In vitro growth systems for human oocytes: From primordial to maturation

Principles and Practice of Fertility Preservation

Volumn , Issue , 2011, Pages 397-408

  Telfer, Evelyn E ^a   McLaughlin, Marie ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84873724972     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1017/CBO9780511921896.036     Document Type: Chapter

References (91)

1. Anderson RA, Wallace WH and Baird DT. Ovarian cryopreservation for fertility preservation: indications and outcomes. Reproduction2008; 136: 681–9.
2. Donnez J, Jadoul P, Squifflet J et al. Ovarian tissue cryopreservation and transplantation in cancer patients. Best Pract Res Clin Obstet Gynaecol2010; 24: 87–100.
3. Meirow D, Hardan I, Dor J et al. Searching for evidence of disease and malignant cell contamination in ovarian tissue stored from hematologic cancer patients. Hum Reprod2008; 23: 1007–13.
4. Telfer EE and McLaughlin M. Natural history of the mammalian oocyte. Reprod Biomed Online2007; 15: 288–95.
5. Picton HM, Harris SE, Muruvi Wand Chambers EL. The in vitro growth and maturation of follicles. Reproduction2008; 136: 703–15.
6. Telfer EE, McLaughlin M, Ding C and Thong KJ. A two step serum free culture system supports development of human oocytes from primordial follicles in the presence of activin. Hum Reprod2008; 23: 1151–8.
7. Xu M, Barrett SL, West-Farrell E et al. In vitro grown human ovarian follicles from cancer patients support oocyte growth. Hum Reprod2009; 24: 2531–40.
8. Smitz J, Dolmans MM, Donnez J et al. Current achievements and future research directions in ovarian tissue culture, in vitro follicle development and transplantation: implications for fertility preservation. Hum Reprod Update2010; 16(4): 395–414.
9. Rodrigues P, Limback D, McGinnis LK, Plancha CE and Albertini DF. Oogenesis: prospects and challenges for the future. J Cell Physiol2008; 216: 355–65.
10. Zuckerman S.The number of oocytes in the mature ovary. Recent Prog Horm Res1951; 6: 63–109.
11. Gougeon A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev1996; 17: 121–55.
12. Gougeon A and Chainy GB. Morphometric studies of small follicles in ovaries of women at different ages. J Reprod Fertil1987; 81: 433–42.
13. Thomas FH, Walters KA and Telfer EE. Howtomake a good oocyte: an update on in vitro models to study follicle regulation. Hum Reprod Update2003; 9: 1–15.
14. Eppig JJ and Schroeder AC. Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol Reprod1989; 41: 268–76.
15. Eppig JJ and O’Brien MJ. Development in vitro of mouse oocytes from primordial follicles. Biol Reprod1996; 54: 197–207.
16. O’Brien MJ, Pendola JK and Eppig JJ. A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol Reprod2003; 68: 1682–6.
17. Spears N, Boland NI, Murray AA and Gosden RG. Mouse oocytes derived from in vitro grown primary ovarian follicles are fertile. Hum Reprod1994; 9: 527–32.
18. Hovatta O, Silye R, Abir R, Krausz T andWinston RM. Extracellular matrix improves survival of both stored and fresh human primordial and primary ovarian follicles in long-term culture. Hum Reprod1997; 12: 1032–6.
19. Hovatta O, Wright C, Krausz T, Hardy K and Winston RM. Human primordial, primary and secondary ovarian follicles in long-term culture: effect of partial isolation. Hum Reprod 1999; 14: 2519–2524.
20. Picton HM and Gosden RG. In vitro growth of human primordial follicles from frozen-banked ovarian tissue. Mol Cell Endocrinol2000; 166: 27–35.
21. Wright CS, Hovatta O, Margara R et al. Effects of follicle-stimulating hormone and serum substitution on the in-vitro growth of human ovarian follicles. Hum Reprod1999: 14: 1555–62.
22. Zhang P, Louhio H, Tuuri T et al. In vitro effect of cyclic adenosine 3’, 5’-monophosphate (cAMP) on early human ovarian follicles. J Assist Reprod Genet2004; 21: 301–6.
23. Abir R, Franks S, Mobberley MA et al. Mechanical isolation and in vitro growth of preantral and small antral human follicles. Fertil Steril1997; 68: 682–8.
24. Abir R, Roizman P, Fisch B et al. Pilot study of isolated early human follicles cultured in collagen gels for 24 hours. Hum Reprod1999; 14: 1299–301.
25. Roy SK and Treacy BJ. Isolation and long-term culture of human preantral follicles. Fertil Steril1993; 59: 783–90.
26. Alak BM, Coskun S, Friedman CI et al. Activin A stimulates meiotic maturation of human oocytes and modulates granulosa cell steroidogenesis in vitro. Fertil Steril1998; 70: 1126–30.
27. Mikkelsen AL, Smith S and Lindenberg S. In-vitro maturation of immature human oocytes. Hum Reprod1998; 13: 23–4.
28. Cha KY and Chian RC. Maturation in vitro of immature human oocytes for clinical use. Hum Reprod Update1998; 4: 103–20.
29. Barnes FL, Crombie A, Gardner DK et al. Blastocyst development and birth after in-vitro maturation of human primary oocytes, intracytoplasmic sperm injection and assisted hatching. Hum Reprod1995; 10: 3243–7.
30. Cha KY, Koo JJ, Ko JJ et al. Pregnancy after in vitro fertilization of human follicular oocytes collected from nonstimulated cycles, their culture in vitro and their transfer in a donor oocyte program. Fertil Steril1991; 55: 109–13.
31. Durlinger AL, Visser JA and Themmen AP. Regulation of ovarian function: the role of anti-Müllerian hormone. Reproduction2002; 124: 601–9.
32. Da Silva-Buttkus P, Marcelli G, Franks S, Stark J and Hardy K. Inferring biological mechanisms from spatial analysis: prediction of a local inhibitor in the ovary. Proc Natl Acad Sci USA2009; 106: 456–61.
33. Jagarlamudi K, Reddy P, Adhikari D and Liu K. Genetically modified mouse models for premature ovarian failure (POF).Mol Cell Endocrinol2010; 315: 1–10.
34. Reddy P, Liu L, Adhikari D et al. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science2008; 319: 611–13.
35. Reddy P, Adhikari D, Zheng W et al. PDK1 signaling in oocytes controls reproductive aging and lifespan by manipulating the survival of primordial follicles. Hum Mol Genet2009; 18: 2813–24.
36. Kim DH, Sarbassov DD, Ali SM et al. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell2002; 110: 163–75.
37. Adhikari D and Liu K. mTOR signaling in the control of activation of primordial follicles. Cell Cycle2010; 9(9): 1673–4.
38. Telfer EE, McLaughlin M, Kini S et al. Inhibition of mTOR Kinase in cultured human ovarian cortex results in altered follicle dynamics. Hum Reprod2009; 24 (Suppl. 1): i800–197.
39. Johnson J, McLaughlin M, Yu J and Telfer EE. Inhibition of mTOR kinase in cultured bovine ovarian cortex results in altered follicle dynamics. Reprod Sci2009; 16: 1031 [Abstr.].
40. Hardy K, Wright CS, Franks S and Winston RM. In vitro maturation of oocytes. Br Med Bull2000; 56: 588–602.
41. Hansen KR, Knowlton NS, Thyer AC et al. A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause. Hum Reprod2008; 23: 699–708.
42. Telfer EE, Ansell JD, Taylor H and Gosden RG. The numbers of clonal precursors in the follicular epithelium of the mouse ovary. J Reprod Fertil1991; 84: 105–10.
43. Albertini DF and Barrett SL. Oocyte-somatic cell communication. Reprod Suppl2003; 61: 49–54.
44. Albertini DF, Combelles CM, Benecchi E and Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction2001; 121: 647–53.
45. Makabe S, Naguro T and Stallone T. Oocyte–follicle cell interactions during ovarian follicle development, as seen by high resolution scanning and transmission electron microscopy in humans. Microsc Res Tech2006; 69: 436–49.
46. Gosden RG and Telfer EE. Scaling of follicular sizes in mammalian ovaries. J Zool London1987; 211: 157–68.
47. Fortune JE.The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Anim Reprod Sci 2003; 78: 135–63.
48. Fair T, Hyttel P and Greve T. Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol Reprod Dev1995; 42: 437–42.
49. Hyttel P, Fair T, Callesen H and Greve T. Oocyte growth, capacitation and final maturation in cattle. Theriogenology1997; 47: 23–32.
50. Van Blerkom J, Davis P, Mathwig V and Alexander S. Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos. Hum Reprod2002; 17: 393–406.
51. Telfer EE, McLaughlin M, Keros V et al. Accelerated development of primordial follicles from vitrified human ovarian tissue within a two-step serum free culture system. Hum Reprod2008; 23: 97 0–239.
52. Durinzi KL, Saniga EM and Lanzendorf SE. The relationship between size and maturation in vitro in the unstimulated human oocyte. Fertil Steril1995; 63: 404–6.
53. Cavilla JL, Kennedy CR, Byskov AG and Hartshorne GM. Human immature oocytes grow during culture for IVM. Hum Reprod2008; 23: 37–45.
54. Wandji SA, Srsen V, Nathanielsz PW, Eppig JJ and Fortune JE. Initiation of growth of baboon primordial follicles in vitro. Hum Reprod1997; 12: 1993–2001.
55. Wandji SA, Srsen V, Voss AK, Eppig JJ and Fortune JE. Initiation in vitro of growth of bovine primordial follicles. Biol Reprod1996; 55: 942–8.
56. McLaughlin M and Telfer E. Oocyte development in bovine primordial follicles is promoted by activin and FSH within a two step serum free culture system. Reproduction2010; 139(6): 971–8.
57. McLaughlin EA and McIver SC. Awakening the oocyte: controlling primordial follicle development. Reproduction2009; 137: 1–11.
58. McCaffery FH, Leask R, Riley, SC and Telfer EE. Culture of bovine preantral follicles in a serum free system: markers for assessment of growth and development. Biol Reprod2000; 63: 267–73.
59. Thomas FH, Leask R, Srˇsen V et al. Effect of ascorbic acid on health and morphology of bovine preantral follicles during long term culture. Reproduction2001; 122: 487–95.
60. Scott JE, Zhang P and Hovatta O. Benefits of 8-bromo-guanosine 3’, 5’-cyclic monophosphate (8-br-cGMP) in human ovarian cortical tissue culture. Reprod Biomed Online2004; 8: 319–24.
61. Ding CC, Thong KJ, Krishna A and Telfer EE. Activin A inhibits activation of human primordial follicles in vitro. J Assist Reprod Genet2010; 27: 141–7.
62. Torrance C, Telfer EE and Gosden RG. Quantitative study of the development of isolated mouse preantral follicles in collagen gel culture. J Reprod Fertil1989; 87: 367–74.
63. Telfer EE, Torrance C and Gosden RG. A morphological study of cultured preantral ovarian follicles after transplantation under the kidney capsule. J Reprod Fertil1990; 89: 565–71.
64. Telfer EE.The development of methods for isolation and culture of preantral follicles from bovine and porcine ovaries. Theriogenology 1996; 45: 101–10.
65. Park KS, Lee TH, Park YK, Song HB and Chun SS. Effects of isolating methods (mechanical or enzymatical) on structure of pre-antral follicles in mouse. J Assist Reprod Genet2005; 22: 355–9.
66. Demeestere I, Delbaere A, Gervy C et al. Effect of preantral follicle isolation technique on in-vitro follicular growth, oocyte maturation and embryo development in mice. Hum Reprod2002; 17: 2152–9.
67. Telfer EE, Binnie JP, McCaffery FH and Campbell B. In vitro development of oocytes from porcine and bovine primary follicles. Mol Cell Endocrinol2000; 25: 117–23.
68. Wandji SA, Eppig JJ and Fortune JE. FSHand growth factors affect the growth and endocrine function in vitro of granulosa cells of bovine preantral follicles. Theriogenology1996; 45: 817–32.
69. Dolmans MM, Michaux N, Camboni A et al. Evaluation of Liberase, a purified enzyme blend, for the isolation of human primordial and primary ovarian follicles. Hum Reprod2006; 21: 413–20.
70. Dolmans MM, Yuan WY, Camboni A et al. Development of antral follicles after xenografting of isolated small human preantral follicles. Reprod Biomed Online2008; 16: 705–11.
71. Rice S, Ojha K and Mason H. Human ovarian biopsies as a viable source of pre-antral follicles. Hum Reprod2008; 23: 600–5.
72. Gosden RG, Mullan J, Picton HM, Yin H and Tan SL. Current perspective on primordial follicle cryopreservation and culture for reproductive medicine. Hum Reprod Update2002; 8: 105–10.
73. Muruvi W, Picton HM, Rodway RG and Joyce IM. In vitro growth of oocytes from primordial follicles isolated from frozen–thawed lamb ovaries. Theriogenology2005; 64: 1357–70.
74. Gosden RG and Telfer E. Numbers of follicles and oocytes in mammalian ovaries and their allometric relationships. J Zool London1987; 211: 169–75.
75. Telfer EE, Binnie JP and Jordan LB. Effect of follicle size on the onset of apoptotic cell death in cultured bovine ovarian follicles.Theriogenology1998; 49: 357.
76. Gutierrez CG, Ralph JH, Telfer EE, Wilmut I and Webb R. Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biol Reprod2000; 62: 1322–8.
77. Thomas FH, Armstrong DG, Campbell BK and Telfer EE. Effects of IGF-1 bioavailability on bovine preantral follicular development in vitro. Reproduction2007; 133: 1121–8.
78. Walters KA, Campbell BK, Armstrong DG and Telfer EE The effects of IGF-I on bovine follicle development and IGFBP-2 expression are dose and stage dependent. Reproduction2006; 131: 515–23.
79. Itoh T, Kacchi M, Abe H, Sendai Y and Hoshi H. Growth, antrum formation, and estradiol production of bovine preantral follicles cultured in a serum-free medium. Biol Reprod2002; 67: 1099–105.
80. Hirao Y, Itoh T, Shimizu M et al. In vitro growth and development of bovine oocyte–granulosa cell complexes on the flat substratum: effects of high polyvinylpyrrolidone concentration in culture medium. Biol Reprod2004; 70: 83–91.
81. Heise M, Koepsel R, Russell AJ and McGee EA. Calcium alginate microencapsulation of ovarian follicles impacts FSH delivery and follicle morphology. Reprod Biol Endocrinol2005; 3: 47.
82. Xu M, West E, Shea LD and Woodruff TK. Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development. Biol Reprod2006; 75: 916–23.
83. Oktay K, Nugent D, Newton H et al. Isolation and characterization of primordial follicles from fresh and cryopreserved human ovarian tissue. Fertil Steril1997; 67: 481–6.
84. Donnez J, Dolmans MM, Demylle D et al. Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet2004; 364: 1405–10.
85. Meirow D, Levron J, Eldar-Geva T et al. Pregnancy after transplantation of cryopreserved ovarian tissue in a patient with ovarian failure after chemotherapy. N Engl J Med2005; 353: 318–21.
86. Amorim CA, Van Langendonckt A, David A, Dolmans MM and Donnez J. Survival of human preantral follicles after cryopreservation of ovarian tissue, follicular isolation and in vitro culture in a calcium alginate matrix. Human Reprod2009; 24: 92–9.
87. Gook DA, McCully BA, Edgar DH and McBain JH. Development of antral follicles in human cryopreserved ovarian tissue following xenografting. Hum Reprod2001; 16: 417–22.
88. Moor RM, Dai Y, Lee C and Fulka J Jr. Oocyte maturation and embryonic failure. Hum Reprod Update1998; 4: 223–36.
89. Banwell KM and Thompson JG. In vitromaturation of mammalian oocytes: outcomes and consequences. Semin Reprod Med2008; 26: 162–74.
90. Combelles CM, Fissore RA, Albertini DF and Racowsky C. In vitro maturation of human oocytes and cumulus cells using a coculture three-dimensional collagen gel system. Hum Reprod2005; 20: 1349–58.
91. Eppig JJ, O’Brien MJ, Wigglesworth K et al. Effect of in vitro maturation of mouse oocytes on the health and lifespan of adult offspring. Hum Reprod2009; 24: 922–8