1932

Abstract

Chemo- and radiation therapies used to treat cancer can have the unintended effect of making patients infertile. Clinically established fertility preservation methods, such as egg and embryo cryopreservation, are not applicable to all patients, which has motivated the development of strategies that involve ovarian tissue removal and cryopreservation before the first sterilizing treatment. To restore fertility at a later date, the early-stage follicles present in the tissue must be matured to produce functional oocytes, a process that is not possible using existing cell culture technologies. This review describes the application of tissue engineering principles to promote ovarian follicle maturation and produce mature oocytes through either in vitro culture or transplantation. The design principles for these engineered systems are presented, along with identification of emerging opportunities in reproductive biology.

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2014-07-11
2024-04-29
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Literature Cited

  1. Adamson GD, Tabangin M, Macaluso M, de Mouzon J. 1.  2013. The number of babies born globally after treatment with the assisted reproductive technologies (ART). Fertil. Steril. 100:Suppl.S42 [Google Scholar]
  2. Nieman CL, Kazer R, Brannigan RE, Zoloth LS, Chase-Lansdale PL. 2.  et al. 2006. Cancer survivors and infertility: a review of a new problem and novel answers. J. Support. Oncol. 4:171–78 [Google Scholar]
  3. Jeruss JS, Woodruff TK. 3.  2009. Preservation of fertility in patients with cancer. N. Engl. J. Med. 360:902–11 [Google Scholar]
  4. Anderson RA, Themmen AP, Al-Qahtani A, Groome NP, Cameron DA. 4.  2006. The effects of chemotherapy and long-term gonadotrophin suppression on the ovarian reserve in premenopausal women with breast cancer. Hum. Reprod. 21:2583–92 [Google Scholar]
  5. Meirow D, Nugent D. 5.  2001. The effects of radiotherapy and chemotherapy on female reproduction. Hum. Reprod. Update 7:535–43 [Google Scholar]
  6. Natl. Cancer Inst 2012. SEER data, 1973–2010. Surveillance, Epidemiology, and End Results (SEER) Program. http://seer.cancer.gov/data
  7. Schover LR, Rybicki LA, Martin BA, Bringelsen KA. 7.  1999. Having children after cancer. A pilot survey of survivors' attitudes and experiences. Cancer 86:697–709 [Google Scholar]
  8. Gosden RG. 8.  2005. Prospects for oocyte banking and in vitro maturation. J. Natl. Cancer Inst. Monogr. 2005:60–63 [Google Scholar]
  9. Ata B, Chian RC, Tan SL. 9.  2010. Cryopreservation of oocytes and embryos for fertility preservation for female cancer patients. Best Pract. Res. Clin. Obstet. Gynaecol. 24:101–12 [Google Scholar]
  10. Loren AW, Mangu PB, Beck LN, Brennan L, Magdalinski AJ. 10.  et al. 2013. Fertility preservation for patients with cancer: American Society of Clinical Oncology clinical practice guideline update. J. Clin. Oncol. 31:2500–10 [Google Scholar]
  11. Oktay K. 11.  2013. Fertility preservation: We are in this for a long haul. Am. J. Obstet. Gynecol. 209:77–79 [Google Scholar]
  12. Siegelmann-Danieli N, Tamir A, Zohar H, Papa MZ, Chetver LL. 12.  et al. 2003. Breast cancer in women with recent exposure to fertility medications is associated with poor prognostic features. Ann. Surg. Oncol. 10:1031–38 [Google Scholar]
  13. Malloch L, Rhoton-Vlasak A. 13.  2013. An assessment of current clinical attitudes toward letrozole use in reproductive endocrinology practices. Fertil. Steril. 100:1740–44 [Google Scholar]
  14. Davis VJ. 14.  2006. Female gamete preservation. Cancer 107:1690–94 [Google Scholar]
  15. Silber S, Kagawa N, Kuwayama M, Gosden RG. 15.  2010. Duration of fertility after fresh and frozen ovary transplantation. Fertil. Steril. 94:2191–96 [Google Scholar]
  16. Donnez J, Dolmans MM, Pellicer A, Diaz-Garcia C, Sanchez Serrano M. 16.  et al. 2013. Restoration of ovarian activity and pregnancy after transplantation of cryopreserved ovarian tissue: a review of 60 cases of reimplantation. Fertil. Steril. 99:1503–13 [Google Scholar]
  17. Silber SJ, DeRosa M, Pineda J, Lenahan K, Grenia D. 17.  et al. 2008. A series of monozygotic twins discordant for ovarian failure: ovary transplantation (cortical versus microvascular) and cryopreservation. Hum. Reprod. 23:1531–37 [Google Scholar]
  18. Ahn RW, Barrett SL, Raja MR, Jozefik JK, Spaho L. 18.  et al. 2013. Nano-encapsulation of arsenic trioxide enhances efficacy against murine lymphoma model while minimizing its impact on ovarian reserve in vitro and in vivo. PLoS ONE 8:e58491 [Google Scholar]
  19. Constine LS, Woolf PD, Cann D, Mick G, McCormick K. 19.  et al. 1993. Hypothalamic-pituitary dysfunction after radiation for brain tumors. N. Engl. J. Med. 328:87–94 [Google Scholar]
  20. Woods DC, Tilly JL. 20.  2013. Isolation, characterization and propagation of mitotically active germ cells from adult mouse and human ovaries. Nat. Protoc. 8:966–88 [Google Scholar]
  21. Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M. 21.  2011. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146:519–32 [Google Scholar]
  22. Tingen C, Kim A, Woodruff TK. 22.  2009. The primordial pool of follicles and nest breakdown in mammalian ovaries. Mol. Hum. Reprod. 15:795–803 [Google Scholar]
  23. Martinovitch PN. 23.  1938. The development in vitro of the mammalian gonad: ovary and ovogenesis. Proc. R. Soc. Ser. B 125:232–49 [Google Scholar]
  24. Eppig JJ. 24.  1977. Mouse oocyte development in vitro with various culture systems. Dev. Biol. 60:371–88 [Google Scholar]
  25. Eppig JJ, Schroeder AC. 25.  1989. Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol. Reprod. 41:268–76 [Google Scholar]
  26. Cortvrindt R, Smitz J, Van Steirteghem AC. 26.  1996. In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simplified culture system. Hum. Reprod. 11:2656–66 [Google Scholar]
  27. Telfer EE, Zelinski MB. 27.  2013. Ovarian follicle culture: advances and challenges for human and nonhuman primates. Fertil. Steril. 99:1523–33 [Google Scholar]
  28. Smitz J, Dolmans MM, Donnez J, Fortune JE, Hovatta O. 28.  et al. 2010. Current achievements and future research directions in ovarian tissue culture, in vitro follicle development and transplantation: implications for fertility preservation. Hum. Reprod. Update 16:395–414 [Google Scholar]
  29. Bhattacharya P, Keating AF. 29.  2012. Impact of environmental exposures on ovarian function and role of xenobiotic metabolism during ovotoxicity. Toxicol. Appl. Pharmacol. 261:227–35 [Google Scholar]
  30. Eppig JJ, O'Brien MJ. 30.  1996. Development in vitro of mouse oocytes from primordial follicles. Biol. Reprod. 54:197–207 [Google Scholar]
  31. O'Brien MJ, Pendola JK, Eppig JJ. 31.  2003. A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol. Reprod. 68:1682–86 [Google Scholar]
  32. Xu J, Lawson MS, Yeoman RR, Molskness TA, Ting AY. 32.  et al. 2013. Fibrin promotes development and function of macaque primary follicles during encapsulated three-dimensional culture. Hum. Reprod. 28:2187–200 [Google Scholar]
  33. Tambe SS, Nandedkar TD. 33.  1993. Steroidogenesis in sheep ovarian antral follicles in culture: time course study and supplementation with a precursor. Steroids 58:379–83 [Google Scholar]
  34. Roy SK, Treacy BJ. 34.  1993. Isolation and long-term culture of human preantral follicles. Fertil. Steril. 59:783–90 [Google Scholar]
  35. Ksiazkiewicz LK. 35.  2006. Recent achievements in in vitro culture and preservation of ovarian follicles in mammals. Reprod. Biol. 6:3–16 [Google Scholar]
  36. Woodruff TK, Shea LD. 36.  2007. The role of the extracellular matrix in ovarian follicle development. Reprod. Sci. 14:6–10 [Google Scholar]
  37. Lenie S, Cortvrindt R, Adriaenssens T, Smitz J. 37.  2004. A reproducible two-step culture system for isolated primary mouse ovarian follicles as single functional units. Biol. Reprod. 71:1730–38 [Google Scholar]
  38. West-Farrell ER, Xu M, Gomberg MA, Chow YH, Woodruff TK, Shea LD. 38.  2009. The mouse follicle microenvironment regulates antrum formation and steroid production: alterations in gene expression profiles. Biol. Reprod. 80:432–39 [Google Scholar]
  39. Kreeger PK, Woodruff TK, Shea LD. 39.  2003. Murine granulosa cell morphology and function are regulated by a synthetic Arg-Gly-Asp matrix. Mol. Cell. Endocrinol. 205:1–10 [Google Scholar]
  40. Lenie S, Cortvrindt R, Eichenlaub-Ritter U, Smitz J. 40.  2008. Continuous exposure to bisphenol A during in vitro follicular development induces meiotic abnormalities. Mutat. Res. 651:71–81 [Google Scholar]
  41. Paulose T, Tannenbaum LV, Borgeest C, Flaws JA. 41.  2012. Methoxychlor-induced ovarian follicle toxicity in mice: dose and exposure duration-dependent effects. Birth Defects Res. B Dev. Reprod. Toxicol. 95:219–24 [Google Scholar]
  42. Pangas SA, Saudye H, Shea LD, Woodruff TK. 42.  2003. Novel approach for the three-dimensional culture of granulosa cell-oocyte complexes. Tissue Eng. 9:1013–21 [Google Scholar]
  43. Amsden B, Turner N. 43.  1999. Diffusion characteristics of calcium alginate gels. Biotechnol. Bioeng. 65:605–10 [Google Scholar]
  44. Wee S, Gombotz WR. 44.  1998. Protein release from alginate matrices. Adv. Drug Deliv. Rev. 31:267–85 [Google Scholar]
  45. Machluf M, Carroll RS. 45.  2003. Cell-based delivery systems for antiangiogenic therapy. Biotechnol. Genet. Eng. Rev. 20:183–95 [Google Scholar]
  46. Wang L, Shansky J, Borselli C, Mooney D, Vandenburgh H. 46.  2012. Design and fabrication of a biodegradable, covalently crosslinked shape-memory alginate scaffold for cell and growth factor delivery. Tissue Eng. Part A 18:2000–7 [Google Scholar]
  47. Tanaka H, Matsumura M, Veliky IA. 47.  1984. Diffusion characteristics of substrates in Ca-alginate gel beads. Biotechnol. Bioeng. 26:53–58 [Google Scholar]
  48. Barrett SL, Albertini DF. 48.  2007. Allocation of γ-tubulin between oocyte cortex and meiotic spindle influences asymmetric cytokinesis in the mouse oocyte. Biol. Reprod. 76:949–57 [Google Scholar]
  49. Kreeger PK, Deck JW, Woodruff TK, Shea LD. 49.  2006. The in vitro regulation of ovarian follicle development using alginate-extracellular matrix gels. Biomaterials 27:714–23 [Google Scholar]
  50. Parrish EM, Siletz A, Xu M, Woodruff TK, Shea LD. 50.  2011. Gene expression in mouse ovarian follicle development in vivo versus an ex vivo alginate culture system. Reproduction 142:309–18 [Google Scholar]
  51. Xu M, Kreeger PK, Shea LD, Woodruff TK. 51.  2006. Tissue-engineered follicles produce live, fertile offspring. Tissue Eng. 12:2739–46 [Google Scholar]
  52. Xu M, West E, Shea LD, Woodruff TK. 52.  2006. Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development. Biol. Reprod. 75:916–23 [Google Scholar]
  53. West ER, Xu M, Woodruff TK, Shea LD. 53.  2007. Physical properties of alginate hydrogels and their effects on in vitro follicle development. Biomaterials 28:4439–48 [Google Scholar]
  54. Torrance C, Telfer E, Gosden RG. 54.  1989. Quantitative study of the development of isolated mouse pre-antral follicles in collagen gel culture. J. Reprod. Fertil. 87:367–74 [Google Scholar]
  55. Sharma GT, Dubey PK, Meur SK. 55.  2009. Survival and developmental competence of buffalo preantral follicles using three-dimensional collagen gel culture system. Anim. Reprod. Sci. 114:115–24 [Google Scholar]
  56. Shikanov A, Xu M, Woodruff T, Shea L. 56.  2009. Interpenetrating fibrin–alginate matrices for in vitro ovarian follicle development. Biomaterials 30:5476–85 [Google Scholar]
  57. Shikanov A, Xu M, Woodruff TK, Shea LD. 57.  2011. A method for ovarian follicle encapsulation and culture in a proteolytically degradable 3 dimensional system. J. Vis. Exp. 2011:492695 doi: 10.3791/2695 [Google Scholar]
  58. Sperling LH, Mishra V. 58.  1996. The current status of interpenetrating polymer networks. Polym. Adv. Technol. 7:197–208 [Google Scholar]
  59. Rowe SL, Stegemann JP. 59.  2006. Interpenetrating collagen-fibrin composite matrices with varying protein contents and ratios. Biomacromolecules 7:2942–48 [Google Scholar]
  60. Kraehenbuehl TP, Zammaretti P, Van der Vlies AJ, Schoenmakers RG, Lutolf MP. 60.  et al. 2008. Three-dimensional extracellular matrix-directed cardioprogenitor differentiation: systematic modulation of a synthetic cell-responsive PEG-hydrogel. Biomaterials 29:2757–66 [Google Scholar]
  61. Shikanov A, Smith RM, Xu M, Woodruff TK, Shea LD. 61.  2011. Hydrogel network design using multifunctional macromers to coordinate tissue maturation in ovarian follicle culture. Biomaterials 32:2524–31 [Google Scholar]
  62. Jin SY, Lei L, Shikanov A, Shea LD, Woodruff TK. 62.  2010. A novel two-step strategy for in vitro culture of early-stage ovarian follicles in the mouse. Fertil. Steril. 93:2633–39 [Google Scholar]
  63. Nilsson EE, Savenkova MI, Schindler R, Zhang B, Schadt EE, Skinner MK. 63.  2010. Gene bionetwork analysis of ovarian primordial follicle development. PLoS ONE 5:e11637 [Google Scholar]
  64. Osborn SM, Gook DA, Stern C, Speirs AL. 64.  1997. The isolation and culture of human primordial follicles from fresh ovarian tissue. Hum. Reprod. 12:Suppl1153 [Google Scholar]
  65. Tingen CM, Kiesewetter SE, Jozefik J, Thomas C, Tagler D. 65.  et al. 2011. A macrophage and theca cell-enriched stromal cell population influences growth and survival of immature murine follicles in vitro. Reproduction 141:809–20 [Google Scholar]
  66. Tagler D, Tu T, Smith RM, Anderson NR, Tingen CM. 66.  et al. 2012. Embryonic fibroblasts enable the culture of primary ovarian follicles within alginate hydrogels. Tissue Eng. Part A 18:1229–38 [Google Scholar]
  67. Tagler D, Makanji Y, Anderson NR, Woodruff TK, Shea LD. 67.  2013. Supplemented αMEM/F12-based medium enables the survival and growth of primary ovarian follicles encapsulated in alginate hydrogels. Biotechnol. Bioeng. 110:3258–68 [Google Scholar]
  68. Gutierrez CG, Ralph JH, Telfer EE, Wilmut I, Webb R. 68.  2000. Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biol. Reprod. 62:1322–28 [Google Scholar]
  69. McLaughlin M, Bromfield JJ, Albertini DF, Telfer EE. 69.  2010. Activin promotes follicular integrity and oogenesis in cultured pre-antral bovine follicles. Mol. Hum. Reprod. 16:644–53 [Google Scholar]
  70. Jewgenow K, Paris MC. 70.  2006. Preservation of female germ cells from ovaries of cat species. Theriogenology 66:93–100 [Google Scholar]
  71. Songsasen N, Woodruff TK, Wildt DE. 71.  2011. In vitro growth and steroidogenesis of dog follicles are influenced by the physical and hormonal microenvironment. Reproduction 142:113–22 [Google Scholar]
  72. Xu M, Fazleabas AT, Shikanov A, Jackson E, Barrett SL. 72.  et al. 2011. In vitro oocyte maturation and preantral follicle culture from the luteal-phase baboon ovary produce mature oocytes. Biol. Reprod. 84:689–97 [Google Scholar]
  73. Xu M, West-Farrell ER, Stouffer RL, Shea LD, Woodruff TK, Zelinski MB. 73.  2009. Encapsulated three-dimensional culture supports development of nonhuman primate secondary follicles. Biol. Reprod. 81:587–94 [Google Scholar]
  74. Hornick JE, Duncan FE, Shea LD, Woodruff TK. 74.  2012. Isolated primate primordial follicles require a rigid physical environment to survive and grow in vitro. Hum. Reprod. 27:1801–10 [Google Scholar]
  75. Xu M, Barrett SL, West-Farrell E, Kondapalli LA, Kiesewetter SE. 75.  et al. 2009. In vitro grown human ovarian follicles from cancer patients support oocyte growth. Hum. Reprod. 24:2531–40 [Google Scholar]
  76. Azziz R, Carmina E, Dewailly D, Diamanti-Kandarakis E, Escobar-Morreale HF. 76.  et al. 2009. The Androgen Excess and PCOS Society criteria for the polycystic ovary syndrome: the complete task force report. Fertil. Steril. 91:456–88 [Google Scholar]
  77. Michelmore KF, Balen AH, Dunger DB, Vessey MP. 77.  1999. Polycystic ovaries and associated clinical and biochemical features in young women. Clin. Endocrinol.(Oxf.) 51:779–86 [Google Scholar]
  78. Michelmore KF. 78.  2000. Polycystic ovary syndrome in adolescence and early adulthood. Hum. Fertil.(Camb.) 3:96–100 [Google Scholar]
  79. Woodruff TK, Shea LD. 79.  2011. A new hypothesis regarding ovarian follicle development: ovarian rigidity as a regulator of selection and health. J. Assist. Reprod. Genet. 28:3–6 [Google Scholar]
  80. Nelson SM, Fleming R. 80.  2007. Obesity and reproduction: impact and interventions. Curr. Opin. Obstet. Gynecol. 19:384–89 [Google Scholar]
  81. Lintsen AM, Pasker–de Jong PC, de Boer EJ, Burger CW, Jansen CA. 81.  et al. 2005. Effects of subfertility cause, smoking and body weight on the success rate of IVF. Hum. Reprod. 20:1867–75 [Google Scholar]
  82. Robker RL. 82.  2008. Evidence that obesity alters the quality of oocytes and embryos. Pathophysiology 15:115–21 [Google Scholar]
  83. Purcell SH, Moley KH. 83.  2011. The impact of obesity on egg quality. J. Assist. Reprod. Genet. 28:517–24 [Google Scholar]
  84. Broekmans FJ, Soules MR, Fauser BC. 84.  2009. Ovarian aging: mechanisms and clinical consequences. Endocr. Rev. 30:465–93 [Google Scholar]
  85. Hirshfeld-Cytron JE, Duncan FE, Xu M, Jozefik JK, Shea LD, Woodruff TK. 85.  2011. Animal age, weight and estrus cycle stage impact the quality of in vitro grown follicles. Hum. Reprod. 26:2473–85 [Google Scholar]
  86. Teissier MP, Chable H, Paulhac S, Aubard Y. 86.  2000. Comparison of follicle steroidogenesis from normal and polycystic ovaries in women undergoing IVF: relationship between steroid concentrations, follicle size, oocyte quality and fecundability. Hum. Reprod. 15:2471–77 [Google Scholar]
  87. Malizia BA, Hacker MR, Penzias AS. 87.  2009. Cumulative live-birth rates after in vitro fertilization. N. Engl. J. Med. 360:236–43 [Google Scholar]
  88. Hassold T, Hunt P. 88.  2001. To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2:280–91 [Google Scholar]
  89. Duncan FE, Chiang T, Schultz RM, Lampson MA. 89.  2009. Evidence that a defective spindle assembly checkpoint is not the primary cause of maternal age-associated aneuploidy in mouse eggs. Biol. Reprod. 81:768–76 [Google Scholar]
  90. Pan H, Ma P, Zhu W, Schultz RM. 90.  2008. Age-associated increase in aneuploidy and changes in gene expression in mouse eggs. Dev. Biol. 316:397–407 [Google Scholar]
  91. Duncan FE, Hornick JE, Lampson MA, Schultz RM, Shea LD, Woodruff TK. 91.  2012. Chromosome cohesion decreases in human eggs with advanced maternal age. Aging Cell 11:1121–24 [Google Scholar]
  92. Hunt P, Hassold T. 92.  2010. Female meiosis: coming unglued with age. Curr. Biol. 20:R699–702 [Google Scholar]
  93. Hornick JE, Duncan FE, Shea LD, Woodruff TK. 93.  2013. Multiple follicle culture supports primary follicle growth through paracrine-acting signals. Reproduction 145:19–32 [Google Scholar]
  94. Silber SJ, Lenahan KM, Levine DJ, Pineda JA, Gorman KS. 94.  et al. 2005. Ovarian transplantation between monozygotic twins discordant for premature ovarian failure. N. Engl. J. Med. 353:58–63 [Google Scholar]
  95. Donnez J. 95.  2013. Introduction. Fertility preservation, from cancer to benign disease to social reasons: the challenge of the present decade. Fertil. Steril. 99:1467–68 [Google Scholar]
  96. Gosden RG. 96.  2008. Ovary and uterus transplantation. Reproduction 136:671–80 [Google Scholar]
  97. Ting AY, Yeoman RR, Lawson MS, Zelinski MB. 97.  2011. In vitro development of secondary follicles from cryopreserved rhesus macaque ovarian tissue after slow-rate freeze or vitrification. Hum. Reprod. 26:2461–72 [Google Scholar]
  98. Nisolle M, Casanas-Roux F, Qu J, Motta P, Donnez J. 98.  2000. Histologic and ultrastructural evaluation of fresh and frozen-thawed human ovarian xenografts in nude mice. Fertil. Steril. 74:122–29 [Google Scholar]
  99. Shikanov A, Zhang Z, Xu M, Smith RM, Rajan A. 99.  et al. 2011. Fibrin encapsulation and vascular endothelial growth factor delivery promotes ovarian graft survival in mice. Tissue Eng. Part A 17:3095–104 [Google Scholar]
  100. Dolmans MM, Luyckx V, Donnez J, Andersen CY, Greve T. 100.  2013. Risk of transferring malignant cells with transplanted frozen-thawed ovarian tissue. Fertil. Steril. 99:1514–22 [Google Scholar]
  101. Dolmans MM, Marinescu C, Saussoy P, Van Langendonckt A, Amorim C, Donnez J. 101.  2010. Reimplantation of cryopreserved ovarian tissue from patients with acute lymphoblastic leukemia is potentially unsafe. Blood 116:2908–14 [Google Scholar]
  102. Poirot CJ, Martelli H, Genestie C, Golmard JL, Valteau-Couanet D. 102.  et al. 2007. Feasibility of ovarian tissue cryopreservation for prepubertal females with cancer. Pediatr. Blood Cancer 49:74–78 [Google Scholar]
  103. Demeestere I, Simon P, Emiliani S, Delbaere A, Englert Y. 103.  2007. Fertility preservation: successful transplantation of cryopreserved ovarian tissue in a young patient previously treated for Hodgkin's disease. Oncologist 12:1437–42 [Google Scholar]
  104. Vanacker J, Luyckx V, Dolmans MM, Des Rieux A, Jaeger J. 104.  et al. 2012. Transplantation of an alginate-matrigel matrix containing isolated ovarian cells: first step in developing a biodegradable scaffold to transplant isolated preantral follicles and ovarian cells. Biomaterials 33:6079–85 [Google Scholar]
  105. Gosden RG. 105.  1990. Restitution of fertility in sterilized mice by transferring primordial ovarian follicles. Hum. Reprod. 5:499–504 [Google Scholar]
  106. Smith RM, Shikanov A, Kniazeva E, Ramadurai D, Woodruff TK, Shea LD. 105a.  2014. Fibrin-mediated delivery of an ovarian follicle pool in a mouse model of infertility. Tissue Eng. Part A. In press
  107. Sittadjody S, Saul JM, Joo S, Yoo JJ, Atala A, Opara EC. 106.  2013. Engineered multilayer ovarian tissue that secretes sex steroids and peptide hormones in response to gonadotropins. Biomaterials 34:2412–20 [Google Scholar]
  108. Krotz SP, Robins JC, Ferruccio TM, Moore R, Steinhoff MM. 107.  et al. 2010. In vitro maturation of oocytes via the pre-fabricated self-assembled artificial human ovary. J. Assist. Reprod. Genet. 27:743–50 [Google Scholar]
  109. Reineeke I, Deuflhard PA. 108.  2007. A complex mathematical model of the human menstrual cycle. J. Theor. Biol. 247:303–30 [Google Scholar]
  110. Clement F, Monniaux D, Stark J, Hardy K, Thalabard JC. 109.  et al. 2001. Mathematical model of FSH-induced cAMP production in ovarian follicles. Am. J. Physiol. Endocrinol. Metab. 281:E35–53 [Google Scholar]
  111. Redding GP, Bronlund JE, Hart AL. 110.  2007. Mathematical modelling of oxygen transport-limited follicle growth. Reproduction 133:1095–106 [Google Scholar]
  112. Wallace WH, Kelsey TW. 111.  2010. Human ovarian reserve from conception to the menopause. PLoS ONE 5:e8772 [Google Scholar]
  113. Echenim N, Monniaux D, Sorine M, Clement F. 112.  2005. Multi-scale modeling of the follicle selection process in the ovary. Math. Biosci. 198:57–79 [Google Scholar]
  114. Bristol-Gould SK, Kreeger PK, Selkirk CG, Kilen SM, Cook RW. 113.  et al. 2006. Postnatal regulation of germ cells by activin: the establishment of the initial follicle pool. Dev. Biol. 298:132–48 [Google Scholar]
  115. Lawrence ND, Girolami M, Rattray M, Sanguinetti G. 114.  2010. Learning and Inference in Computational Systems Biology Cambridge, MA: MIT Press
  116. Memili E, Peddinti D, Shack LA, Nanduri B, McCarthy F. 115.  et al. 2007. Bovine germinal vesicle oocyte and cumulus cell proteomics. Reproduction 133:1107–20 [Google Scholar]
  117. Peddinti D, Memili E, Burgess SC. 116.  2010. Proteomics-based systems biology modeling of bovine germinal vesicle stage oocyte and cumulus cell interaction. PLoS ONE 5:e11240 [Google Scholar]
  118. Revelli A, Delle Piane L, Casano S, Molinari E, Massobrio M, Rinaudo P. 117.  2009. Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics. Reprod. Biol. Endocrinol. 7:40 doi: 10.1186/1477-7827-7-40 [Google Scholar]
  119. Vanselow J, Spitschak M, Nimz M, Furbass R. 118.  2010. DNA methylation is not involved in preovulatory down-regulation of CYP11A1, HSD3B1, and CYP19A1 in bovine follicles but may have a role in permanent silencing of CYP19A1 in large granulosa lutein cells. Biol. Reprod. 82:289–98 [Google Scholar]
  120. Hasegawa A, Kumamoto K, Mochida N, Komori S, Koyama K. 119.  2009. Gene expression profile during ovarian folliculogenesis. J. Reprod. Immunol. 83:40–44 [Google Scholar]
  121. Yoon SJ, Kim KH, Chung HM, Choi DH, Lee WS. 120.  et al. 2006. Gene expression profiling of early follicular development in primordial, primary, and secondary follicles. Fertil. Steril. 85:193–203 [Google Scholar]
  122. Pan H, O'Brien MJ, Wigglesworth K, Eppig JJ, Schultz RM. 121.  2005. Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev. Biol. 286:493–506 [Google Scholar]
  123. Skinner MK, Schmidt M, Savenkova MI, Sadler-Riggleman I, Nilsson EE. 122.  2008. Regulation of granulosa and theca cell transcriptomes during ovarian antral follicle development. Mol. Reprod. Dev. 75:1457–72 [Google Scholar]
  124. Sasson R, Dantes A, Tajima K, Amsterdam A. 123.  2003. Novel genes modulated by FSH in normal and immortalized FSH-responsive cells: new insights into the mechanism of FSH action. FASEB J. 17:1256–66 [Google Scholar]
  125. Sriraman V, Rudd MD, Lohmann SM, Mulders SM, Richards JS. 124.  2006. Cyclic guanosine 5′-monophosphate-dependent protein kinase II is induced by luteinizing hormone and progesterone receptor-dependent mechanisms in granulosa cells and cumulus oocyte complexes of ovulating follicles. Mol. Endocrinol. 20:348–61 [Google Scholar]
  126. Chin KV, Seifer DB, Feng B, Lin Y, Shih WC. 125.  2002. DNA microarray analysis of the expression profiles of luteinized granulosa cells as a function of ovarian reserve. Fertil. Steril. 77:1214–18 [Google Scholar]
  127. Hernandez-Gonzalez I, Gonzalez-Robayna I, Shimada M, Wayne CM, Ochsner SA. 126.  et al. 2006. Gene expression profiles of cumulus cell oocyte complexes during ovulation reveal cumulus cells express neuronal and immune-related genes: Does this expand their role in the ovulation process?. Mol. Endocrinol. 20:1300–21 [Google Scholar]
  128. Wood JR, Nelson VL, Ho C, Jansen E, Wang CY. 127.  et al. 2003. The molecular phenotype of polycystic ovary syndrome (PCOS) theca cells and new candidate PCOS genes defined by microarray analysis. J. Biol. Chem. 278:26380–90 [Google Scholar]
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