ABSTRACT
Tissue banking of ovarian material is being increasingly offered to a variety of patients as a means of fertility preservation. This tissue comprises thin cortical surface biopsies that contain predominantly primordial follicles, and currently the only option to restore fertility is by transplantation. However, this is not a viable option for all patients. The potential of this tissue could be realized by the development of in vitro systems to support complete growth from the early primordial stages through to maturity. This technology would have many therapeutic applications including the production of competent oocytes for assisted reproduction technologies, determination of toxicological effects on germ cell development, assessment of cryopreserved ovarian tissue before transplantation for fertility preservation as well as providing an experimental model to address basic scientific questions concerning human oocyte development. Complete oocyte development in vitro from the primordial stage has been achieved in mice, but the larger size and longer growth period of human follicles has made the interspecies translation of these techniques difficult. Recently progress has been made in defining conditions that support different stages of follicle development in vitro that make a complete in vitro system from primordial to maturation a possible reality. This article deals with our current understanding of in vitro development.
KEYWORDS
Human - primordial - preantral - oocyte - in vitro - cryopreservation - antral
REFERENCES
-
1
Zuckerman S.
The number of oocytes in the mature ovary.
Recent Prog Horm Res.
1951;
6
63-109
-
2
Tingen C M, Bristol-Gould S K, Kiesewetter S E, Wellington J T, Shea L, Woodruff T K.
Prepubertal primordial follicle loss in mice is not due to classical apoptotic pathways.
Biol Reprod.
2009;
81
(1)
16-25
-
3
Hardy K, Wright C S, Franks S, Winston R M.
In vitro maturation of oocytes.
Br Med Bull.
2000;
56
(3)
588-602
-
4
Hansen K R, Knowlton N S, Thyer A C, Charleston J S, Soules M R, Klein N A.
A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause.
Hum Reprod.
2008;
23
(3)
699-708
-
5
Gougeon A.
Regulation of ovarian follicular development in primates: facts and hypotheses.
Endocr Rev.
1996;
17
(2)
121-155
-
6
Gougeon A, Chainy G B.
Morphometric studies of small follicles in ovaries of women at different ages.
J Reprod Fertil.
1987;
81
(2)
433-442
-
7
Picton H M, Harris S E, Muruvi W, Chambers E L.
The in vitro growth and maturation of follicles.
Reproduction.
2008;
136
(6)
703-715
-
8
Thomas F H, Walters K A, Telfer E E.
How to make a good oocyte: an update on in vitro models to study follicle regulation.
Hum Reprod Update.
2003;
9(6)
541-555
-
9
Eppig J J, Schroeder A C.
Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro.
Biol Reprod.
1989;
41
(2)
268-276
-
10
Eppig J J, O'Brien M J.
Development in vitro of mouse oocytes from primordial follicles.
Biol Reprod.
1996;
54
(1)
197-207
-
11
O'Brien M J, Pendola J K, Eppig J J.
A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence.
Biol Reprod.
2003;
68
(5)
1682-1686
-
12
Spears N, Boland N I, Murray A A, Gosden R G.
Mouse oocytes derived from in vitro grown primary ovarian follicles are fertile.
Hum Reprod.
1994;
9
(3)
527-532
-
13
Telfer E E, McLaughlin M, Ding C, Thong K J.
A two-step serum-free culture system supports development of human oocytes from primordial follicles in the presence of activin.
Hum Reprod.
2008;
23
(5)
1151-1158
-
14
Hovatta O, Silye R, Abir R, Krausz T, Winston R M.
Extracellular matrix improves survival of both stored and fresh human primordial and primary ovarian follicles in long-term culture.
Hum Reprod.
1997;
12
(5)
1032-1036
-
15
Hovatta O, Wright C, Krausz T, Hardy K, Winston R M.
Human primordial, primary and secondary ovarian follicles in long-term culture: effect of partial isolation.
Hum Reprod.
1999;
14
(10)
2519-2524
-
16
Picton H M, Gosden R G.
In vitro growth of human primordial follicles from frozen-banked ovarian tissue.
Mol Cell Endocrinol.
2000;
166
(1)
27-35
-
17
Wright C S, Hovatta O, Margara R et al..
Effects of follicle-stimulating hormone and serum substitution on the in-vitro growth of human ovarian follicles.
Hum Reprod.
1999;
14
(6)
1555-1562
-
18
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 Genet.
2004;
21
(8)
301-306
-
19
Abir R, Franks S, Mobberley M A, Moore P A, Margara R A, Winston R M.
Mechanical isolation and in vitro growth of preantral and small antral human follicles.
Fertil Steril.
1997;
68
(4)
682-688
-
20
Abir R, Roizman P, Fisch B et al..
Pilot study of isolated early human follicles cultured in collagen gels for 24 hours.
Hum Reprod.
1999;
14
(5)
1299-1301
-
21
Xu M, Barrett S L, West-Farrell E et al..
In vitro grown human ovarian follicles from cancer patients support oocyte growth.
Hum Reprod.
2009;
24
(10)
2531-2540
-
22
Otala M, Mäkinen S, Tuuri T et al..
Effects of testosterone, dihydrotestosterone, and 17beta-estradiol on human ovarian tissue survival in culture.
Fertil Steril.
2004;
82
(Suppl 3)
1077-1085
-
23
Roy S K, Treacy B J.
Isolation and long-term culture of human preantral follicles.
Fertil Steril.
1993;
59
(4)
783-790
-
24
Alak B M, Coskun S, Friedman C I, Kennard E A, Kim M H, Seifer D B.
Activin A stimulates meiotic maturation of human oocytes and modulates granulosa cell steroidogenesis in vitro.
Fertil Steril.
1998;
70
(6)
1126-1130
-
25
Mikkelsen A L, Smith S D, Lindenberg S.
In-vitro maturation of human oocytes from regularly menstruating women may be successful without follicle stimulating hormone priming.
Hum Reprod.
1999;
14
(7)
1847-1851
-
26
Cha K Y, Chian R C.
Maturation in vitro of immature human oocytes for clinical use.
Hum Reprod Update.
1998;
4
(2)
103-120
-
27
Barnes F L, Crombie A, Gardner D K et al..
Blastocyst development and birth after in-vitro maturation of human primary oocytes, intracytoplasmic sperm injection and assisted hatching.
Hum Reprod.
1995;
10
(12)
3243-3247
-
28
Cha K Y, Koo J J, Ko J J, Choi D H, Han S Y, Yoon T K.
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 Steril.
1991;
55
(1)
109-113
-
29
Telfer E, Ansell J D, Taylor H, Gosden R G.
The number of clonal precursors of the follicular epithelium in the mouse ovary.
J Reprod Fertil.
1988;
84
(1)
105-110
-
30
Telfer E E, McLaughlin M.
Natural history of the mammalian oocyte.
Reprod Biomed Online.
2007;
15
(3)
288-295
-
31
Albertini D F, Barrett S L.
Oocyte-somatic cell communication.
Reprod Suppl.
2003;
61
49-54
-
32
Albertini D F, Combelles C M, Benecchi E, Carabatsos M J.
Cellular basis for paracrine regulation of ovarian follicle development.
Reproduction.
2001;
121
(5)
647-653
-
33
Makabe S, Naguro T, Stallone T.
Oocyte-follicle cell interactions during ovarian follicle development, as seen by high resolution scanning and transmission electron microscopy in humans.
Microsc Res Tech.
2006;
69
(6)
436-449
-
34
Gosden R G, Telfer E E.
Scaling of follicular sizes in mammalian ovaries.
J Zool.
1987;
211
157-168
-
35
Rodrigues P, Limback D, McGinnis L K, Plancha C E, Albertini D F.
Oogenesis: prospects and challenges for the future.
J Cell Physiol.
2008;
216
(2)
355-365
-
36
Fortune J E.
The early stages of follicular development: activation of primordial follicles and growth of preantral follicles.
Anim Reprod Sci.
2003;
78
(3-4)
135-163
-
37
Fair T, Hyttel P, Greve T.
Bovine oocyte diameter in relation to maturational competence and transcriptional activity.
Mol Reprod Dev.
1995;
42
(4)
437-442
-
38
Hyttel P, Fair T, Callesen H, Greve T.
Oocyte growth, capacitation and final maturation in cattle.
Theriogenology.
1997;
47
23-32
-
39
Van Blerkom J, Davis P, Mathwig V, Alexander S.
Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos.
Hum Reprod.
2002;
17
(2)
393-406
-
40
Moor R M, Dai Y, Lee C, Fulka Jr J.
Oocyte maturation and embryonic failure.
Hum Reprod Update.
1998;
4
(3)
223-236
-
41
Adhikari D, Liu K.
Molecular mechanisms underlying the activation of mammalian primordial follicles.
Endocr Rev.
2009;
30
(5)
438-464
-
42
McLaughlin E A, McIver S C.
Awakening the oocyte: controlling primordial follicle development.
Reproduction.
2009;
137
(1)
1-11
-
43
Yang M Y, Fortune J E.
Vascular endothelial growth factor stimulates the primary to secondary follicle transition in bovine follicles in vitro.
Mol Reprod Dev.
2007;
74
(9)
1095-1104
-
44
Yang M Y, Fortune J E.
Testosterone stimulates the primary to secondary follicle transition in bovine follicles in vitro.
Biol Reprod.
2006;
75
(6)
924-932
-
45
Fortune J E, Kito S, Wandji S A, Srsen V.
Activation of bovine and baboon primordial follicles in vitro.
Theriogenology.
1998;
49
(2)
441-449
-
46
Wandji S A, Srsen V, Nathanielsz P W, Eppig J J, Fortune J E.
Initiation of growth of baboon primordial follicles in vitro.
Hum Reprod.
1997;
12
(9)
1993-2001
-
47
Wandji S A, Srsen V, Voss A K, Eppig J J, Fortune J E.
Initiation in vitro of growth of bovine primordial follicles.
Biol Reprod.
1996a;
55
(5)
942-948
-
48
Abir R, Fisch B, Jin S, Barnnet M, Kessler-Icekson G, Ao A.
Expression of stem cell factor and its receptor in human fetal and adult ovaries.
Fertil Steril.
2004;
82
(Suppl 3)
1235-1243
-
49
Abir R, Ben-Haroush A, Melamed N, Felz C, Krissi H, Fisch B.
Expression of bone morphogenetic proteins 4 and 7 and their receptors IA, IB, and II in human ovaries from fetuses and adults.
Fertil Steril.
2008;
89
(5, Suppl)
1430-1440
-
50
Abir R, Fisch B, Jin S et al..
Immunocytochemical detection and RT-PCR expression of leukaemia inhibitory factor and its receptor in human fetal and adult ovaries.
Mol Hum Reprod.
2004;
10
(5)
313-319
-
51
Martins da Silva S J, Bayne R AL, Cambray N, Hartley P S, McNeilly A S, Anderson R A.
Expression of activin subunits and receptors in the developing human ovary: activin A promotes germ cell survival and proliferation before primordial follicle formation.
Dev Biol.
2004;
266
(2)
334-345
-
52
Reddy P, Liu L, Adhikari D et al..
Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool.
Science.
2008;
319
(5863)
611-613
-
53
Liu K, Rajareddy S, Liu L et al..
Control of mammalian oocyte growth and early follicular development by the oocyte PI3 kinase pathway: new roles for an old timer.
Dev Biol.
2006;
299
(1)
1-11
-
54
Yaba A, Bianchi V, Borini A, Johnson J.
A putative mitotic checkpoint dependent on mTOR function controls cell proliferation and survival in ovarian granulosa cells.
Reprod Sci.
2008;
15
(2)
128-138
-
55
Telfer E E, McLaughlin M, Kini S, Thong K J, Anderson R A, Johnson J.
Inhibition of mTOR kinase in cultured human ovarian cortex results in altered follicle dynamics.
Hum Reprod.
2009;
24
(1, Suppl)
197
-
56
Elvin J A, Yan C, Wang P, Nishimori K, Matzuk M M.
Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary.
Mol Endocrinol.
1999;
13
(6)
1018-1034
-
57
Dong J, Albertini D F, Nishimori K, Kumar T R, Lu N, Matzuk M M.
Growth differentiation factor-9 is required during early ovarian folliculogenesis.
Nature.
1996;
383
(6600)
531-535
-
58
Li T Y, Colley D, Barr K J, Yee S P, Kidder G M.
Rescue of oogenesis in Cx37-null mutant mice by oocyte-specific replacement with Cx43.
J Cell Sci.
2007;
120
(Pt 23)
4117-4125
-
59
Telfer E E, McLaughlin M, Keros V, Carlsson I B, Thong K J, Hovatta O.
Accelerated development of primordial follicles from vitrified human ovarian tissue within a two-step serum free culture system.
Hum Reprod.
2008;
23
97
-
60
Durinzi K L, Saniga E M, Lanzendorf S E.
The relationship between size and maturation in vitro in the unstimulated human oocyte.
Fertil Steril.
1995;
63
(2)
404-406
-
61
Cavilla J L, Kennedy C R, Byskov A G, Hartshorne G M.
Human immature oocytes grow during culture for IVM.
Hum Reprod.
2008;
23
(1)
37-45
-
62
Torrance C, Telfer E E, Gosden R G.
Quantitative study of the development of isolated mouse pre-antral follicles in collagen gel culture.
J Reprod Fertil.
1989;
87
(1)
367-374
-
63
Telfer E E, Torrance C, Gosden R G.
Morphological study of cultured preantral ovarian follicles of mice after transplantation under the kidney capsule.
J Reprod Fertil.
1990;
89
(2)
565-571
-
64
Telfer E E.
The development of methods for isolation and culture of preantral follicles from bovine and porcine ovaries.
Theriogenology.
1996;
45
101-110
-
65
Park K S, Lee T H, Park Y K, Song H B, Chun S S.
Effects of isolating methods (mechanical or enzymatical) on structure of pre-antral follicles in mouse.
J Assist Reprod Genet.
2005;
22
(9-10)
355-359
-
66
Demeestere I, Delbaere A, Gervy C, Van Den Bergh M, Devreker F, Englert Y.
Effect of preantral follicle isolation technique on in-vitro follicular growth, oocyte maturation and embryo development in mice.
Hum Reprod.
2002;
17
(8)
2152-2159
-
67
Telfer E E, Binnie J P, McCaffery F H, Campbell B K.
In vitro development of oocytes from porcine and bovine primary follicles.
Mol Cell Endocrinol.
2000;
163
(1-2)
117-123
-
68
Wandji S A, Eppig J J, Fortune J E.
FSH and growth factors affect the growth and endocrine function in vitro of granulosa cells of bovine preantral follicles.
Theriogenology.
1996;
45
(4)
817-832
-
69
Dolmans M M, Michaux N, Camboni A et al..
Evaluation of Liberase, a purified enzyme blend, for the isolation of human primordial and primary ovarian follicles.
Hum Reprod.
2006;
21
(2)
413-420
-
70
Dolmans M M, Yuan W Y, Camboni A et al..
Development of antral follicles after xenografting of isolated small human preantral follicles.
Reprod Biomed Online.
2008;
16
(5)
705-711
-
71
Rice S, Ojha K, Mason H.
Human ovarian biopsies as a viable source of pre-antral follicles.
Hum Reprod.
2008;
23
(3)
600-605
-
72
Oktay K, Nugent D, Newton H, Salha O, Chatterjee P, Gosden R G.
Isolation and characterization of primordial follicles from fresh and cryopreserved human ovarian tissue.
Fertil Steril.
1997;
67
(3)
481-486
-
73
Amorim C A, Van Langendonckt A, David A, Dolmans M M, Donnez J.
Survival of human pre-antral follicles after cryopreservation of ovarian tissue, follicular isolation and in vitro culture in a calcium alginate matrix.
Hum Reprod.
2009;
24
(1)
92-99
-
74
Gosden R G, Mullan J, Picton H M, Yin H, Tan S L.
Current perspective on primordial follicle cryopreservation and culture for reproductive medicine.
Hum Reprod Update.
2002;
8
(2)
105-110
-
75
Muruvi W, Picton H M, Rodway R G, Joyce I M.
In vitro growth of oocytes from primordial follicles isolated from frozen-thawed lamb ovaries.
Theriogenology.
2005;
64
(6)
1357-1370
-
76
Gosden R G, Telfer E.
Numbers of follicles and oocytes in mammalian ovaries and their allometric relationships.
J Zool (Lond).
1987;
211
169-175
-
77
Telfer E E, Binnie J P, Jordan L B.
Effect of follicle size on the onset of apoptotic cell death in cultured bovine ovarian follicles.
Theriogenology.
1998;
49
357
-
78
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 Reprod.
2008;
23
(5)
1007-1013
-
79
Gutierrez C G, Ralph J H, Telfer E E, Wilmut I, Webb R.
Growth and antrum formation of bovine preantral follicles in long-term culture in vitro.
Biol Reprod.
2000;
62
(5)
1322-1328
-
80
McCaffery F H, Leask R, Riley S C, Telfer E E.
Culture of bovine preantral follicles in a serum-free system: markers for assessment of growth and development.
Biol Reprod.
2000;
63
(1)
267-273
-
81
Thomas F H, Leask R, Sršen V, Riley S C, Spears N, Telfer E E.
Effect of ascorbic acid on health and morphology of bovine preantral follicles during long-term culture.
Reproduction.
2001;
122
487-495
-
82
Thomas F H, Armstrong D G, Campbell B K, Telfer E E.
Effects of IGF -1 bioavailability on bovine preantral follicular development in vitro.
Reproduction.
2007;
133
(6)
1121-1128
-
83
Walters K A, Binnie J P, Campbell B K, Armstrong D G, Telfer E E.
The effects of IGF-I on bovine follicle development and IGFBP-2 expression are dose and stage dependent.
Reproduction.
2006;
131
(3)
515-523
-
84
Itoh T, Kacchi M, Abe H, Sendai Y, Hoshi H.
Growth, antrum formation, and estradiol production of bovine preantral follicles cultured in a serum-free medium.
Biol Reprod.
2002;
67
(4)
1099-1105
-
85
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 Reprod.
2004;
70
(1)
83-91
-
86
Heise M, Koepsel R, Russell A J, McGee E A.
Calcium alginate microencapsulation of ovarian follicles impacts FSH delivery and follicle morphology.
Reprod Biol Endocrinol.
2005;
3
47
-
87
Xu M, West E, Shea L D, Woodruff T K.
Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development.
Biol Reprod.
2006;
75
(6)
916-923
-
88
Donnez J, Dolmans M M, Demylle D et al..
Livebirth after orthotopic transplantation of cryopreserved ovarian tissue.
Lancet.
2004;
364
(9443)
1405-1410
-
89
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 Med.
2005;
353
(3)
318-321
-
90
Gook D A, McCully B A, Edgar D H, McBain J C.
Development of antral follicles in human cryopreserved ovarian tissue following xenografting.
Hum Reprod.
2001;
16
(3)
417-422
-
91
Banwell K M, Thompson J G.
In vitro maturation of mammalian oocytes: outcomes and consequences.
Semin Reprod Med.
2008;
26
(2)
162-174
-
92
Combelles C M, Fissore R A, Albertini D F, Racowsky C.
In vitro maturation of human oocytes and cumulus cells using a co-culture three-dimensional collagen gel system.
Hum Reprod.
2005;
20
(5)
1349-1358
Evelyn E TelferPh.D.
Centre for Integrative Physiology, University of Edinburgh, Hugh Robson Building
George Square, Edinburgh EH8 9XD, UK
Email: evelyn.telfer@ed.ac.uk
