spermatozoa from a frozen-thawed testicular biopsy specimen. Hum Reprod. 1996;11:2472–2473
  34. Keros V. Cryopreservation of human fetus testicular tissue and low temperature bank creation for further application in clinical transplantology. Prob Cryobiol. 1999;3:54–58
  35. Anchordoguy TJ, Rudolph AS, Carpenter JF, Crowe JH. Modes of interaction of cryoprotectants with membrane phospholipids during freezing. Cryobiology. 1987;24:324–331
  36. Gao DY, Lin S, Watson PF, Critser JK. Fracture phenomena in an isotonic salt solution during freezing and their elimination using glycerol. Cryobiology. 1995;32:270–284
  37. Lovelock JE. The mechanism of the protective action of glycerol against haemolysis by freezing and thawing. Biochim Biophys Acta. 1953;11:28–36
  38. Fuller B, Paynter S. Fundamentals of cryobiology in reproductive medicine. Reprod Biomed Online. 2004;9:680–691
  39. Elmoazzen HY, Elliott JA, McGann LE. Cryoprotectant equilibration in tissues. Cryobiology. 2005;51:85–91
  40. Dubochet J, Adrian M, Chang JJ, Homo JC, Lepault J, McDowall AW, et al. Cryo-electron microscopy of vitrified specimens. Q Rev Biophys. 1988;21:129–228
  41. Steven AC, Aebi U. The next ice age: cryo-electron tomography of intact cells. Trends Cell Biol. 2003;13:107–110
  42. Pegg DE. Cryobiology. In: Proceedings of the Fourth International Cryogenic Engineering Conference, Eindhoven. IPC Science and Technology Press, Guilford, UK, 1972, pp. 47–54.
  43. Trombetta C, Liguori G, Gianaroli L, Magli MC, Selman HA, Colpi G, et al. Testicular sperm extraction combined with cryopreservation of testicular tissue in the treatment of azoospermia. Urol Int. 2000;65:15–20

PII: S0093-691X(09)00390-2

doi: 10.1016/j.theriogenology.2009.08.004

Theriogenology
Volume 73, Issue 1 , Pages 86-96 , 1 January 2010