Theriogenology
Volume 73, Issue 6 , Pages 740-747 , 1 April 2010

Xenotransplantation in immunodeficient mice to study ovarian follicular development in domestic animals

  • P.E.J. Bols

      Affiliations

    • Laboratory of Veterinary Physiology, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, Wilrijk, Belgium
    • Corresponding Author InformationCorresponding author. Tel.: +32 3 820 23 95; fax: +32 3 820 24 33.
    • ,
  • J.M.J. Aerts

      Affiliations

    • Laboratory of Cell Biology and Histology, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, Antwerpen, Belgium
    • ,
  • A. Langbeen

      Affiliations

    • Laboratory of Veterinary Physiology, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, Wilrijk, Belgium
    • ,
  • I.G.F. Goovaerts

      Affiliations

    • Laboratory of Veterinary Physiology, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, Wilrijk, Belgium
    • ,
  • J.L.M.R. Leroy

      Affiliations

    • Laboratory of Veterinary Physiology, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, Wilrijk, Belgium

Received 1 April 2009 ,Accepted 8 August 2009.

References 

  1. Aerts JMJ, Bols PEJ. Ovarian follicular dynamics. A review with emphasis on the bovine species. Part I: folliculogenesis and preantral follicle development. Reprod Domest Anim 2009, in press, doi:10.1111/j.1439-0531-2008.01302.x.
  2. Aerts JMJ, Bols PEJ. Ovarian follicular dynamics. A review with emphasis on the bovine species. Part II: antral development, exogenous influence and future prospects. Reprod Domest Anim 2009, in press, doi:10.1111/j.1439-0531-2008.01298.x.
  3. Fortune JE. The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Anim Reprod Sci. 2003;78:135–163
  4. Cortvrindt R, Smitz J, Van Steirteghem AC. In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simplified culture system. Hum Reprod. 1996;11:2656–2666
  5. Oktem O, Oktay K. The ovary: anatomy and function throughout human life. Ann N Y Acad Sci. 2008;1127:1–9
  6. Adams GP, Pierson RA. Bovine model for study of ovarian follicular dynamics in humans. Theriogenology. 1995;43:113–120
  7. Malhi PS, Adams GP, Singh J. Bovine model for the study of reproductive ageing in women: follicular, luteal, and endocrine characteristics. Biol Reprod. 2005;73:45–53
  8. Baerwald AR, Adams GP, Pierson RA. A new model for ovarian follicular development during the human menstrual cycle. Fertil Steril. 2003;80:116–122
  9. Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squifflet J, et al. Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet. 2004;364:1405–1410
  10. Demeestere I, Simon P, Emiliani S, Delbaere A, Englert Y. Fertility preservation: successful transplantation of cryopreserved ovarian tissue in a young patient previously treated for Hodgkins's disease. Oncologist. 2007;12:1437–1442
  11. Bedaiwy MA, El-Nashar SA, El Saman AM, Evers JLH, Sandadi S, Desai N, et al. Reproductive outcome after transplantation of ovarian tissue: a systematic review. Hum Reprod. 2008;23:2709–2717
  12. Shaw J, Trounson A. Oncological implications in the replacement of ovarian tissue. Hum Reprod. 1997;12:403–405
  13. Kim SS, Radford J, Harris M, Varley J, Rutherford AJ, Lieberman B, et al. Ovarian tissue harvested from lyphoma patients to preserve fertility may be safe for autotransplantation. Hum Reprod. 2001;16:2056–2060
  14. Kim SS, Soules MR, Battaglia DE. Follicular development, ovulation and corpus luteum formation in cryopreserved human ovarian tissue after xenotransplantation. Fertil Steril. 2002;78:77–82
  15. Liu J, Van der Elst J, Van Den Broecke , Dumortier F, Dhondt M. Maturation of mouse primordial follicles by combination of grafting and in vitro culture. Biol Reprod. 2000;62:1218–1223
  16. Telfer EE, McLaughin M, Ding C, Thong KJ. A two-step serum-free culture system supports development of human oocytes from primordial follicles in the presence of activin. Hum Reprod. 2008;23:1151–1158
  17. Smitz JE, Cortvrindt RG. The earliest stages of folliculogenesis in vitro. Reproduction. 2002;123:185–202
  18. Torrents E, Boiso I, Barri PN, Veiga A. Applications of ovarian tissue transplantation in experimental biology and medicine. Hum Reprod Update. 2003;9:471–481
  19. Senbon S, Ishii K, Fukumi Y, Miyano T. Fertilization and development of bovine oocytes grown in female SCID mice. Zygote. 2005;13:309–315
  20. Donnez J, Martinez-Madrid B, Jadoul P, Van Langendonckt A, Demylle D, Dolmans MM. Ovarian tissue cryopreservation and transplantation: a review. Hum Reprod Update. 2006;12:519–535
  21. Baird DT, Campbell B, de Souza C, Telfer E. Long-term ovarian function in sheep after ovariectomy and autotransplantation of cryopreserved cortical strips. Eur J Obstet Gynecol Reprod Biol. 2004;113(Suppl 1):S55–S59
  22. Kim SS, Kang HG, Kim NH, Lee HC, Lee HH. Assessment of the integrity of human oocytes retrieved from cryopreserved ovarian tissue after xenotransplantation. Hum Reprod. 2005;20:2502–2508
  23. Aerts JMJ, Oste M, Bols PEJ. Development and practical applications of a method for repeated transvaginal, ultrasound-guided biopsy collection of the bovine ovary. Theriogenology. 2005;64:947–957
  24. Bols PEJ, Vandenheede JMM, Van Soom A, de Kruif A. Transvaginal ovum pick-up (OPU) in the cow: a new disposable needle guidance system. Theriogenology. 1995;43:677–687
  25. Aerts JMJ, Martinez-Madrid B, Flothmann K, de Clercq JPB, Van Aelst S, Bols PEJ. Quantification and viability assessment of isolated bovine primordial and primary ovarian follicles retrieved through a standardized biopsy pick-up procedure. Reprod Domest Anim. 2008;43:360–366
  26. Flanagan SP. ‘Nude’ a new hairless gene with pleiotropic effects in the mouse. Genet Res. 1966;8:295–309
  27. Bosma GC, Custer RP, Bosma MJ. A severe combined immunodeficiency mutation in the mouse. Nature. 1983;301:527–530
  28. Weissman A, Gotlieb L, Colgan T, Jurisicova A, Greenblatt EM, Casper RF. Preliminary experience with subcutaneous human ovarian cortex transplantation in the NOD-SCID mouse. Biol Reprod. 1999;60:1462–1467
  29. Oktay K, Yih M. Preliminary experience with orthotopic and heterotopic transplantation of ovarian cortical strips. Semin Reprod Med. 2002;20:63–74
  30. Oktay K, Buyuk E, Rosenwaks Z, Rucinski J. A technique for transplantation of ovarian cortical strips to the forearm. Fertil Steril. 2003;80:193–198
  31. Gosden RG, Boulton MI, Grant K, Webb R. Follicular development from ovarian xenografts in SCID mice. J Reprod Fertil. 1994;101:619–623
  32. Eimani H, Siadat SF, Eftekhari-Yazdi P, Parivar K, Rezazade M, Shahverdi A. Comparative study between intact and non-intact intramuscular autologous mouse ovaries. Reprod Biomed Online. 2009;18:53–60
  33. Yang HY, Cox SL, Jenkin G, Findlay J, Trounson A, Shaw J. Graft site and gonadotrophin stimulation influences the number and quality of oocytes from murine ovarian tissue grafts. Reproduction. 2006;131:851–859
  34. Hernandez-Fonseca H, Bosch P, Sirisathien S, Wininger JD, Massey JB, Brackett BG. Effect of site of transplantation on follicular development of human ovarian tissue transplanted into intact or castrated immunodeficient mice. Fertil Steril. 2004;81(Suppl 1):888–892
  35. Aerts JMJ, De Clercq JPB, Andries S, Leroy JLMR, Van Aelst S, Bols PEJ. Follicle survival and growth to antral stages in short-term murine ovarian cortical transplants after cryologic solid surface vitrification or slow-rate freezing. Cryobiology. 2008;57:163–169
  36. Koos RD. Potential relevance of angiogenic factors to ovarian physiology. Semin Reprod Endocrinol. 1989;7:29–40
  37. Gosden RG, Byatt-Smith JG. Oxygen concentration gradient across the ovarian follicular epithelium: model, predictions and implications. Hum Reprod. 1986;1:65–68
  38. Krohn PL. Transplantation of the ovary. In: The Ovary, Volume 2, Zuckerman S, Weir BJ, (Eds.), Academic Press, 1989, pp. 101–128.
  39. Jones EC, Krohn PL. Orthotopic ovarian transplantation in mice. J Endocrinol. 1960;20:135–146
  40. Felicio LS, Nelson JF, Gosden RG, Finch CE. Restoration of ovulatory cycles by young ovarian grafts in aging mice: potentiation by long term ovariectomy decreases with age. Proc Natl Acad Sci U S A. 1983;80:3076–3080
  41. Aubard Y, Piver P, Cognie Y, Fermeaux V, Poulin N, Driancourt MA. Orthotopic and heterotopic autografts of frozen-thawed ovarian cortex in sheep. Hum Reprod. 1999;14:2149–2154
  42. Hernandez-Fonseca HJ, Bosch P, Miller DM, Wininger JD, Massey JB, Brackett BG. Time course of follicular development after bovine ovarian tissue transplantation in male non-obese diabetic severe combined immunodeficient mice. Fertil Steril. 2005;83(Suppl 1):1180–1187
  43. Liu J, Van der Elst J, Van den Broecke R, Dhont M. Early massive follicle loss and apoptosis in heterotopically grafted newborn mouse ovaries. Hum Reprod. 2002;17:605–611
  44. Baird DT, Webb R, Campbell BK, Harkness LM, Gosden RG. Long-term ovarian function in sheep after ovariectomy and transplantation of autografts stored at -196C. Endocrinology. 1999;140:462–471
  45. Nugent D, Meirow D, Brook PF, Aubard Y, Gosden RG. Transplantation in reproductive medicine: previous experience, present knowledge and future prospects. Hum Reprod Update. 1997;3:267–280
  46. Dissen GA, Lara HE, Fahrenbach WH, Costa ME, Ojeda SR. Immature rat ovaries become revascularized rapidly after autotransplantation and show a gonadotropin-dependent increase in angiogenic factor gene expression. Endocrinology. 1994;134:1146–1154
  47. Van Eyck A, Jordan BF, Gallez B, Heilier J-F, Van Langendonckt A, Donnez J. Electron paramagnetic resonance as a tool to evaluate human ovarian tissue reoxygenation after xenografting. Fertil Steril. 2009;92:374–381
  48. Candy CJ, Wood MJ, Whittingham DG. Follicular development in cryopreserved marmoset ovarian tissue after transplantation. Hum Reprod. 1995;10:2334–2338
  49. Wolvekamp MC, Cleary ML, Cox SL, Shaw JM, Jenkin G, Trounson AO. Follicular development in cryopreserved common wombat ovarian tissue xenografted to nude rats. Anim Reprod Sci. 2001;65:135–147
  50. Paris MC, Snow M, Cox SL, Shaw JM. Xenotransplantation: a tool for reproductive biology and animal conservation?. Theriogenology. 2004;61:277–291
  51. Cleary M, Paris MCJ, Shaw JM, Jenkin G. Development of antral follicles in cryopreserved wombat ovarian tissue following xenotransplantation. Theriogenology. 2002;57:580
  52. Mattiske D, Snow M, Cox SL, Shaw G, Shaw JM. Development of oocytes following grafting of marsupial ovarian tissue to a eutherian recipient. In: Proceedings of the 47th Annual Scientific Meeting of the Australian Mammal Society 2100:35.
  53. Newton H, Aubard Y, Rutherford A, Sharma V, Gosden R. Low temperature storage and grafting of human ovarian tissue. Hum Reprod. 1996;11:1487–1491
  54. Nugent D, Newton H, Gallivan L, Gosden RG. Protective effect of vitamin E on ischaemia-reperfusion injury in ovarian grafts. J Reprod Fertil. 1998;114:341–346
  55. Parks DA, Bulkley GB, Granger DN, Hamilton SR, McCord JM. Ischemic injury in the cat small intestine: role of superoxide radicals. Gastroenterology. 1982;82:9–15
  56. Candy CJ, Wood MJ, Whittingham DG. Restoration of a normal reproductive lifespan after grafting of cryopreserved mouse ovaries. Hum Reprod. 2000;15:1300–1304
  57. Kim SS, Soules MR, Battaglia DE. Follicular development, ovulation, and corpus luteum formation in cryopreserved human ovarian tissue after xenotransplantation. Fertil Steril. 2002;78:77–82
  58. Kagawa N, Sakurai Y, Miyano T, Manabe N. Effects of long-term grafting on follicular growth in porcine ovarian cortical grafts xenoplanted to severe combined immunodeficient (SCID) mice. J Reprod Dev. 2005;51:77–85
  59. Metcalfe SS, Shaw JM, Gunn IM. Xenografting of canine ovarian tissue to ovariectomized severe combined immunodeficient (SCID) mice. J Reprod Fertil Suppl. 2001;57:323–329
  60. Bosch P, Hernandez-Fonseca HJ, Miller DM, Wininger JD, Massey JB, Lamb SV, et al. Development of antral follicles in cryopreserved cat ovarian tissue transplanted to immunodeficient mice. Theriogenology. 2004;61:581–594
  61. Semple E, Weissman A, Gotlieb L, Casper RF, Leibo SP. Transplantation of fresh or cryopreserved bovine ovarian cortex to NOD-SCID mice. Theriogenology. 2000;53:254
  62. Senbon S, Ota A, Tachibana M, Miyano T. Bovine oocytes in secondary follicles grow and acquire meiotic competence in severe combined immunodeficient mice. Zygote. 2003;11:139–149
  63. Oktay K, Newton H, Mullan J, Gosden RG. Development of human primordial follicles to antral stages in SCID/hpg mice stimulated with follicle stimulating hormone. Hum Reprod. 1998;13:1133–1138
  64. Hoyer PB, Devine PJ. Endocrinology and toxicology: the female reproductive system. In: Handbook of Toxicology, 2nd edition, Derelank MJ, Hollinger MA (Eds.), CRC Press, 2002, pp. 573-596.
  65. Baird DT, Campbell BK, Mann GE, McNeilly AS. Inhibin and oestradiol in the control of FSH secretion in the sheep. J Reprod Fertil Suppl. 1991;43:125–138
  66. Varghese AC, du Plessis SS, Falcone T, Agarwal A. Cryopreservation/transplantation of ovarian tissue and in vitro maturation of follicles and oocytes: challenges for fertility preservation. Reprod Biol Endocrinol. 2008;6:47–57
  67. Leroy JLMR, Opsomer G, Van Soom A, Goovaerts IGF, Bols PEJ. Reduced fertility in high yielding dairy cows: are the oocyte and embryo in danger? Part I: the importance of negative energy balance and altered corpus luteum function to the reduction of oocyte and embryo quality in high yielding dairy cows. Reprod Domest Anim. 2008;43:612–622
  68. Leroy JLMR, Van Soom A, Opsomer G, Goovaerts IGF, Bols PEJ. Reduced fertility in high yielding dairy cows: are the oocyte and embryo in danger? Part II: mechanisms linking nutrition and reduced oocyte and embryo quality in high yielding dairy cows. Reprod Domest Anim. 2008;43:623–632
  69. Aerts JMJ, Martinez-Madrid B, Leroy JLMR, Van Aelst S, Bols PEJ. Xenotransplantation by injection of a suspension of isolated preantral ovarian follicles and stroma cells under the kidney capsule of nude mice. Fertil Steril 2009, in press, doi:10.1016/j.fertnstert.2009.03.055.

PII: S0093-691X(09)00430-0

doi: 10.1016/j.theriogenology.2009.10.002

Theriogenology
Volume 73, Issue 6 , Pages 740-747 , 1 April 2010

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