Vol. 6, No. 1
3
REVIEW
Recent achievements in in vitro culture and
preservation of ovarian follicles in mammals
Lucyna Kątska-Książkiewicz1
Department of Biotechnology of Animal Reproduction, National
Research Institute of Animal Production, Balice, Poland
Received: 12 December 2005; accepted: 25 February 2006
SUMMARY
The mammalian ovary contains a large number of follicles that are in
various developmental stages. The largest portion of them are primordial
follicles. However, throughout the female reproductive lifespan only
a small proportion of these follicles will produce oocytes competent to
undergo successful maturation and ovulation. The rest of the ovarian
oocytes (>99.9%) undergo atresia. It would be of great practical benefit
to rescue some of these follicles by growing them in culture in order
to provide an extra source of gametes. There is considerable interest in
developing technologies that aim to produce fully-grown, developmentally
competent oocytes from a pool of early developmental stages of follicles.
Two methods have been used: 1/ long-term in vitro culture of either
follicles or oocytes, and 2/ transplantation of ovarian tissue grafts. The
development of efficient technologies may provide an additional source of
oocytes for livestock production and reproduction in humans and rare or
endangered species. The aim of this paper is to present a comprehensive
1
Address for correspondence: Department of Biotechnology of Animal Reproduction, National
Research Institute of Animal Production, Krakowska Street 1, 32-083 Balice;
e-mail: [email protected]
Copyright © 2006 by the Society for Biology of Reproduction
4
Culture and preservation of ovarian follicles
review of recent achievements in the utilization of small ovarian follicles
(primordial, preantral and early antral) by long-term in vitro culture and/
or transplantation of ovarian tissue grafts (fresh and cryopreserved) in
mammals including humans. Reproductive Biology 2006 6 (1): 3–16.
Key words: ovary, follicles, long-term culture, ovarian grafts, cryopreservation, transplantation
INTRODUCTION
Efforts to increase the utilization of reproductive potential in mammals
have been made by means of multiple ovulation and embryo transfer
procedures and, more recently, by in vitro embryo production (IVP). Both
procedures, however, utilized only a small portion of the available follicles.
Mammalian ovaries contain thousands of oocytes which are enclosed
in non-growing (primordial) and growing follicles that are in various
developmental stages. Normal follicular development of an oocyte that is
capable of maturation, fertilization and embryonic development depends
upon a complex sequence of cellular interactions within the follicle. These
interactions create a unique and progressively shifting environment during
the development of the oocyte. At any stage during this development, the
follicle may continue to develop normally or, more frequently, proceed
toward atresia.
In cattle, approximately 235 000 small, non-growing and growing
oocytes are enclosed in ovarian follicles of a newborn calf and 130 000
in a heifer’s ovaries [19]. However, a population of bovine females, as
other mammalians, is characterized by extreme individual variation. The
limits of this variation within the population sampled between birth and
24 months of age were zero (sterile) and 700 000 germ cells [19]. The
largest and relatively stable pool among them is constituted by primordial
follicles. When non-growing oocytes (with a diameter of 30 μm) enclosed
in primordial follicles enter the growth phase, their growth to the final size
(125 μm) takes a long time [5, 39]. However, throughout the reproductive
lifespan of a mammalian female, only a limited number of follicles grow
Kątska-Książkiewicz
5
to full size when their oocytes successfully mature and are ovulated.
Most ovarian follicles (>99.9%) gradually become atretic [19, 57]. In the
ovary, there is a greater number of early antral follicles than follicles at
more advanced growth stages. The large store of these follicles creates a
potential source of oocytes for biotechnological purposes. It would be of
great practical benefit to rescue some of these follicles by growing them
in culture in order to provide an extra source of oocytes. Such oocytes
can be used, for example, for the multiplication of domestic animals of
high genetic merit; conservation programs for rare or endangered animal
species; and conservation of fertility and assisted conception in humans.
As an alternative to long-term in vitro culture, transplantation of
cryopreserved or fresh grafts of ovarian cortical tissue can be applied.
Preservation of reproductive potential has been demonstrated in several
species with numerous live young produced following transplantation of
ovarian tissue in rodents [8, 14, 37, 38, 51-53, 61, 69], small mammals
[2, 12, 13, 42], farm animals [1, 24, 29, 56, 58-60] and monkeys [36].
In 2004, the first live birth in humans after orthotopic transplantation of
cryopreserved ovarian tissue was reported [15].
Long-term culture of ovarian follicles
Predictable production of fully competent oocytes depends on utilization
of appropriate biotechnology techniques. Currently, oocyte availability
in cattle is limited to a small number of antral follicles (with diameter
2 to 8 mm) present in the ovary. An alternative option is to recover
smaller follicles, which are not developmentally competent at the time
of recovering ovaries, and carry out in vitro culture of these follicles or
oocytes. Studies involving isolation of ovarian follicles and analysis of the
culture requirements, metabolism, and differentiation processes in in vitro
conditions have already been undertaken using rodents as experimental
models [6, 9, 17, 18, 47, 63, 72].
Preantral and early antral follicles. Several culture systems have been
successfully used to support long-term culture of follicles in mice [9, 17,
6
Culture and preservation of ovarian follicles
18, 47, 63, 72]. The first live mouse pup was obtained from the culture
of oocyte-granulosa cell complexes isolated from neonatal primordial
follicles using a complex two-step culture system developed by Eppig and
O’Brien [18]. However, the birth of offspring derived from primordial and
preantral follicles cultured entirely in vitro has been reported only for mice
[17, 18, 47]. Many attempts have been made to apply these methods in
farm animals in order to establish a complete in vitro system for preantral
follicles.
In contrast to the variety of systems established for production of mouse
oocytes, the developmental competence in vitro of oocytes originating from
preantral follicles of human or domestic animals ovaries has not yet been
so successful. The reason is that the ovulatory size of a mouse follicle is
only 0.5 mm in diameter, whereas in cattle the ovulatory size is larger than
1.6 cm. Secondly, the length of time taken for cultured murine preantral
follicles to grow to Graafian follicles is six days, which corresponds to the
length of time taken by follicles in vivo. In contrast, follicular development
in cattle and sheep from the preantral stages to ovulatory size can take a
number of months [5, 39]. Luissier et al [39] showed that a bovine follicle
which has formed an antrum needs 40 days to reach ovulatory size. By
extrapolation of these data it was estimated that the preantral stage follicle
(primary or secondary) requires at least 60 to 80 days to reach maturity
and the primordial stage requires at least 100 days [5, 39]. Thirdly, various
factors might influence the culture of farm animal follicles such as age
of animal, species, stage of follicle development and size, as well as the
presence of a thick theca, which restricts the transport of nutrients and gases
during the long-term culture period required for follicle growth. Finally,
other factors affecting the culture of preantral follicles of farm animals
are related to the technique of follicles isolation which has appeared to
be more time consuming and difficult than that in rodents, mainly due to
the tough, fibrous structure of the ovary. The above limitations may partly
explain why the research was primary focused on the growth of follicles
but not on the quality of their oocytes.
In cattle, as in other farm animals, in vitro follicle culture conditions are
not yet optimal, as the meiotic and developmental competence of oocytes
Kątska-Książkiewicz
7
from cultured follicles is far below what one would expect from healthy
in vivo grown follicles. Up to now, embryos have been produced from in
vitro-grown oocytes of porcine preantral follicles with diameter 0.3 mm
[71], and live births have been reported from in vitro-grown oocytes of
bovine small antral follicles, with a diameter larger than 0.5 mm [27, 73].
However, when bovine follicles smaller than 0.5 mm in diameter were
used, only limited success was achieved [10, 11, 24-33, 41, 46, 67, 68, 73].
Problems may arise because these bovine preantral follicles require a longer
growth period and different culture conditions in order to achieve complete
growth and development. Obtaining meiotically competent oocytes from
cultured preantral and early antral follicles requires not only the viable
oocyte and the granulosa cells, but also the presence of gap junctions and
metabolic cooperation between these cells. This is essential for oocyte
growth and development. Indeed, the oocyte development depends on
the surrounding granulosa cells which provide nutrients via extensive
gap junctions. Also, granulosa cell contact with oocyte is essential to the
maintenance of the oocyte in meiotic arrest. The removal of granulosa
cells or disruption of the gap junction communications between granulosa
cells and the oocyte, results in spontaneous germinal vesicle breakdown
and leads to degeneration [16].
In studies with ovine oocyte-granulosa cell complexes [46] it has been
demonstrated that cells migrated away from the oocytes in the complexes that
had lost their spherical shape. These findings and my personal observation on
the culture of bovine oocyte-granulosa complexes [30-33] suggest that it is
more difficult in in vitro conditions to maintain the proper association between
the oocyte and granulosa cells in large animal species than in mice. During
the long-term culture of bovine oocyte-granulosa complexes, the majority
of granulosa cells migrate out of the follicle or follicle-like structures. The
oocyte becomes denuded of cumulus cells, which could drastically reduce
its quality and competence [32, 43, 73]. Unfortunately, some recent reports
describing preantral follicle culture have given no information concerning
oocyte quality and competence [25, 28, 72].
In sheep, Newton et al [46] analyzed the capacity of enzymatically
isolated cumulus-oocyte complexes (COCs) to form antrum and to release
8
Culture and preservation of ovarian follicles
estradiol. There is no information provided on the oocyte meiotic or
developmental competence.
In cattle, it has been shown [55, 67, 68] that preantral follicles with a
diameter of 35 to 100 μm survived in culture for six or seven days, but the
quality of oocyte ultrastructure appeared to be unsatisfactory, not only after
culture but even immediately after follicle isolation [55, 67, 68]. Bovine
late preantral and early antral follicles with a diameter approx. 170 μm can
grow and survive in vitro even up to 23 days [30, 33]. After 14 days of
intact follicle culture, meiotic arrest was preserved in 71.9% of enclosed
oocytes [33]. Frequency of the germinal vesicle stage did not significantly
differ among oocytes evaluated immediately after follicle dissection from
the ovary and those cultured in the intact follicle for 6, 8, 11 or 14 days
[33]. The comparison of meiotic competence of oocytes from early antral
follicles with diameter 0.2 to 0.4 mm and 0.4 to 0.7 mm subjected to
in vitro maturation (IVM) following long-term growth culture [31, 32]
showed that a higher proportion of oocytes from the larger follicles mature
to metaphase-I (30.9%), telophase I (1.8%) and metaphase-II (18.2%)
compared to oocytes from follicles 0.2 to 0.4 mm that mature only to
metaphase-I (15.4%).
Up to now the greatest degree of success in in vitro growth culture of
bovine oocytes has been associated with the culture of cumulus-oocyte
complexes surrounded with parietal granulosa cells (COCGs), isolated
from relatively large, early antral follicles with a diameter of 0.5 to 0.7 mm,
followed by maturation of isolated COCs and in vitro fertilization (IVF;
[26, 27, 33, 43, 73]). Harada et al [26] reported that 70% of bovine oocytes
isolated from early antral follicles 0.5-0.7 mm in diameter showed normal
morphology after eight days of culture, and increased in diameter (from
95.9±2.8 to 117.7±9.7 µm). The overall maturation potential (percentage
of metaphase II oocytes) was 7 and 11% after 7 and 11 days of culture,
respectively.
Furthermore, using a similar follicle culture system, Miyano [43]
reported that only 5% of the oocytes showed developmental competence
to the blastocyst stage after IVF. In a recent study by Hirao et al [27]
bovine oocytes (with a mean diameter of 95 μm) originating from follicles
Kątska-Książkiewicz
9
of 0.5-0.7 mm in diameter were cultured on the flat substratum in medium
supplemented with polyvinylpyrrolidione (PVP). The described culture
system [27] allowed improving the efficiency of oocyte development to
the blastocyst stage to 12%. The calves were only born from the cultured
COCGs originating from early antral follicles with diameter 0.5 to 0.7 mm
[27, 73].
When preantral follicles from prepubertal sheep were cultured,
only 4 to 5% of oocytes from these follicles reached metaphase II after
subsequent in vitro maturation [10]. Porcine preantral follicles (200 to 310
µm in diameter) have been cultured to the antral stage, and after culture for
four days, 51% of oocytes from these follicles were capable of reaching
metaphase II after subsequent IVM [71]. Therefore, a variable efficiency
in acquisition of maturational competence by in vitro grown oocytes of
different species has been observed.
Primordial follicles. The largest proportion of ovarian follicles are resting,
primordial follicles. Presently, the complete methods of in vitro growth
of these follicles in large animals have not been developed. The first
successful experiment in which a mouse pup was obtained from an oocyte
in primordial follicle has been carried out by Eppig and O’Brien [18]. In
this experiment primordial follicles were grown to full-grown stage by
two culture methods: organ culture followed by 14-day in vitro culture of
isolated complexes of oocyte-granulosa cells. The resulting fully grown
oocytes were used for in vitro maturation and fertilization, then developing
embryos were transferred to recipient females and one pup was born.
Regardless of the low efficiency of the procedure (1 mouse out of 190
embryos) this result opened the possibility of utilizing primordial follicles
as a potential source of oocytes in mice, as well as other mammalian species.
It is also convenient and important that cryostorage of ovarian tissue
can be successfully applied [24, 44, 46, 48, 49, 54]. Our understanding
of primordial follicle activation and early follicle and oocyte growth has
progressed to some extent using organ culture of ovarian cortical slices in
large animal species [5] and whole ovary culture in rodents [18]. These
culture systems remain poorly defined because they contain a wide range
10
Culture and preservation of ovarian follicles
of cell types. In addition, because of the size of the tissue samples being
cultured, oxygen and nutrient exchange problems may be difficult to
overcome with culture of cortical slices. On the other hand, culture of
isolated primordial follicles requires a culture system that is considerably
extended in time.
Muruvi et al [44] recently conducted investigations on enzymatically
isolated neonatal sheep primordial follicles. The cryopreserved follicles,
after thawing, were cultured on lectin-aggregates in a serum-free culture
system over 28 days and showed long-term survival and oocyte growth. This
achievement creates the basis for an in vitro growth system of oocytes from
primordial follicles of large animals, but it needs further investigations and
improvement. Up to now the only possible way of utilizing primordial follicles
can be achieved by a combination of xenografting and in vitro culture.
Cryopreservation and transplantation of ovarian grafts
Xenotransplantation of ovarian tissue grafts to nude or severe combined
immunodeficient (SCID) mice can be applied as a substitute for long-term
in vitro culture system. Mice homozygous for the SCID mutation lack
both humoral and cell-mediated immunity due to the absence of T and B
lymphocytes [3, 4]; therefore they readily accept ovarian tissue explants from
other mammalian species. It was first reported by Gosden et al in 1994 [24]
that sheep and cat follicles in ovarian xenografts survived and developed
to the antral stage in immunodeficient mice after several months. Recently,
xenografting of the ovaries of 3-week-old mice into rats was successful in
the generation of pups [61]. Cross-species transplantation of ovaries from
large mammals, including humans [21-23, 35, 70], monkeys [7], cows [60],
pigs [29], dogs [42] and marsupials [40] to recipient mice resulted in the
development of antral follicles and even mature oocytes. Preservation of
reproductive potential has been demonstrated in several mammalian species
with numerous live young produced following transplantation of fresh or
cryopreserved ovarian cortical tissue in mice [8, 14, 37, 38, 52, 61, 62, 69],
hamsters [51], rabbits [53], domestic cats [2], wombats [12, 13], sheep [1,
24, 56], pigs [29], cows [58-60] and monkeys [7].
Kątska-Książkiewicz
11
In humans, it has been known for several years that many young
women are likely to suffer ovarian failure as a consequence of aggressive
chemotherapy or radiotherapy treatments of malignant disease. The
possibility of circumventing this loss of fertility by cryopreserving ovarian
tissue prior to treatment has appeared to be possible. The preservation
of morphological integrity, growth and development of follicles in
transplanted grafts has been reported by several investigators [21-23, 34,
54, 65, 66]. In contrast to the ovarian grafts used in animal studies, which
were generally obtained from juvenile animals and exhibited uniform
follicle density, the human ovarian tissue is likely to be more variable
with respect to number of follicles, their distribution and fibrous content.
All these parameters may impact the cryopreservation and transplantation
outcome. Moreover, it is well established that there is a negative correlation
between primordial follicle density and patient’s age [20]. Therefore a
major factor in determining the likelihood of successful application of
ovarian graft transplantation is a collection of sufficient surface of grafts
for cryopreservation and storage. In order to cryopreserve approximately
1000 primordial and primary follicles it is necessary to dissect an ovarian
cortex with the thickness of approximately 1 mm and the surface area of
at least 3 mm2 before 10 years of age, 15 mm2 between 10 and 15 years
and 50 mm2 from 15 to 34 years [54]. It has been established that the
follicle survival rate was 74% after freezing, thawing and xenografting
[45]. Therefore approximately 700 follicles may be available from each
fragment. The size and number of ovarian tissue grafts should be adapted
accordingly to patient’s age.
Recently follicular growth from the primordial to the antral stage
has been observed within cryopreserved human ovarian tissue following
xenografting [21, 65, 66] and these follicles can undergo a normal response
to hormonal treatment [22, 35]. The autotransplantation of human ovarian
tissue may be done to the pelvic side wall [49], forearm and beneath the
skin of the abdomen [50]. In 2004, the first live birth after orthotopic
transplantation of cryopreserved ovarian tissue in humans was reported
[15]. This approach opens new perspectives for young cancer patients
facing premature ovarian failure. Ovarian tissue cryopreservation should
12
Culture and preservation of ovarian follicles
be an option offered to young women diagnosed with cancer, in conjunction
with other existing biotechnological methods for fertility preservation
such as immature oocyte retrieval, in vitro maturation of oocytes, in vitro
fertilization and embryo cryopreservation. Candidates for ovarian tissue
banking cannot have cancer, but, if they do, the malignancy must not involve
the ovaries or be in remission. Nevertheless, it may never be possible to
adopt a zero-risk policy with transplantation, and this conclusion will
continue to drive efforts to develop follicle culture technology.
There have been significant scientific advances in the field of
preservation and utilization of a pool of small ovarian follicles in mammals.
It has been expected that the emergent technologies may provide an
additional source of oocytes for livestock production and reproduction in
humans and endangered species. The preantral follicle culture system can
be applied as an in vitro assay in reproductive toxicology. This method
permits identifying direct and indirect effects of environmental chemicals
on the somatic compartment (follicle and theca cells) that may lead to
disturbances of oocyte growth and maturation or chromosome segregation
[64]. Therefore, preantral and early antral follicle culture and transplantation
of ovarian grafts appear to provide effective and reliable methods both for
laboratory and clinical applications.
ACKNOWLEDGEMENTS
The paper was supported by the statutory activity in the National Research
Institute of Animal Production, Poland.
REFERENCES
1.
2.
Baird DT, Webb R, Campbell BK, Harkness LM, Gosden RG 1999 Long-term ovarian function
in sheep after ovariectomy and transplantation of autografts stored at –196oC. Endocrinology
140 462-471.
Bosch P, Hernandez-Fonseca HJ, Miller DM, Wininger JD, Massey JB, Lamb SV, Brackett
BG 2004 Development of antral follicles in cryopreserved cat ovarian tissue transplanted to
immunodeficient mice. Theriogenology 61 581-594.
Kątska-Książkiewicz
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
13
Bosma MJ, Carroll AM 1991 The SCID mouse mutant: definition, characterization, and
potential uses. Annual Review of Immunology 9 323-350.
Bosma GC, Custer RP, Bosma MJ 1983 A severe combined immunodeficiency mutation in the
mouse. Nature 301 527-530.
Braw-Tal R, Yossefi S 1997 Studies in vivo and in vitro on the initiation of follicle growth in
the bovine ovary. Journal of Reproduction and Fertility 109 165-171.
Cain L, Chatterjee S, Collins TJ 1995 In vitro folliculogenesis of rat preantral follicles.
Endocrinology 136 3369-3377.
Candy CJ, Wood MJ, Whittingham DG 1995 Follicular development in cryopreserved
marmoset ovarian tissue after xenografting. Human Reproduction 10 2334-2338.
Candy CJ, Wood MJ, Whittingham DG 2000 Restoration of a normal reproductive lifespan
after grafting of cryopreserved mouse ovaries. Human Reproduction 15 1300-1304.
Carroll J, Whittingham DG, Wood MJ, Telfer E, Gosden RG 1990 Extra-ovarian production
of mature viable mouse oocytes from frozen primary follicles. Journal of Reproduction and
Fertility 90 321-327.
Cecconi S, Barboni B, Coccia M, Mattioli M 1999 In vitro development of sheep preantral
follicles. Biology of Reproduction 60 594-601.
Cecconi S, Capacchietti G, Russo V, Berardinell P, Mattioli M 2004 In vitro growth of preantral
follicles isolated from cryopreserved ovine ovarian tissue. Biology of Reproduction 70 12-17.
Cleary M, Paris MC, Shaw J, Jenkin G, Trounson AO 2003 Effect of ovariectomy and graft
position on cryopreserved common wombat (Vombatus ursinus) ovarian tissue following
xenografting to nude mice. Reproduction, Fertility and Development 15 333-342.
Cleary M, Shaw JM, Jenkin G, Trounson AO 2004 Influence of hormone environment and
donor age on cryopreserved common wombat (Vombatus ursinus) ovarian tissue xenografted
into nude mice. Reproduction, Fertility and Development 16 699-707.
Cox SL, Shaw J, Jenkin G 1996 Transplantation of cryopreserved fetal ovarian tissue to adult
recipients in mice. Journal of Reproduction and Fertility 107 315-322.
Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squiffet J, Martinez-Madrid B, Van
Langendonckt A 2004 Livebirth after orthotopic transplantation of cryo-preserved ovarian
tissue. The Lancet 364 1405-1410.
Eppig JJ, Downs SM 1987 The effect of hypoxanthine on mouse oocyte growth and
development in vitro: maintenance of meiotic arrest and gonadotropin-induced oocyte
maturation. Developmental Biology 119 313-321.
Eppig JJ, Schroeder AC 1989 Capacity of mouse oocytes from preantral follicles to undergo
embryogenesis and development to live young after growth, maturation, and fertilization in
vitro. Biology of Reproduction 41 268-276.
Eppig JJ, O’Brien MJ 1996 Development in vitro of mouse oocytes from primordial follicles.
Biology of Reproduction 54 197-207.
Erickson BH 1966 Development and senescence of the postnatal bovine ovary. Journal of
Animal Science 25 800-805.
Faddy MJ, Gosden RG 1996 A model conforming the decline in follicle numbers to the age of
menopause in women. Human Reproduction 11 1484-1486.
Gook DA, McCully BA, Edgar DH, McBain JC 2001 Development of antral follicles in human
cryopreserved ovarian tissue following xenografting. Human Reproduction 16 417-422.
Gook DA, Edgar DH, Borg J, Archer J, Lutjen PJ, McBain JC 2003 Oocyte maturation, follicle
rupture and luteinization in human cryopreserved ovarian tissue following xenografting.
Human Reproduction 18 1772-1781.
14
Culture and preservation of ovarian follicles
23. Gook DA, Edgar DH, Borg J, Archer J, McBain JC 2005 Diagnostic assessment of the
developmental potential of human cryopreserved ovarian tissue from multiple patients using
xenografting. Human Reproduction 20 72-78.
24. Gosden RG, Baird DT, Wade JC, Webb R 1994 Restoration of fertility to oophorectomized
sheep by ovarian autografts stored at -196ºC. Human Reproduction 9 597-603.
25. Gutierrez CG, Ralph JH, Telfer EE, Wilmut I, Webb R 2000 Growth and antrum formation
of bovine preantral follicles in long-term culture in vitro. Biology of Reproduction 62 13221328.
26. Harada M, Miyano T, Matsumura K, Osaki S, Miyake M, Kato S 1997 Bovine oocytes from
early antral follicles grow to meiotic competence in vitro: Effect of FSH and hypoxanthine.
Theriogenology 48 743-755.
27. Hirao Y, Itoh T, Shimizu M, Iga K, Aoyagi K, Kobayashi M, Kacchi M, Hoshi H, Takenouchi
N 2004 In vitro growth and development of bovine oocyte-granulosa cell complexes on the flat
substratum: effects of high polyvinylpyrrolidione concentration in culture medium. Biology of
Reproduction 70 83-91.
28. Itoh T, Kacchi M, Abe H, Sendai Y, Hoshi H 2002 Growth, antrum formation, and estradiol
production of bovine preantral follicles cultured in a serum-free medium. Biology of
Reproduction 67 1099-1105.
29. Kaneko H, Kikuchi K, Noguchi J, Hosoe M, Akita T 2003 Maturation and fertilization of
porcine oocytes from primordial follicles by a combination of xenografting and in vitro
culture. Biology of Reproduction 69 1488-1493.
30. Kątska L, Ryńska B 1998 The isolation and in vitro culture of bovine preantral and early antral
follicles of different size classes. Theriogenology 50 213-222.
31. Kątska-Książkiewicz L, Alm H 2004 Determination of long term in vitro culture conditions
of bovine oocytes from early antral ovarian follicles. In Reproductive Biology and Human
Reproductive Health, pp 160-161. Ed Kuczyński W. Białystok, Poland.
32. Kątska-Książkiewicz L, Alm H 2005 Effect of culture methods on cumulus and oocyte
morphology and meiotic competence of bovine oocytes from early antral follicles. Archiv fűr
Tierzucht Dummerstorf 48 562-571.
33. Kątska L, Alm H, Ryńska B 2000 Nuclear configuration of bovine oocytes derived from fresh
and in vitro cultured preantral and early antral ovarian follicles. Theriogenology 54 247-260.
34. Kim SS 2003 Ovarian tissue banking for cancer patients: to do or not to do? Human
Reproduction 18 1759-1761.
35. Kim SS, Soules MR, Battaglia DE 2002 Follicular development, ovulation and corpus luteum
formation in cryopreserved human ovarian tissue after xenotransplantation. Fertility and
Sterility 78 77-82.
36. Lee DM, Yeoman RR, Battaglia DE, Stouffer RL, Zelinski-Wooten MB, Fanton JW, Wolf DP
2004 Live birth after ovarian tissue transplant. Nature 428 137-138.
37. Liu J, Van der Elst J, Van den Broecke R, Dhont M 2001 Live offspring by in vitro fertilization of
oocytes from cryopreserved primordial mouse follicles after sequential in vivo transplantation
an in vitro maturation. Biology of Reproduction 64 171-178.
38. Liu J, Van der Elst J, Van den Broecke R, Dhont M 2002 Early massive follicle loss and apoptosis
in heterotopically grafted newborn mouse ovaries. Human Reproduction 17 605-611.
39. Luisier JP, Matton P, Dufour JJ 1987 Growth rates of follicles in the ovary of the cow. Journal
of Reproduction and Fertility 81 301-307.
40. Mattiske D, Shaw G, Shaw JM 2002 Influence of donor age on development of gonadal tissue
from pouch young of the tammar wallaby, Macropus eugenii, after cryopreservation and
xenografting into mice. Reproduction 123 143-153.
Kątska-Książkiewicz
15
41. Matos MHT, Andrade ER, Lucci CM, Báo SN, Silva JRV, Santos RR, Ferreira MAL, Costa
SHF, Celestino JJH, Figueiredo JR 2004 Morphological and ultrastructural analysis of sheep
primordial follicles preserved in 0.9% saline solution and TCM 199. Theriogenology 62 65-80.
42. Metcalfe SS, Shaw JM, Gunn IM 2001 Xenografting of canine ovarian tissue to ovariectomized
severe combined immunodeficient (SCID) mice. Journal of Reproduction and Fertility (Suppl)
57 323-329.
43. Miyano T 2003 Bringing up small oocytes to eggs in pigs and cows. Theriogenology 59 61-72.
44. Muruvi W, Picton HM, Rodway RG, Joyce IM 2005 In vitro growth of oocytes from primordial
follicles isolated from frozen-thawed lamb ovaries. Theriogenology 64 1357-1370.
45. Newton H, Aubard Y, Rutherford A, Sharma V, Gosden RG 1996 Low temperature storage and
grafting of human ovarian tissue. Human Reproduction 11 1487-1491.
46. Newton H, Picton H, Gosden RG 1999 In vitro growth of oocytes-granulosa cell complexes
isolated from cryopreserved ovine tissue. Journal of Reproduction and Fertility 115 141-150.
47. O’Brien MJ, Pentola JK, Eppig JJ 2003 A revised protocol for on vitro development of mouse
oocytes from primordial follicles dramatically improves their developmental competence.
Biology of Reproduction 68 1682-1686.
48. Oktay K, Newton H, Aubard Y, Salha O, Gosden RG 1998 Cryopreservation of immature
human oocytes and ovarian tissue: an emerging technology? Fertility and Sterility 69 1-7.
49. Oktay K, Karlikaya G 2000 Ovarian function after transplantation of frozen, banked autologous
ovarian tissue. The New England Journal of Medicine 342 1919.
50. Oktay K, Economos K, Kan M, Rucinski J, Veeck L, Rosenwaks Z 2001 Endocrine function
and oocyte retrieval after autologous transplantation of ovarian cortical strips to the forearm.
The Journal of the American Medical Association 286 1490-1493.
51. Parrott DMV 1959 Orthotopic ovarian grafts in the golden hamster. Journal of Endocrinology
19 126-138.
52. Parrott DMV 1960 The fertility of mice with orthotopic ovarian grafts derived from frozen
tissue. Journal of Reproduction and Fertility 1 230-241.
53. Petroianu A, de Souza Vasconcellos L, Alberti LR, Fonseca de Castro LP, Barbosa Leite JM
2002 Natural pregnancy in rabbits that underwent oophorectomy and orthotopic allogeneic or
autologous ovarian transplantation. Fertility and Sterility 77 1298-1299.
54. Poirot C, Vacher-Lavenu MC, Helardot P Guibert J, Brugières L, Jouannet P 2002 Human
ovarian tissue cryopreservation: indications and feasibility. Human Reproduction 17 14471452.
55. Saha S, Shimizu M, Geshi M, Izaike Y 2000 In vitro culture of bovine preantral follicles.
Animal Reproduction Science 63 27-39.
56. Salle B, Demirci B, Franck M, Rudigoz RC, Guerin JF, Lornage J 2002 Normal pregnancies
and live births after autograft of frozen-thawed hemiovaries into ewes. Fertility and Sterility
77 403-408.
57. Saumande J 1991 The folliculogenesis in ruminants. (in French) Recueil de Medecine
Veterinaire 167 205-218.
58. Senbon S, Ota A, Tachibana M, Miyano T 2003 Bovine oocytes in secondary follicles grow and
acquire meiotic competence in severe combined immunodeficient mice. Zygote 11 139-149.
59. Senbon S, Fukumi Y, Hamawaki A, Yoshikawa M, Miyano T 2004 Bovine oocytes grown
in serum-free medium acquire fertilization competence. Journal of Reproduction and
Development 50 541-547.
60. Senbon S, Ota A, Tachibana M, Miyano T 2004 Xenografting of bovine secondary follicles
into ovariectomized female severe combined immunodeficient mice. Journal of Reproduction
and Development 50 439-444.
16
Culture and preservation of ovarian follicles
61. Shaw JM, Cox SL, Trounson AO, Jenkin G 2000 Evaluation of the long term function of
cryopreserved ovarian grafts in the mouse, implications for human applications. Molecular
and Cellular Endocrinology 161 103-110.
62. Snow M, Cox SL, Jenkin G, Trounson A, Shaw J 2002 Generation of live young from
xenografted mouse ovaries. Science 297 2227.
63. Spears N, Boland NI, Murray AA, Gosden RG 1994 Mouse oocytes derived from in vitro
grown primary ovarian follicles are fertile. Human Reproduction 9 527-532.
64. Sun F, Betzendahl I, Shen Y, Cortvrindt R, Smitz J, Eichenlaub-Ritter U 2004 Preantral follicle
culture as a novel in vitro assay in reproductive toxicology testing in mammalian oocytes.
Mutagenesis 19 13-25.
65. Van den Broecke R, Liu J, Handyside A, Van der Elst JC, Krausz T, Dhont M, Winston RM,
Hovatta O 2001 Follicular growth in fresh and cryopreserved human ovarian cortical grafts
transplanted to immunodeficient mice. European Journal of Obstetrics, Gynecology, and
Reproductive Biology 97 193-201.
66. Van den Broecke R, Liu J, Van der Elst JC, Dhont M 2001 Timing of FSH-stimulation and
follicular development in cryopreserved human ovarian grafts. Reproductive Biomedicine
Online 4 21-26.
67. Van den Hurk R, Spek ER, Hage WJ, Fair T, Ralph JH, Schotanus K 1998 Ultrastructure and
viability of isolated bovine preantral follicles. Human Reproduction Update 4 833-841.
68. Wandji SA, Eppig JJ, Fortune JE 1996 FSH and growth factors affect the growth and endocrine
functions in vitro of granulosa cells of bovine preantral follicles. Theriogenology 45 817832.
69. Waterhouse T, Cox SL, Snow M, Jenkin G, Shaw J 2004 Offspring produced from heterotopic
ovarian allografts in male and female recipient mice. Reproduction 127 689-694.
70. Weissman A, Gotlieb L, Colgan T, Jurisicova A, Greenblatt EM, Casper RF 1999 Preliminary
experience with subcutaneous human ovarian cortex transplantation in the NOD-SCID mouse.
Biology of Reproduction 60 1462-1467.
71. Wu J, Carrell DT, Wilcox AL 2001 Development of in-vitro matured oocytes from porcine
preantral follicles following intracytoplasmic sperm injection. Biology of Reproduction 65
1579-1585.
72. Wycherley G, Downey D, Kane MT, Hynes AC 2004 A novel follicle culture system markedly
increases follicle volume, cell number and oestradiol secretion. Reproduction 127 669-677.
73. Yamamoto K, Otoi T, Koyama N, Horikita N, Tachikawa S, Miyano T 1999 Development
to live young bovine small oocytes after growing, maturation and fertilization in vitro.
Theriogenology 52 81-89.