Skip to main content

Advertisement

Log in

Use of nonhuman primates for the development of bioengineered female reproductive organs

  • Feature Article
  • Regenerative Medicine
  • Published:
Tissue Engineering and Regenerative Medicine Aims and scope

Abstract

Nonhuman primates (NHPs) have been widely used in reproductive biology, neuroscience, and drug development since a number of primate species are phylogenetically close to humans. In this review, we summarize the use of NHPs for nonclinical application in the reproductive system disorders including the loss or failure of an organ or tissue. Causes of infertility include congenital aplasia and acquired disorders of the reproductive organs. In addition, anti-cancer treatments can deplete ovarian follicles, leading to premature ovarian failure, infertility and long-term health risks. Along with a limited supply of human reproductive organs, anatomic/physiologic similarities to humans support the need for NHP models (New-World monkeys such as the common marmoset and Old-World monkeys such as cynomolgus and rhesus monkeys) to promote the advances in female infertility studies. For maintaining and executing animal studies using NHP, special protocols including animal care, anesthetic protocol, surgical technique, and immunosuppressive protocol are necessary. With a growing interest in the potential therapies such as endometrial tissue engineering, and ovary/follicle cryopreservation and grafting in Korea, this review can be useful in selecting appropriate animal models and can bridge between nonclinical studies and clinical applications by providing detailed information on the use of NHPs in the field of reproductive organ disorders.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Talmor A, Dunphy B. Female obesity and infertility. Best Pract Res Clin Obstet Gynaecol 2015;29:498–506.

    Article  PubMed  Google Scholar 

  2. Cates W, Farley TM, Rowe PJ. Worldwide patterns of infertility: is Africa different? Lancet 1985;2:596–598.

    Article  CAS  PubMed  Google Scholar 

  3. Practice Committee of the American Society for Reproductive Medicine. Effectiveness and treatment for unexplained infertility. Fertil Steril 2006; 86:S111–S114.

    Google Scholar 

  4. Griffin JE, Edwards C, Madden JD, Harrod MJ, Wilson JD. Congenital absence of the vagina. The Mayer-Rokitansky-Kuster-Hauser syndrome. Ann Intern Med 1976;85:224–236.

    CAS  PubMed  Google Scholar 

  5. Nahum GG. Uterine anomalies. How common are they, and what is their distribution among subtypes? J Reprod Med 1998;43:877–887.

    CAS  PubMed  Google Scholar 

  6. Sonoda Y, Abu-Rustum NR, Gemignani ML, Chi DS, Brown CL, Poynor EA, et al. A fertility-sparing alternative to radical hysterectomy: how many patients may be eligible? Gynecol Oncol 2004;95:534–538.

    Article  PubMed  Google Scholar 

  7. Marshall LM, Spiegelman D, Barbieri RL, Goldman MB, Manson JE, Colditz GA, et al. Variation in the incidence of uterine leiomyoma among premenopausal women by age and race. Obstet Gynecol 1997;90:967–973.

    Article  CAS  PubMed  Google Scholar 

  8. Buttram VC Jr, Reiter RC. Uterine leiomyomata: etiology, symptomatology, and management. Fertil Steril 1981;36:433–445.

    Article  PubMed  Google Scholar 

  9. Lü SH, Wang HB, Liu H, Wang HP, Lin QX, Li DX, et al. Reconstruction of engineered uterine tissues containing smooth muscle layer in collagen/matrigel scaffold in vitro. Tissue Eng Part A 2009;15:1611–1618.

    Article  PubMed  CAS  Google Scholar 

  10. Ding L, Li X, Sun H, Su J, Lin N, Péault B, et al. Transplantation of bone marrow mesenchymal stem cells on collagen scaffolds for the functional regeneration of injured rat uterus. Biomaterials 2014;35:4888–4900.

    Article  CAS  PubMed  Google Scholar 

  11. Deans R, Abbott J. Review of intrauterine adhesions. J Minim Invasive Gynecol 2010;17:555–569.

    Article  PubMed  Google Scholar 

  12. American College of Obstetricians and Gynecologists. ACOG Practice Bulletin No. 101: Ultrasonography in pregnancy. Obstet Gynecol 2009;113:451–461.

    Article  Google Scholar 

  13. Raju TN. The problem of late-preterm (near-term) births: a workshop summary. Pediatr Res 2006;60:775–776.

    Article  PubMed  Google Scholar 

  14. Chen SU, Chien CL, Wu MY, Chen TH, Lai SM, Lin CW, et al. Novel direct cover vitrification for cryopreservation of ovarian tissues increases follicle viability and pregnancy capability in mice. Hum Reprod 2006;21:2794–2800.

    Article  PubMed  Google Scholar 

  15. Jeruss JS, Woodruff TK. Preservation of fertility in patients with cancer. N Engl J Med 2009;360:902–911.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Blumenfeld Z. Chemotherapy and fertility. Best Pract Res Clin Obstet Gynaecol 2012;26:379–390.

    Article  PubMed  Google Scholar 

  17. Fleischer RT, Vollenhoven BJ, Weston GC. The effects of chemotherapy and radiotherapy on fertility in premenopausal women. Obstet Gynecol Surv 2011;66:248–254.

    Article  PubMed  Google Scholar 

  18. Katoh MA, Cain KT, Hughes LA, Foxworth LB, Bishop JB, Generoso WM. Female-specific dominant lethal effects in mice. Mutat Res 1990;230:205–217.

    Article  CAS  PubMed  Google Scholar 

  19. Elizur SE, Chian RC, Pineau CA, Son WY, Holzer HE, Huang JY, et al. Fertility preservation treatment for young women with autoimmune diseases facing treatment with gonadotoxic agents. Rheumatology (Oxford) 2008;47:1506–1509.

    Article  CAS  Google Scholar 

  20. Elizur SE, Chian RC, Holzer HE, Gidoni Y, Tulandi T, Tan SL. Cryopreservation of oocytes in a young woman with severe and symptomatic endometriosis: a new indication for fertility preservation. Fertil Steril 2009;91:293. e1-e3.

  21. Huang JY, Tulandi T, Holzer H, Lau NM, Macdonald S, Tan SL, et al. Cryopreservation of ovarian tissue and in vitro matured oocytes in a female with mosaic Turner syndrome: case report. Hum Reprod 2008;23:336–339.

    Article  CAS  PubMed  Google Scholar 

  22. Mihara M, Kisu I, Hara H, Iida T, Araki J, Shim T, et al. Uterine autotransplantation in cynomolgus macaques: the first case of pregnancy and delivery. Hum Reprod 2012;27:2332–2340.

    Article  PubMed  Google Scholar 

  23. Klemm P, Tozzi R, Köhler C, Hertel H, Schneider A. Does radical trachelectomy influence uterine blood supply? Gynecol Oncol 2005;96:283–286.

    Article  PubMed  Google Scholar 

  24. Palacios Jaraquemada JM, García Mínaco R, Barbosa NE, Ferle L, Iriarte H, Conesa HA. Lower uterine blood supply: extrauterine anastomotic system and its application in surgical devascularization techniques. Acta Obstet Gynecol Scand 2007;86:228–234.

    Article  PubMed  Google Scholar 

  25. Mihara M, Kisu I, Hara H, Iida T, Yamamoto T, Araki J, et al. Uterus autotransplantation in cynomolgus macaques: intraoperative evaluation of uterine blood flow using indocyanine green. Hum Reprod 2011;26:3019–3027.

    Article  PubMed  Google Scholar 

  26. Fageeh W, Raffa H, Jabbad H, Marzouki A. Transplantation of the human uterus. Int J Gynaecol Obstet 2002;76:245–251.

    Article  CAS  PubMed  Google Scholar 

  27. Erman Akar M, Ozkan O, Aydinuraz B, Dirican K, Cincik M, Mendilcioglu I, et al. Clinical pregnancy after uterus transplantation. Fertil Steril 2013;100:1358–1363.

    Article  PubMed  Google Scholar 

  28. Langer R, Vacanti JP. Tissue engineering. Science 1993;260:920–926.

    Article  CAS  PubMed  Google Scholar 

  29. Atala A. Tissue engineering of reproductive tissues and organs. Fertil Steril 2012;98:21–29.

    Article  CAS  PubMed  Google Scholar 

  30. Jonkman MF, Kauer FM, Nieuwenhuis P, Molenaar I. Segmental uterine horn replacement in the rat using a biodegradable microporous synthetic tube. Artif Organs 1986;10:475–480.

    Article  CAS  PubMed  Google Scholar 

  31. Taveau JW, Tartaglia M, Buchannan D, Smith B, Koenig G, Thomfohrde K, et al. Regeneration of uterine horn using porcine small intestinal submucosa grafts in rabbits. J Invest Surg 2004;17:81–92.

    Article  PubMed  Google Scholar 

  32. Putnam AJ, Mooney DJ. Tissue engineering using synthetic extracellular matrices. Nat Med 1996;2:824–826.

    Article  CAS  PubMed  Google Scholar 

  33. Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD. The extracellular matrix of animals. Molecular biology of the cell. New York: Garland Publishing; 1994. p. 971–995.

    Google Scholar 

  34. Yan X, Chen B, Lin Y, Li Y, Xiao Z, Hou X, et al. Acceleration of diabetic wound healing by collagen-binding vascular endothelial growth factor in diabetic rat model. Diabetes Res Clin Pract 2010;90:66–72.

    Article  CAS  PubMed  Google Scholar 

  35. Boccafoschi F, Habermehl J, Vesentini S, Mantovani D. Biological performances of collagen-based scaffolds for vascular tissue engineering. Biomaterials 2005;26:7410–7417.

    Article  CAS  PubMed  Google Scholar 

  36. Mathias FJ, D’Souza F, Uppangala S, Salian SR, Kalthur G, Adiga SK. Ovarian tissue vitrification is more efficient than slow freezing in protecting oocyte and granulosa cell DNA integrity. Syst Biol Reprod Med 2014;60:317–322.

    Article  CAS  PubMed  Google Scholar 

  37. Huang JY, Tulandi T, Holzer H, Tan SL, Chian RC. Combining ovarian tissue cryobanking with retrieval of immature oocytes followed by in vitro maturation and vitrification: an additional strategy of fertility preservation. Fertil Steril 2008;89:567–572.

    Article  PubMed  Google Scholar 

  38. Trounson A, Mohr L. Human pregnancy following cryopreservation, thawing and transfer of an eight-cell embryo. Nature 1983;305:707–709.

    Article  CAS  PubMed  Google Scholar 

  39. Porcu E, Fabbri R, Damiano G, Giunchi S, Fratto R, Ciotti PM, et al. Clinical experience and applications of oocyte cryopreservation. Mol Cell Endocrinol 2000;169:33–37.

    Article  CAS  PubMed  Google Scholar 

  40. 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.

    Article  CAS  PubMed  Google Scholar 

  41. Keros V, Xella S, Hultenby K, Pettersson K, Sheikhi M, Volpe A, et al. Vitrification versus controlled-rate freezing in cryopreservation of human ovarian tissue. Hum Reprod 2009;24:1670–1683.

    Article  CAS  PubMed  Google Scholar 

  42. Wang X, Catt S, Pangestu M, Temple-Smith P. Live offspring from vitrified blastocysts derived from fresh and cryopreserved ovarian tissue grafts of adult mice. Reproduction 2009;138:527–535.

    Article  CAS  PubMed  Google Scholar 

  43. Yeoman RR, Wolf DP, Lee DM. Coculture of monkey ovarian tissue increases survival after vitrification and slow-rate freezing. Fertil Steril 2005;83 Suppl 1:1248–1254.

    Article  PubMed  Google Scholar 

  44. Xing W, Zhou C, Bian J, Montag M, Xu Y, Li Y, et al. Solid-surface vitrification is an appropriate and convenient method for cryopreservation of isolated rat follicles. Reprod Biol Endocrinol 2010;8:42.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Vajta G, Holm P, Greve T, Callesen H. Vitrification of porcine embryos using the open pulled straw (OPS) method. Acta Vet Scand 1997;38:349–352.

    CAS  PubMed  Google Scholar 

  46. Dinnyés A, Dai Y, Jiang S, Yang X. High developmental rates of vitrified bovine oocytes following parthenogenetic activation, in vitro fertilization, and somatic cell nuclear transfer. Biol Reprod 2000;63:513–518.

    Article  PubMed  Google Scholar 

  47. von Schönfeldt V, Chandolia R, Kiesel L, Nieschlag E, Schlatt S, Sonntag B. Advanced follicle development in xenografted prepubertal ovarian tissue: the common marmoset as a nonhuman primate model for ovarian tissue transplantation. Fertil Steril 2011;95:1428–1434.

    Article  Google Scholar 

  48. Ting AY, Yeoman RR, Lawson MS, Zelinski MB. In vitro development of secondary follicles from cryopreserved rhesus macaque ovarian tissue after slow-rate freeze or vitrification. Hum Reprod 2011;26:2461–2472.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Kim KJ, Kim BG, Kim YH, Lee YA, Kim BJ, Jung SE, et al. In vitro spermatogenesis using bovine testis tissue culture techniques. Tissue Eng Regen Med 2015;5:314–323.

    Article  CAS  Google Scholar 

  50. El-Akouri RR, Mölne J, Groth K, Kurlberg G, Brännström M. Rejection patterns in allogeneic uterus transplantation in the mouse. Hum Reprod 2006;21:436–442.

    Article  PubMed  Google Scholar 

  51. Díaz-García C, Akhi SN, Wallin A, Pellicer A, Brännström M. First report on fertility after allogeneic uterus transplantation. Acta Obstet Gynecol Scand 2010;89:1491–1494.

    Article  PubMed  Google Scholar 

  52. Avison DL, DeFaria W, Tryphonopoulos P, Tekin A, Attia GR, Takahashi H, et al. Heterotopic uterus transplantation in a swine model. Transplantation 2009;88:465–469.

    Article  PubMed  Google Scholar 

  53. Hanafy A, Diaz-Garcia C, Olausson M, Brännström M. Uterine transplantation: one human case followed by a decade of experimental research in animal models. Aust N Z J Obstet Gynaecol 2011;51:199–203.

    Article  PubMed  Google Scholar 

  54. Ozkan O, Akar ME, Ozkan O, Erdogan O, Hadimioglu N, Yilmaz M, et al. Preliminary results of the first human uterus transplantation from a multiorgan donor. Fertil Steril 2013;99:470–476.

    Article  PubMed  Google Scholar 

  55. Akar ME, Ozkan O, Aydinuraz B, Dirican K, Cincik M, Mendilcioglu I, et al. Clinical pregnancy after uterus transplantation. Fertil Steril 2013;100:1358–1563.

    Article  Google Scholar 

  56. Hansen A. Swedish surgeons report world’s first uterus transplantations from mother to daughter. BMJ 2012;345:e6357.

    Article  PubMed  Google Scholar 

  57. Li X, Sun H, Lin N, Hou X, Wang J, Zhou B, et al. Regeneration of uterine horns in rats by collagen scaffolds loaded with collagen-binding human basic fibroblast growth factor. Biomaterials 2011;32:8172–8181.

    Article  CAS  PubMed  Google Scholar 

  58. Campbell GR, Turnbull G, Xiang L, Haines M, Armstrong S, Rolfe BE, et al. The peritoneal cavity as a bioreactor for tissue engineering visceral organs: bladder, uterus and vas deferens. J Tissue Eng Regen Med 2008;2:50–60.

    Article  CAS  PubMed  Google Scholar 

  59. Hellström M, El-Akouri RR, Sihlbom C, Olsson BM, Lengqvist J, Bäckdahl H, et al. Towards the development of a bioengineered uterus: comparison of different protocols for rat uterus decellularization. Acta Biomater 2014;10:5034–5042.

    Article  PubMed  CAS  Google Scholar 

  60. Wang T, Koh C, Yoo JJ. Creation of an engineered uterus for surgical reconstruction. New Orleans: American Academy of Pediatrics Section on Urology; 2003.

    Google Scholar 

  61. Song T, Zhao X, Sun H, Li X, Lin N, Ding L, et al. Regeneration of uterine horns in rats using collagen scaffolds loaded with human embryonic stem cell-derived endometrium-like cells. Tissue Eng Part A 2015;21:353–361.

    Article  PubMed  CAS  Google Scholar 

  62. House M, Sanchez CC, Rice WL, Socrate S, Kaplan DL. Cervical tissue engineering using silk scaffolds and human cervical cells. Tissue Eng Part A 2010;16:2101–2112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Mahendroo MS, Porter A, Russell DW, Word RA. The parturition defect in steroid 5alpha-reductase type 1 knockout mice is due to impaired cervical ripening. Mol Endocrinol 1999;13:981–992.

    CAS  PubMed  Google Scholar 

  64. Ji H, Dailey TL, Long V, Chien EK. Androgen-regulated cervical ripening: a structural, biomechanical, and molecular analysis. Am J Obstet Gynecol 2008;198:543. e1-e9.

  65. Simon C, Einspanier A. The hormonal induction of cervical remodeling in the common marmoset monkey (Callithrix jacchus). Reproduction 2009;137:517–525.

    Article  CAS  PubMed  Google Scholar 

  66. El Maradny E, Kanayama N, Kobayashi H, Hossain B, Khatun S, Liping S, et al. The role of hyaluronic acid as a mediator and regulator of cervical ripening. Hum Reprod 1997;12:1080–1088.

    Article  PubMed  Google Scholar 

  67. Chwalisz K, Shao-Qing S, Garfield RE, Beier HM. Cervical ripening in guinea-pigs after a local application of nitric oxide. Hum Reprod 1997;12:2093–2101.

    Article  CAS  PubMed  Google Scholar 

  68. De Filippo RE, Yoo JJ, Atala A. Engineering of vaginal tissue in vivo. Tissue Eng 2003;9:301–306.

    Article  PubMed  Google Scholar 

  69. Desai N, AbdelHafez F, Ali MY, Sayed EH, Abu-Alhassan AM, Falcone T, et al. Mouse ovarian follicle cryopreservation using vitrification or slow programmed cooling: assessment of in vitro development, maturation, ultra-structure and meiotic spindle organization. J Obstet Gynaecol Res 2011;37:1–12.

    Article  PubMed  Google Scholar 

  70. Harp R, Leibach J, Black J, Keldahl C, Karow A. Cryopreservation of murine ovarian tissue. Cryobiology 1994;31:336–343.

    Article  CAS  PubMed  Google Scholar 

  71. Jeong JH, Jin ES, Min JK, Jeon SR, Choi KH. Wnt3a-producing fibroblasts in ovariectomy-induced osteoporosis in a rat model. Tissue Eng Regen Med 2015;5:306–313.

    Article  CAS  Google Scholar 

  72. Gosden RG, Baird DT, Wade JC, Webb R. Restoration of fertility to oophorectomized sheep by ovarian autografts stored at -196 degrees C. Hum Reprod 1994;9:597–603.

    CAS  PubMed  Google Scholar 

  73. Petroianu A, de Souza Vasconcellos L, Alberti LR,Fonseca de Castro LP,Barbosa Leite JM. Natural pregnancy in rabbits that underwent oophorectomy and orthotopic allogeneic or autologous ovarian transplantation. Fertil Steril 2002;77:1298–1299.

    Article  PubMed  Google Scholar 

  74. Milenkovic M, Diaz-Garcia C, Wallin A, Brännström M. Viability and function of the cryopreserved whole rat ovary: comparison between slow-freezing and vitrification. Fertil Steril 2012;97:1176–1182.

    Article  PubMed  Google Scholar 

  75. Arav A, Revel A, Nathan Y, Bor A, Gacitua H, Yavin S, et al. Oocyte recovery, embryo development and ovarian function after cryopreservation and transplantation of whole sheep ovary. Hum Reprod 2005;20:3554–3559.

    Article  CAS  PubMed  Google Scholar 

  76. Imhof M, Bergmeister H, Lipovac M, Rudas M, Hofstetter G, Huber J. Orthotopic microvascular reanastomosis of whole cryopreserved ovine ovaries resulting in pregnancy and live birth. Fertil Steril 2006;85 Suppl 1:1208–1215.

    Article  PubMed  Google Scholar 

  77. Nicacio AC, Simões R, de Paula-Lopes FF, de Barros FR, Peres MA, Assumpção ME, et al. Effects of different cryopreservation methods on post-thaw culture conditions of in vitro produced bovine embryos. Zygote 2012;20:117–122.

    Article  CAS  PubMed  Google Scholar 

  78. Xu Z, Wang X, Wu Y, Meng Y, Wu F, Zhou N, et al. Slow-controlled freezing versus speed-cooling for cryopreservation of whole guinea pig ovaries. Theriogenology 2012;77:483–491.

    Article  PubMed  Google Scholar 

  79. Hotchkiss CE, Wang C, Slikker W Jr. Effect of prolonged ketamine exposure on cardiovascular physiology in pregnant and infant rhesus monkeys (Macaca mulatta). J Am Assoc Lab Anim Sci 2007;46:21–28.

    CAS  PubMed  Google Scholar 

  80. Young SS, Schilling AM, Skeans S, Ritacco G. Short duration anaesthesia with medetomidine and ketamine in cynomolgus monkeys. Lab Anim 1999;33:162–168.

    Article  CAS  PubMed  Google Scholar 

  81. Orsi A, Rees D, Andreini I, Venturella S, Cinelli S, Oberto G. Overview of the marmoset as a model in nonclinical development of pharmaceutical products. Regul Toxicol Pharmacol 2011;59:19–27.

    Article  CAS  PubMed  Google Scholar 

  82. Zühlke U, Weinbauer G. The common marmoset (Callithrix jacchus) as a model in toxicology. Toxicol Pathol 2003;31 Suppl:123–127.

    Article  PubMed  Google Scholar 

  83. Bernacky BJ, Gibson SV, Keeling ME, Abee CR. Nonhuman primates. In: Fox JG, Anderson LC, Loew FM, Quimby FW, editors. Laboratory animal medicine. San Diego, CA: Academic Press; 2008. p. 702–703.

    Google Scholar 

  84. Okano H, Hikishima K, Iriki A, Sasaki E. The common marmoset as a novel animal model system for biomedical and neuroscience research applications. Semin Fetal Neonatal Med 2012;17:336–340.

    Article  PubMed  Google Scholar 

  85. Mubiru JN, Garcia-Forey M, Cavazos N, Hemmat P, Dick EJ Jr, Owston MA, et al. Serum prostate specific antigen changes in cynomolgus monkeys (Macaca fascicularis) on a high sugar high fat diet. Prostate 2012;72:469–475.

    Article  CAS  PubMed  Google Scholar 

  86. Mattison JA, Roth GS, Beasley TM, Tilmont EM, Handy AM, Herbert RL, et al. Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 2012;489:318–321.

    Article  CAS  PubMed  Google Scholar 

  87. Weinbauer GF, Niehoff M, Niehaus M, Srivastav S, Fuchs A, Van Esch E, et al. Physiology and endocrinology of the ovarian cycle in macaques. Toxicol Pathol 2008;36:7S-23S.

  88. Trisomboon H, Malaivijitnond S, Cherdshewasart W, Watanabe G, Taya K. Effect of Pueraria mirifica on the sexual skin coloration of aged menopausal cynomolgus monkeys. J Reprod Dev 2006;52:537–542.

    Article  PubMed  Google Scholar 

  89. Waitt C, Gerald MS, Little AC, Kraiselburd E. Selective attention toward female secondary sexual color in male rhesus macaques. Am J Primatol 2006;68:738–744.

    Article  PubMed  Google Scholar 

  90. Committee for the Update of the Guide for the Care and Use of Laboratory Animals, Institute for Laboratory Animal Research, Division on Earth and Life Studies, National Research Council. Guide for the care and use of laboratory animals. 8th ed. Washington, DC: National Academies Press; 2011.

    Google Scholar 

  91. Gottlieb DH, Ghirardo S, Minier DE, Sharpe N, Tatum L, McCowan B. Efficacy of 3 types of foraging enrichment for rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci 2011;50:888–894.

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Mahmud N, Klipa D, Ahsan N. Antibody immunosuppressive therapy in solid-organ transplant: Part I. MAbs 2010;2:148–156.

    Article  PubMed  PubMed Central  Google Scholar 

  93. Kisu I, Mihara M, Banno K, Hara H, Masugi Y, Araki J, et al. Uterus allotransplantation in cynomolgus macaque: a preliminary experience with non-human primate models. J Obstet Gynaecol Res 2014;40:907–918.

    Article  CAS  PubMed  Google Scholar 

  94. Calne RY, Rolles K, White DJ, Thiru S, Evans DB, McMaster P, et al. Cyclosporin A initially as the only immunosuppressant in 34 recipients of cadaveric organs: 32 kidneys, 2 pancreases, and 2 livers. Lancet 1979;2:1033–1036.

    Article  CAS  PubMed  Google Scholar 

  95. Kholkute SD, Katkam RR, Nandedkar TD, Puri CP. Leukaemia inhibitory factor in the endometrium of the common marmoset Callithrix jacchus: localization, expression and hormonal regulation. Mol Hum Reprod 2000;6:337–343.

    Article  CAS  PubMed  Google Scholar 

  96. Hackelöer BJ. The role of ultrasound in female infertility management. Ultrasound Med Biol 1984;10:35–50.

    Article  PubMed  Google Scholar 

  97. Martin LD, Dissen GA, McPike MJ, Brambrink AM. Effects of anesthesia with isoflurane, ketamine, or propofol on physiologic parameters in neonatal rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci 2014;53:290–300.

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Bergman SA. Ketamine: review of its pharmacology and its use in pediatric anesthesia. Anesth Prog 1999;46:10–20.

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Eger EI 2nd. Characteristics of anesthetic agents used for induction and maintenance of general anesthesia. Am J Health Syst Pharm 2004;61 Suppl 4:S3–S10.

    CAS  PubMed  Google Scholar 

  100. Authier S, Chaurand F, Legaspi M, Breault C, Troncy E. Comparison of three anesthetic protocols for intraduodenal drug administration using endoscopy in rhesus monkeys (Macaca mulatta). J Am Assoc Lab Anim Sci 2006;45:73–79.

    CAS  PubMed  Google Scholar 

  101. Spencer TE, Dunlap KA, Filant J. Comparative developmental biology of the uterus: insights into mechanisms and developmental disruption. Mol Cell Endocrinol 2012;354:34–53.

    Article  CAS  PubMed  Google Scholar 

  102. Enskog A, Johannesson L, Chai DC, Dahm-Kähler P, Marcickiewicz J, Nyachieo A, et al. Uterus transplantation in the baboon: methodology and long-term function after auto-transplantation. Hum Reprod 2010;25:1980–1987.

    Article  CAS  PubMed  Google Scholar 

  103. Johannesson L, Enskog A, Dahm-Kähler P, Hanafy A, Chai DC, Mwenda JM, et al. Uterus transplantation in a non-human primate: long-term follow-up after autologous transplantation. Hum Reprod 2012;27:1640–1648.

    Article  CAS  PubMed  Google Scholar 

  104. Kisu I, Mihara M, Banno K, Hara H, Yamamoto T, Araki J, et al. A new surgical technique of uterine auto-transplantation in cynomolgus monkey: preliminary report about two cases. Arch Gynecol Obstet 2012;285:129–137.

    Article  PubMed  Google Scholar 

  105. Ramirez ER, Ramirez Nessetti DK, Nessetti MB, Khatamee M, Wolfson MR, Shaffer TH, et al. Pregnancy and outcome of uterine allotransplantation and assisted reproduction in sheep. J Minim Invasive Gynecol 2011;18:238–245.

    Article  PubMed  Google Scholar 

  106. Johannesson L, Enskog A, Mölne J, Diaz-Garcia C, Hanafy A, Dahm-Kähler P, et al. Preclinical report on allogeneic uterus transplantation in non-human primates. Hum Reprod 2013;28:189–198.

    Article  CAS  PubMed  Google Scholar 

  107. Del Priore G, Schlatt S, Malanowska-Stega J. Uterus transplant techniques in primates: 10 years’ experience. Exp Clin Transplant 2008;6:87–94.

    PubMed  Google Scholar 

  108. von Schönfeldt V, Chandolia R, Ochsenkühn R, Nieschlag E, Kiesel L, Sonntag B. FSH prevents depletion of the resting follicle pool by promoting follicular number and morphology in fresh and cryopreserved primate ovarian tissues following xenografting. Reprod Biol Endocrinol 2012;10:98.

    Article  CAS  Google Scholar 

  109. Candy CJ, Wood MJ, Whittingham DG. Follicular development in cryopreserved marmoset ovarian tissue after transplantation. Hum Reprod 1995;10:2334–2338.

    Article  CAS  PubMed  Google Scholar 

  110. Lee DM, Yeoman RR, Battaglia DE, Stouffer RL, Zelinski-Wooten MB, Fanton JW, et al. Live birth after ovarian tissue transplant. Nature 2004;428:137–138.

    Article  CAS  PubMed  Google Scholar 

  111. Schnorr J, Oehninger S, Toner J, Hsiu J, Lanzendorf S, Williams R, et al. Functional studies of subcutaneous ovarian transplants in non-human primates: steroidogenesis, endometrial development, ovulation, menstrual patterns and gamete morphology. Hum Reprod 2002;17:612–619.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Byeong-Cheol Kang or Seung-Yup Ku.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yun, JW., Kim, Y.Y., Ahn, J.H. et al. Use of nonhuman primates for the development of bioengineered female reproductive organs. Tissue Eng Regen Med 13, 323–334 (2016). https://doi.org/10.1007/s13770-016-9091-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13770-016-9091-4

Key Words

Navigation