Therapeutic Potential of In Vitro–Derived Oocytes for the Restoration and Treatment of Female Fertility

Literature Cited

1. 1. 

   Picton HM, Harris SE, Muruvi W, Chambers EL 2008. The in vitro growth and maturation of follicles. Reproduction 136:703–15
   [Google Scholar]
2. 2. 

   Guzel Y, Oktem O. 2017. Understanding follicle growth in vitro: Are we getting closer to obtaining mature oocytes from in vitro-grown follicles in human?. Mol. Reprod. Dev. 84:544–59
   [Google Scholar]
3. 3. 

   Yang Q, Zhu L, Jin L 2020. Human follicle in vitro culture including activation, growth, and maturation: a review of research progress. . Front. Endocrinol. 11:548
   [Google Scholar]
4. 4. 

   Telfer EE, Andersen CY. 2021. In vitro growth and maturation of primordial follicles and immature oocytes. Fertil. Steril. 115:1116–25
   [Google Scholar]
5. 5. 

   Picton HM. 2018. Preservation of female fertility in humans and animal species. Anim. Reprod. 15:301–9
   [Google Scholar]
6. 6. 

   Campos LB, Praxedes ÉCG, Saraiva MVA, Comizzoli P, Silva AR 2019. Advances and challenges of using ovarian preantral follicles to develop biobanks of wild mammals. Biopreserv. Biobank. 17:334–41
   [Google Scholar]
7. 7. 

   Figueiredo JR, Cadenas J, Lima LF, Santos RR. 2018. Advances in in vitro folliculogenesis in domestic ruminants. Anim. Reprod. 16:52–65
   [Google Scholar]
8. 8. 

   Eppig JJ, O'Brien MJ. 1996. Development in vitro of mouse oocytes from primordial follicles. Biol. Reprod. 54:197–207
   [Google Scholar]
9. 9. 

   Hikabe O, Hamazaki N, Nagamatsu G, Obata Y, Hirao Y et al. 2016. Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature 539:299–303
   [Google Scholar]
10. 10. 

    Morohaku K, Tanimoto R, Sasaki K, Kawahara-Miki R, Kono T et al. 2016. Complete in vitro generation of fertile oocytes from mouse primordial germ cells. PNAS 113:9021–26
    [Google Scholar]
11. 11. 

    Gougeon A. 1996. Regulation of ovarian follicular development in primates—facts and hypotheses. Endocr. Rev. 17:121–55
    [Google Scholar]
12. 12. 

    Simon LE, Kumar TR, Duncan FE. 2020. In vitro ovarian follicle growth: a comprehensive analysis of key protocol variables. Biol. Reprod. 103:455–70
    [Google Scholar]
13. 13. 

    Rios PD, Kniazeva E, Lee HC, Xiao S, Oakes RS et al. 2015. Retrievable hydrogels for ovarian follicle transplantation and oocyte collection. Biotechnol. Bioeng. 115:2075–86
    [Google Scholar]
14. 14. 

    McLaughlin M, Albertini DF, Wallace WHB, Anderson RA, Telfer EE 2018. Metaphase II oocytes from human unilaminar follicles grown in a multi-step culture system. Mol. Hum. Reprod. 24:135–42
    [Google Scholar]
15. 15. 

    Telfer EE, Zelinski MB. 2013. Ovarian follicle cultures: advances and challenges for human and nonhuman primates. Fertil. Steril. 99:1523–33
    [Google Scholar]
16. 16. 

    de Sá NAR, Ferreira ACA, Sousa FGC, Duarte ABG, Paes VM et al. 2020. First pregnancy after in vitro culture of early antral follicles in goats: positive effects of anethole on follicle development and steroidogenesis. Mol. Reprod. Dev. 87:966–77
    [Google Scholar]
17. 17. 

    Aguiar FLN, Gastal GDA, Alves KA, Alves BG, Figueiredo JR, Gastal EL. 2020. Supportive techniques to investigate in vitro culture and cryopreservation efficiencies of equine ovarian tissue: a review. Theriogenology 156:296–309
    [Google Scholar]
18. 18. 

    Wiedemann C, Zahmel J, Jewgenow K. 2013. Short-term culture of ovarian cortex pieces to assess the cryopreservation outcome in wild felids for genome conservation. BMC Vet. Res. 9:37
    [Google Scholar]
19. 19. 

    Nation A, Selwood L. 2009. The production of mature oocytes from adult ovaries following primary follicle culture in a marsupial. Reproduction 138:247–55
    [Google Scholar]
20. 20. 

    Picton H. 2019. In vivo oocyte development. In How to Prepare the Egg and Embryo to Maximize IVF Success G Kovacs, A Rutherford, DK Gardner 22–35 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
21. 21. 

    Sanfins A, Rodrigues P, David F, Albertini DF 2018. GDF-9 and BMP-15 direct the follicle symphony. J. Assist. Reprod. Genet. 35:1741–50
    [Google Scholar]
22. 22. 

    Harris SE, Leese HJ, Gosden RG, Picton HM. 2009. Pyruvate and oxygen consumption throughout the growth and development of murine oocytes. Mol. Reprod. Dev. 76:231–38
    [Google Scholar]
23. 23. 

    Collado-Fernandez E, Picton HM, Dumollard R. 2012. Metabolism throughout follicle and oocyte development in mammals. Int. J. Dev. Biol. 56:799–808
    [Google Scholar]
24. 24. 

    Hsueh AJW, Kawamura K, Cheng Y, Fauser BCJM. 2015. Intraovarian control of early folliculogenesis. Endocr. Rev. 36:1–24
    [Google Scholar]
25. 25. 

    Shah JS, Sabouni R, Kamaria C, Vaught C, Owen CM et al. 2018. Biomechanics and mechanical signaling in the ovary: a systematic review. J. Assist. Reprod. Genet. 35:1135–48
    [Google Scholar]
26. 26. 

    De Vos M, Grynberg M, Ho TM, Yuan Y, Albertini DF, Gilchrist RB. 2021. Perspectives on the development and future of oocyte IVM in clinical practice. J. Assist. Reprod. Genet. 38:1265–80
    [Google Scholar]
27. 27. 

    Anderson RA, McLaughlin M, Wallace WH, Albertini DF, Telfer EE. 2014. The immature human ovary shows loss of abnormal follicles and increasing follicle developmental competence through childhood and adolescence. Hum. Reprod. 29:97–106
    [Google Scholar]
28. 28. 

    Mastrorocco A, Cacopardo L, Lamanna D, Temerario L, Brunetti G et al. 2021. Bioengineering approaches to improve in vitro performance of prepubertal lamb oocytes. Cells 10:1458
    [Google Scholar]
29. 29. 

    Leese HJ. 2012. Metabolism of the preimplantation embryo: 40 years on. Reproduction 143:417–27
    [Google Scholar]
30. 30. 

    Cecconi S, Barboni B, Coccia M, Mattioli M 1999. In vitro development of sheep preantral follicles. Biol. Reprod. 60:594–601
    [Google Scholar]
31. 31. 

    Jin P, Harris SE, Picton HM 2007. Effect of oxygen tension on ovine follicle growth in vitro. Fertility 2007:P35
    [Google Scholar]
32. 32. 

    Smitz J, Cortvrindt R, Van Steirteghem AC. 1996. Normal oxygen atmosphere is essential for the solitary long-term culture of early preantral mouse follicles. Mol. Reprod. Dev. 45:466–75
    [Google Scholar]
33. 33. 

    Hu Y, Betzendahl I, Cortvrindt R, Smitz J, Eichenlaub-Ritter U. 2001. Effects of low O₂ and ageing on spindles and chromosomes in mouse oocytes from pre-antral follicle culture. Hum. Reprod. 16:737–48
    [Google Scholar]
34. 34. 

    Naillat F, Saadeh H, Nowacka-Woszuk J, Gahurova L, Santos F et al. 2021. Oxygen concentration affects de novo DNA methylation and transcription in in vitro cultured oocytes. Clin. Epigenet. 13:132
    [Google Scholar]
35. 35. 

    Jorssen EP, Langbeen A, Fransen E, Martinez EL, Leroy JL, Bols PE 2014. Monitoring preantral follicle survival and growth in bovine ovarian biopsies by repeated use of neutral red and cultured in vitro under low and high oxygen tension. Theriogenology 82:387–95
    [Google Scholar]
36. 36. 

    Talevi R, Sudhakaran S, Barbato V, Merolla A, Braun S et al. 2018. Is oxygen availability a limiting factor for in vitro folliculogenesis?. PLOS ONE 13:e0192501
    [Google Scholar]
37. 37. 

    Wright CS, Hovatta O, Margara R, Trew G, Winston RM et al. 1999. Effects of follicle-stimulating hormone and serum substitution on the in-vitro growth of human ovarian follicles. Hum. Reprod. 14:1555–62
    [Google Scholar]
38. 38. 

    Rodriguez Jimenez C, Araújo VR, Penintente-Filho JM, de Azevedo JL, Silveira RG, Torres CAA 2016. The base medium affects ultrastructure and survival of bovine preantral follicles cultured in vitro. Theriogenology 85:1019–29
    [Google Scholar]
39. 39. 

    Picton HM, Mkandla A, Salha O, Wynn P, Gosden RG 1999. Initiation of human primordial follicle growth in vitro in ultra-thin slices of ovarian cortex. Hum. Reprod. 14:Suppl. 311
    [Google Scholar]
40. 40. 

    Spears N, Boland NI, Murray AA, Gosden RG. 1994. Mouse oocytes derived from in vitro grown primary ovarian follicles are fertile. Hum. Reprod. 9:527–32
    [Google Scholar]
41. 41. 

    Newton H, Picton H, Gosden RG. 1999. In vitro growth of oocyte-granulosa cell complexes isolated from cryopreserved ovine tissue. J. Reprod. Fertil. 115:141–50
    [Google Scholar]
42. 42. 

    Abir R, Franks S, Mobberley MA, Moore PA, Margara RA, Winston RM. 1997. Mechanical isolation and in vitro growth of preantral and small antral human follicles. Fertil. Steril. 68:682–88
    [Google Scholar]
43. 43. 

    O'Brien MJ, Pendola JK, Eppig JJ 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]
44. 44. 

    Muruvi W, Picton HM, Rodway RG, Joyce IM. 2009. In vitro growth and differentiation of primary follicles isolated from cryopreserved sheep ovarian tissue. Anim. Reprod. Sci. 112:36–50
    [Google Scholar]
45. 45. 

    Telfer EE, McLaughlin M, Ding C, Thong KJ 2008. A two-step serum-free culture system supports development of human oocytes from primordial follicles in the presence of activin. Hum. Reprod. 23:1151–58
    [Google Scholar]
46. 46. 

    Young LE, Fernandes K, McEvoy TG, Butterwith SC, Gutierrez CG et al. 2001. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat. Genet. 27:153–54
    [Google Scholar]
47. 47. 

    Fernández-Gonzalez R, Moreira P, Bilbao A, Jiménez A, Pérez-Crespo M et al. 2004. Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior. PNAS 101:5880–85
    [Google Scholar]
48. 48. 

    Celestino JJH, Bruno JB, Saraiva MVA, Rocha RMP, Brito IR et al. 2011. Steady-state level of epidermal growth factor (EGF) mRNA and effect of EGF on in vitro culture of caprine preantral follicles. Cell Tissue Res. 344:539–50
    [Google Scholar]
49. 49. 

    Peng X, Yang M, Wang L, Tong C, Guo Z 2010. In vitro culture of sheep lamb ovarian cortical tissue in a sequential culture medium. J. Assist. Reprod. Genet. 27:247–57
    [Google Scholar]
50. 50. 

    Huntriss J, Balen AH, Sinclair KD, Brison DR, Picton HM, R. Coll Obstet. Gynaecol. 2018. Epigenetics and reproductive medicine: scientific impact paper No. 57. BJOG 125:e43–e54
    [Google Scholar]
51. 51. 

    Xu J, Bernuci MP, Lawson MS, Yeoman RR, Fisher TE et al. 2010. Survival, growth, and maturation of secondary follicles from prepubertal, young and older adult rhesus monkeys during encapsulated three-dimensional culture: effects of gonadotrophins and insulin. Reproduction 140:685–97
    [Google Scholar]
52. 52. 

    Lima LF, Rocha RMP, Alves AMCV, Carvalho AA, Chaves RN et al. 2016. Comparison between the additive effects of diluted (rFSH) and diluted/dynamized (FSH 6 cH) recombinant follicle-stimulating hormone on the in vitro culture of ovine preantral follicles enclosed in ovarian tissue. Complement. Ther. Med. 25:39–44
    [Google Scholar]
53. 53. 

    Picton HM, Danfour MA, Harris SE, Chambers EL, Huntriss J. 2003. Growth and maturation of oocytes in vitro. Reprod. Suppl. 61:445–62
    [Google Scholar]
54. 54. 

    Filatov M, Khramova Y, Parshina E, Bagaeva T, Semenova M. 2017. Influence of gonadotropins on ovarian follicle growth and development in vivo and in vitro. Zygote 25:235–43
    [Google Scholar]
55. 55. 

    McLaughlin M, Telfer EE. 2010. Oocyte development in bovine primordial follicles is promoted by activin and FSH within a two-step serum-free culture system. Reproduction 139:971–78
    [Google Scholar]
56. 56. 

    Tanaka Y, Matsuzaki T, Tanaka N, Iwasa T, Kuwahara A, Irahara M 2019. Activin effects on follicular growth in in vitro preantral follicle culture. J. Med. Investig. 66:165–71
    [Google Scholar]
57. 57. 

    Silva GM, Araújo VR, Duarte ABG, Chaves RN, Silva CMG et al. 2011. Ascorbic acid improves the survival and in vitro growth of isolated caprine preantral follicles. Anim. Reprod. 8:14–24
    [Google Scholar]
58. 58. 

    Wang T-r, Yan L-y, Yan J, Lu C-l, Xia X et al. 2014. Basic fibroblast growth factor promotes the development of human ovarian early follicles during growth in vitro. J. Hum. Reprod. 29:568–76
    [Google Scholar]
59. 59. 

    Xu F, Lawson MS, Bean Y, Ting AY, Pejovic T et al. 2021. Matrix-free 3D culture supports human follicular development from the unilaminar to the antral stage in vitro yielding morphologically normal metaphase II oocytes. Hum. Reprod. 36:1326–38
    [Google Scholar]
60. 60. 

    Xu J, Xu F, Lawson MS, Tkachenko OY, Ting AY et al. 2018. Anti-Müllerian hormone is a survival factor and promotes the growth of rhesus macaque preantral follicles during matrix free culture. Biol. Reprod. 98:197–207
    [Google Scholar]
61. 61. 

    Conti M, Hsieh M, Park JY, Su YQ 2006. Role of the epidermal growth factor network in ovarian follicles. Mol. Endocrinol. 20:715–23
    [Google Scholar]
62. 62. 

    Peluffo M, Stouffer RL, Hennebold JD, Zelinski MB. 2010. Cumulus oocyte complexes from small antral follicles during the early follicular phase of spontaneous cycles in rhesus monkeys can expand and yield oocytes capable of maturation in vitro. Biol. Reprod. 83:525–32
    [Google Scholar]
63. 63. 

    Silva AWB, Ribeiro RP, Menezes VG, Barberino RS, Passos JRS et al. 2017. Expression of TNF-α system members in bovine ovarian follicles and the effects of TNF-α or dexamethasone on preantral follicle survival, development and ultrastructure in vitro. Anim. Reprod. Sci. 182:56–68
    [Google Scholar]
64. 64. 

    Cortvrindt R, Smitz J, Van Steirteghem AC. 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]
65. 65. 

    Smitz J, Dolmans MM, Donnez J, Fortune JE, Hovatta O 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]
66. 66. 

    Lee J, Kim EJ, Kong HS, Youm HW, Kim SK et al. 2018. Comparison of the oocyte quality derived from two-dimensional follicle culture methods and developmental competence of in vitro grown and matured oocytes. BioMed. Res. Int. 2018:7907092
    [Google Scholar]
67. 67. 

    Araujo VR, Gastal MO, Wischral A, Figueiredo JR, Gastal EL. 2014. In vitro development of bovine secondary follicles in two- and three- dimensional culture systems using vascular endothelial growth factor, insulin-like growth factor-1, and growth hormone. Theriogenology 82:1246–53
    [Google Scholar]
68. 68. 

    Jamalzaei P, Rezazadeh Valojerdi M, Montazeri L, Baharvand H 2020. Applicability of hyaluronic acid-alginate hydrogel and ovarian cells for in vitro development of mouse preantral follicles. Cell J. 22:Suppl. 149–60
    [Google Scholar]
69. 69. 

    Vanacker J, Amorim CA. 2017. Alginate: a versatile biomaterial to encapsulate isolated ovarian follicles. Ann. Biomed. Eng. 45:1633–49
    [Google Scholar]
70. 70. 

    Hornick JE, Duncan FE, Shea LD, Woodruff TK. 2012. Isolated primate primordial follicles require a rigid physical environment to survive and grow in vitro. Hum. Reprod. 27:1801–10
    [Google Scholar]
71. 71. 

    Sadr SZ, Fatehi R, Maroufizadeh S, Amorim CA, Ebrahimi B. 2018. Utilizing fibrin-alginate and matrigel-alginate for mouse follicle development in three-dimensional culture systems. Biopreserv. Biobank. 16:120–27
    [Google Scholar]
72. 72. 

    Kedem A, Hourvitz A, Fisch B, Shachar M, Cohen S et al. 2011. Alginate scaffold for organ culture of cryopreserved-thawed human ovarian cortical follicles. . J. Assist. Reprod. Genet. 28:761–69
    [Google Scholar]
73. 73. 

    Laronda MM, Duncan FE, Hornick JE, Xu M, Pahnke JE et al. 2014. Alginate encapsulation supports the growth and differentiation of human primordial follicles within ovarian cortical tissue. J. Assist. Reprod. Genet. 31:1013–28
    [Google Scholar]
74. 74. 

    Correia HHV, Lima LF, Sousa FGC, Ferreira ACA, Cadenas J et al. 2020. Activation of goat primordial follicles in vitro: influence of alginate and ovarian tissue. Reprod. Domest. Anim. 55:105–9
    [Google Scholar]
75. 75. 

    Shikanov A, Xu M, Woodruff TK, Shea LD. 2011. A method for ovarian follicle encapsulation and culture in a proteolytically degradable 3 dimensional system. . J. Vis. Exp. 49:2695
    [Google Scholar]
76. 76. 

    Brito IR, Lima IM, Xu M, Shea LD, Woodruff TK, Figueiredo JR. 2014. Three-dimensional systems for in vitro follicular culture: overview of alginate-based matrices. Reprod. Fertil. Dev. 26:915–30
    [Google Scholar]
77. 77. 

    Xu M, West-Farrell ER, Stouffer RL, Shea LD, Woodruff TK, Zelinski MB. 2009. Encapsulated three-dimensional culture supports development of nonhuman primate secondary follicles. Biol. Reprod. 81:587–94
    [Google Scholar]
78. 78. 

    Xu J, Lawson MS, Yeoman RR, Pau KY, Barrett SL et al. 2011. Secondary follicle growth and oocyte maturation during encapsulated three-dimensional culture in rhesus monkeys: effects of gonadotrophins, oxygen and fetuin. Hum. Reprod. 26:1061–72
    [Google Scholar]
79. 79. 

    Xu M, Fazleabas AT, Shikanov A, Jackson E, Barrett SL, Hirshfeld-Cytron J 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]
80. 80. 

    Xu J, Lawson MS, Yeoman RR, Molskness TA, Ting AY et al. 2013. Fibrin promotes development and function of macaque primary follicles during encapsulated three-dimensional culture. Hum. Reprod. 28:2187–200
    [Google Scholar]
81. 81. 

    Xiao S, Zhang J, Romero MM, Smith KN, Shea LD, Woodruff TK. 2015. In vitro follicle growth supports human oocyte meiotic maturation. Sci. Rep. 5:17323
    [Google Scholar]
82. 82. 

    Green LJ, Shikanov A. 2016.. In vitro culture methods of preantral follicles. Theriogenology 86:229–38
    [Google Scholar]
83. 83. 

    Heise M, Koepsel R, Russel AJ, McGee EA 2005. Calcium alginate microencapsulation of ovarian follicles impacts on FSH delivery and follicle morphology. Reprod. Biol. Endocrinol. 3:47
    [Google Scholar]
84. 84. 

    Mainigi MA, Ord T, Schultz RM. 2011. Meiotic and developmental competence in mice are compromised following follicle development in vitro using an alginate-based culture system. Biol. Reprod. 85:269–76
    [Google Scholar]
85. 85. 

    Desai N, Abdelhafez F, Calabro A, Falcon ET 2012. Three dimensional culture of fresh and vitrified mouse pre-antral follicles in a hyaluronan-based hydrogel: a preliminary investigation of a novel biomaterial for in vitro follicle maturation. Reprod. Biol. Endocrinol. 10:29
    [Google Scholar]
86. 86. 

    Hao J, Tuck AR, Prakash CR, Damdimopoulos A, Sjödin MO et al. 2020. Culture of human ovarian tissue in xeno-free conditions using laminin components of the human ovarian extracellular matrix. J. Assist. Reprod. Genet. 37:2137–50
    [Google Scholar]
87. 87. 

    Pors SE, Ramløse M, Nikiforov D, Lundsgaard K, Cheng J et al. 2019. Initial steps in reconstruction of the human ovary: survival of pre-antral stage follicles in a decellularized human ovarian scaffold. Hum. Reprod. 34:1523–35
    [Google Scholar]
88. 88. 

    Kim EJ, Yang C, Lee J, Youm HW, Lee JR et al. 2020. The new biocompatible material for mouse ovarian follicle development in three-dimensional in vitro culture systems. Theriogenology 144:33–40
    [Google Scholar]
89. 89. 

    Arunakumari G, Shanmugasundaram N, Rao VH. 2010. Development of morulae from the oocytes of cultured sheep preantral follicles. Theriogenology 74:884–94
    [Google Scholar]
90. 90. 

    Antonino DC, Soares MM, Júnior JM, de Alvarenga PB, Mohallem RFF et al. 2019. Three-dimensional levitation culture improves in-vitro growth of secondary follicles in bovine model. Reprod. Biomed. Online 38:300–11
    [Google Scholar]
91. 91. 

    Chambers EL, Gosden RG, Yap C, Picton HM. 2010. In situ identification of follicles in ovarian cortex as a tool for quantifying follicle density, viability and developmental potential in strategies to preserve female fertility. Hum. Reprod. 25:2559–68
    [Google Scholar]
92. 92. 

    Wilken-Jensen HN, Kristensen SG, Jeppesen JV, Andersen CY. 2014. Developmental competence of oocytes isolated from surplus medulla tissue in connection with cryopreservation of ovarian tissue for fertility preservation. Acta Obstet. Gynecol. Scand. 93:32–37
    [Google Scholar]
93. 93. 

    Lucci CM, Kacinskis MA, Lopes LHR, Rumpf R, Báo SN 2004. Effect of different cryoprotectants on the structural preservation of follicles in frozen zebu bovine (Bos indicus) ovarian tissue. Theriogenology 61:1101–14
    [Google Scholar]
94. 94. 

    Ouni E, Bouzin C, Dolmans MM, Marbaix E, Pyr dit Ruys S et al. 2020. Spatiotemporal changes in mechanical matrisome components of the human ovary from prepuberty to menopause. Hum. Reprod. 35:1391–410
    [Google Scholar]
95. 95. 

    Amargant F, Manuel SL, Tu Q, Parkes WS, Rivas F et al. 2020. Ovarian stiffness increases with age in the mammalian ovary and depends on collagen and hyaluronan matrices. Aging Cell 19:e13259
    [Google Scholar]
96. 96. 

    Vanacker J, Camboni A, Dath C, Van Langedonckt A, Dolmans M-M et al. 2011. Enzymatic isolation of human primordial and primary ovarian follicles with Liberase DH: protocol for application in a clinical setting. Fertil. Steril. 96:379–89
    [Google Scholar]
97. 97. 

    Kristensen SG, Rasmussen A, Byskov AG, Andersen CY. 2011. Isolation of pre-antral follicles from human ovarian medulla tissue. Hum. Reprod. 26:157–66
    [Google Scholar]
98. 98. 

    Shiomi-Sugaya N, Komatsu K, Wang J, Yamashita M, Kikkawa F, Iwase A 2015. Regulation of secondary follicle growth by theca cells and insulin-like growth factor 1. J. Reprod. Dev. 61:161–68
    [Google Scholar]
99. 99. 

    Vanacker J, Luyckx V, Amorim C, Dolmans M-M, Van Langedonckt A et al. 2013. Should we isolate human preantral follicles before or after cryopreservation of ovarian tissue?. Fertil. Steril. 99:1363–68.e2
    [Google Scholar]
100. 100. 

     Kristensen SG, Liu Q, Mamsen LS, Greve T, Pors SE et al. 2018. A simple method to quantify follicle survival in cryopreserved human ovarian tissue. Hum. Reprod. 33:2276–84
     [Google Scholar]
101. 101. 

     Bulgarelli DL, Ting AY, Gordon BJ, de Sá Rosa-E-Silva ACJ, Zelinski MB. 2018. Development of macaque secondary follicles exposed to neutral red prior to 3-dimensional culture. J. Assist. Reprod. Genet. 35:71–79
     [Google Scholar]
102. 102. 

     Hornick JE, Duncan FE, Shea LD, Woodruff TK. 2013. Multiple follicle culture supports primary follicle growth through paracrine-acting signals. Reproduction 145:19–32
     [Google Scholar]
103. 103. 

     Barboni B, Russo V, Cecconi S, Curini V, Colosimo A et al. 2011. In vitro grown sheep preantral follicles yield oocytes with normal nuclear-epigenetic maturation. PLOS ONE 6:e27550
     [Google Scholar]
104. 104. 

     Cotterill M, Catt SL, Picton HM. 2012. Characterisation of the cellular and molecular responses of ovine oocytes and their supporting somatic cells to pre-ovulatory levels of LH and FSH during in vitro maturation. Reproduction 144:195–207
     [Google Scholar]
105. 105. 

     Hemmings KE, Leese HJ, Picton HM 2012. Amino acid turnover by bovine oocytes provides an index of oocyte developmental competence in vitro. Biol. Reprod. 86:165
     [Google Scholar]
106. 106. 

     Wynn P, Picton HM, Krapez JA, Rutherford AJ, Balen AH, Gosden RG. 1998. Pretreatment with follicle stimulating hormone promotes the numbers of human oocytes reaching metaphase II by in-vitro maturation. Hum. Reprod. 13:3132–38
     [Google Scholar]
107. 107. 

     Smitz J, Picton HM, Platteau P, Rutherford A, Cortvrindt R et al. 2007. Principal findings from a multicenter trial investigating the safety of follicular-fluid meiosis-activating sterol for in vitro maturation of human cumulus-enclosed oocytes. Fertil. Steril. 87:949–64
     [Google Scholar]
108. 108. 

     Trapphoff T, Heiligentag M, Dankert D, Demond H, Deutsch D et al. 2016. Postovulatory aging affects dynamics of mRNA, expression and localization of maternal effect proteins, spindle integrity and pericentromeric proteins in mouse oocytes. Hum. Reprod. 31:133–49
     [Google Scholar]
109. 109. 

     Yin H, Kristensen SG, Jiang H, Rasmussen A, Andersen CY. 2016. Survival and growth of isolated pre-antral follicles from human ovarian medulla tissue during long-term 3D culture. Hum. Reprod. 31:1531–39
     [Google Scholar]
110. 110. 

     Castillo-Fernandez J, Herrera-Puerta E, Demond H, Clark SJ, Hanna CW et al. 2020. Increased transcriptome variation and localised DNA methylation changes in oocytes from aged mice revealed by parallel single-cell analysis. Aging Cell 19:e13278
     [Google Scholar]
111. 111. 

     Apolloni LB, Bruno JB, Alves BG, Ferreira ACA, Paes VM et al. 2016. Accelerated follicle growth during the culture of isolated caprine preantral follicles is detrimental to follicular survival and oocyte meiotic resumption. Theriogenology 86:1530–40
     [Google Scholar]
112. 112. 

     Anckaert E, De Rycke M, Smitz J. 2013. Culture of oocytes and risk of imprinting defects. Hum. Reprod. Update 19:52–66
     [Google Scholar]
113. 113. 

     Saenz-de-Juano MD, Billooye K, Smitz J, Anckaert E. 2016. The loss of imprinted DNA methylation in mouse blastocysts is inflicted to a similar extent by in vitro follicle culture and ovulation induction. Mol. Hum. Reprod. 22:427–41
     [Google Scholar]
114. 114. 

     Saenz-de-Juano MD, Ivanova E, Billooye K, Herta AC, Smitz J et al. 2019. Genome-wide assessment of DNA methylation in mouse oocytes reveals effects associated with in vitro growth, superovulation, and sexual maturity. Clin. Epigenet. 11:197
     [Google Scholar]
115. 115. 

     Saenz-de-Juano MD, Ivanova E, Romero S, Lolicato F, Sánchez F et al. 2019. DNA methylation and mRNA expression of imprinted genes in blastocysts derived from an improved in vitro maturation method for oocytes from small antral follicles in polycystic ovary syndrome patients. Hum. Reprod. 34:1640–49
     [Google Scholar]
116. 116. 

     Hirao Y, Naruse K, Kaneda M, Somfai T, Iga K et al. 2013. Production of fertile offspring from oocytes grown in vitro by nuclear transfer in cattle. Biol. Reprod. 89:57
     [Google Scholar]
117. 117. 

     Guzman L, Orgega-Hreppich C, Albuz FK, Verheyen G, Devroey P et al. 2012. Developmental capacity of in vitro-matured human oocyte retrieved from polycystic ovary syndrome ovaries containing so follicles larger than 6mm. Fertil. Steril. 98:503–7.e1–2
     [Google Scholar]
118. 118. 

     Sánchez F, Romero S, De Vos M, Verheyen G, Smitz J. 2015. Human cumulus-enclosed germinal vesicle oocytes from early antral follicles reveal heterogeneous cellular and molecular features associated with in vitro maturation capacity. Hum. Reprod. 30:1396–409
     [Google Scholar]
119. 119. 

     Gruhn JR, Kristensen SG, Andersen CY, Hoffmann ER. 2018. In-vitro maturation and culture of human oocytes. Methods Mol. Biol. 1818:23–30
     [Google Scholar]
120. 120. 

     Swain JE, Lai D, Takayama S, Smith GD 2013. Thinking big by thinking small: application of microfluidic technology to improve ART. Lab Chip 13:1213–24
     [Google Scholar]
121. 121. 

     Sharma S, Venzac B, Burgers T, Le Gac S, Schlatt S 2020. Microfluidics in male reproduction: Is ex vivo culture of primate testis tissue a future strategy for ART or toxicology research?. Mol. Hum. Reprod. 26:179–92
     [Google Scholar]
122. 122. 

     Nagashima JB, El Assal R, Songsasen N, Demirci U 2018. Evaluation of an ovary-on-a-chip in large mammalian models: species specificity and influence of follicle isolation status. J. Tissue Eng. Regen. Med. 12:e1926–e35
     [Google Scholar]
123. 123. 

     Healy MW, Dolitsky SN, Villancio-Wolter M, Raghavan M, Tillman AR et al. 2021. Creating an artificial 3-dimensional ovarian follicle culture system using a microfluidic system. Micromachines 12:261
     [Google Scholar]
124. 124. 

     He X. 2017. Microfluidic encapsulation of ovarian follicles for 3D culture. Ann. Biomed. Eng. 45:1676–84
     [Google Scholar]
125. 125. 

     Kawamura K, Cheng Y, Suzuki N, Deguchi M, Sato Y et al. 2013. Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. PNAS 110:17474–79
     [Google Scholar]
126. 126. 

     Bertoldo MJ, Walters KA, Ledger WL, Gilchrist RB, Mermillod P, Locatelli Y 2018. In-vitro regulation of primordial follicle activation: challenges for fertility preservation strategies. Reprod. Biomed. Online 36:491–99
     [Google Scholar]
127. 127. 

     Lunding SA, Pors SE, Kristensen SG, Landersoe SK, Jeppesen JV et al. 2019. Biopsying, fragmentation and autotransplantation of fresh ovarian cortical tissue in infertile women with diminished ovarian reserve. Hum. Reprod. 34:1924–36
     [Google Scholar]
128. 128. 

     Devenutto L, Quintana R, Quintana T. 2020. In vitro activation of ovarian cortex and autologous transplantation: a novel approach to primary ovarian insufficiency and diminished ovarian reserve. Hum. Reprod. Open 2020:4hoaa046
     [Google Scholar]
129. 129. 

     Vo KCT, Kawamura K. 2021. In vitro activation early follicles: from the basic science to the clinical perspectives. Int. J. Mol. Sci. 22:3785
     [Google Scholar]
130. 130. 

     Adhikari D, Gorre N, Risal S, Zhao Z, Zhang H et al. 2012. The safe use of a PTEN inhibitor for the activation of dormant mouse primordial follicles and generation of fertilizable eggs. PLOS ONE 7:e39034
     [Google Scholar]
131. 131. 

     Adhikari D, Risal S, Liu K, Shen Y. 2013. Pharmacological inhibition of mTORC1 prevents over-activation of the primordial follicle pool in response to elevated PI3 K signaling. PLOS ONE 8:e53810
     [Google Scholar]
132. 132. 

     Cheng Y, Kim J, Li XX, Hsueh AJ 2015. Promotion of ovarian follicle growth following mTOR activation: synergistic effects of AKT stimulators. PLOS ONE 10:e0117769
     [Google Scholar]
133. 133. 

     McLaughlin M, Kinnell HL, Anderson RA, Telfer EE 2014. Inhibition of phosphatase and tensin homologue (PTEN) in human ovary in vitro results in increased activation of primordial follicles but compromises development of growing follicles. Mol. Hum. Reprod. 20:736–44
     [Google Scholar]
134. 134. 

     Novella-Maestre E, Herraiz S, Rodríguez-Iglesias B, Díaz-García C, Pellicer A. 2015. Short-term PTEN inhibition improves in vitro activation of primordial follicles, preserves follicular viability, and restores AMH levels in cryopreserved ovarian tissue from cancer patients. PLOS ONE 10:e0127786
     [Google Scholar]
135. 135. 

     De Roo C, Lierman S, Tilleman K, De Sutter P. 2020. In-vitro fragmentation of ovarian tissue activates primordial follicles through the Hippo pathway. Hum. Reprod. Open 2020:4hoaa048
     [Google Scholar]
136. 136. 

     Monte APO, Bezerra MÉS, Menezes VG, Gouveia BB, Barberino RS et al. 2021. Involvement of phosphorylated Akt and FOXO3a in the effects of Growth and Differentiation Factor-9 (GDF-9) on inhibition of follicular apoptosis and induction of granulosa cell proliferation after in vitro culture of sheep ovarian tissue. Reprod. Sci. 28:2174–85
     [Google Scholar]
137. 137. 

     Liu Z, Ren YA, Pangas SA, Adams J, Zhou W et al. 2015. FOXO1/3 and PTEN depletion in granulosa cells promotes ovarian granulosa cell tumor development. Mol. Endocrinol. 29:1006–24
     [Google Scholar]