Abstract
Follicle culture in vitro provides a method for investigating stages of folliculogenesis that can lead to preserving fertility through cryopreservation techniques. This study aims to assess the effects of various concentrations of human follicular fluid (hFF) on growth, development, and expression of the proliferating cell nuclear antigen (PCNA) gene in mouse ovarian follicles in vitro. Preantral follicles were isolated from 14-day NMRI mouse ovaries. The follicles were cultured in basic media enriched with FBS, FSH, and insulin-transferrin-selenium, and supplemented with different concentrations of hFF (10, 20, and 30%) for 12 days. During the culture period, survival rate and follicular maturation, follicular diameter, levels of estrogen and progesterone secretion, and PCNA gene expression rate were evaluated. Survival rate, maturation, and antrum formation were significantly higher in the 10% hFF group than in the 20 and 30% hFF groups. On day 4, follicle diameter in the 10% hFF group was also higher than in the 20 and the 30% hFF group. In comparison with other groups, significantly higher estrogen and progesterone production levels were measured in the 10% hFF group. PCNA gene expression was also higher with 10 than 20 and 30% hFF concentrations. The present study suggests that addition of 10% hFF to mice ovarian preantral follicle culture media enhances follicle growth and oocyte maturation.
References
1.
Aguilar
JJ
, Woods
GL
, Miragaya
MH
, Olsen
LM
, Vanderwall
DK
. Effect of homologous preovulatory follicular fluid on in vitro maturation of equine cumulus-oocyte complexes
. Theriogenology
. 2001
Sep
;56
(5
):745
–58
.
[PubMed]
0093-691X2.
Algriany
O
, Bevers
M
, Schoevers
E
, Colenbrander
B
, Dieleman
S
. Follicle size-dependent effects of sow follicular fluid on in vitro cumulus expansion, nuclear maturation and blastocyst formation of sow cumulus oocytes complexes
. Theriogenology
. 2004
Nov
;62
(8
):1483
–97
.
[PubMed]
0093-691X3.
Andrade
P
, Chaves
R
, Alves
A
, Rocha
R
, Lima
L
, Carvalho
A
, et al Effects of α-MEM and TCM-199 culture media and epidermal growth factor on survival and growth of goat and sheep preantral follicles cultured in vitro
. Animal Reproduction (AR)
. 2018
;11
:567
–72
.4.
Araújo
VR
, Gastal
MO
, Figueiredo
JR
, Gastal
EL
. In vitro culture of bovine preantral follicles: a review
. Reprod Biol Endocrinol
. 2014
Aug
;12
(1
):78
.
[PubMed]
1477-78275.
Barboni
B
, Russo
V
, Cecconi
S
, Curini
V
, Colosimo
A
, Garofalo
ML
, et al In vitro grown sheep preantral follicles yield oocytes with normal nuclear-epigenetic maturation
. PLoS One
. 2011
;6
(11
):e27550
.
[PubMed]
1932-62036.
Basuino
L
, Silveira
CF
Jr. Human follicular fluid and effects on reproduction
. JBRA Assist Reprod
. 2016
Mar
;20
(1
):38
–40
.
[PubMed]
1517-56937.
Bezerra
MÉ
, Barberino
RS
, Menezes
VG
, Gouveia
BB
, Macedo
TJ
, Santos
JM
, et al Insulin-like growth factor-1 (IGF-1) promotes primordial follicle growth and reduces DNA fragmentation through the phosphatidylinositol 3-kinase/protein kinase B (PI3K/AKT) signalling pathway
. Reprod Fertil Dev
. 2018
Oct
;30
(11
):1503
–13
.
[PubMed]
1031-36138.
Buratini
J
, Price
CA
. Follicular somatic cell factors and follicle development
. Reprod Fertil Dev
. 2011
;23
(1
):32
–9
.
[PubMed]
1031-36139.
Coleman
NV
, Shagiakhmetova
GA
, Lebedeva
IY
, Kuzmina
TI
, Golubev
AK
. In vitro maturation and early developmental capacity of bovine oocytes cultured in pure follicular fluid and supplementation with follicular wall
. Theriogenology
. 2007
Mar
;67
(5
):1053
–9
.
[PubMed]
0093-691X10.
Comizzoli
P
. Biobanking and fertility preservation for rare and endangered species
. Animal Reproduction (AR)
. 2018
;14
(1
):30
–3
. 11.
Comizzoli
P
, Wildt
DE
. Cryobanking biomaterials from wild animal species to conserve genes and biodiversity: relevance to human biobanking and biomedical research, Biobanking of Human Biospecimens
. Springer
; 2017
. pp. 217
–35
.12.
Cook-Andersen
H
, Curnow
KJ
, Su
HI
, Chang
RJ
, Shimasaki
S
. Growth and differentiation factor 9 promotes oocyte growth at the primary but not the early secondary stage in three-dimensional follicle culture
. J Assist Reprod Genet
. 2016
Aug
;33
(8
):1067
–77
.
[PubMed]
1058-046813.
Cruz
MH
, Saraiva
NZ
, Cruz
JF
, Oliveira
CS
, Del Collado
M
, Fernandes
H
, et al Effect of follicular fluid supplementation during in vitro maturation on total cell number in bovine blastocysts produced in vitro
. Rev Bras Zootec
. 2014
;43
(3
):120
–6
. 1516-359814.
Devesa
J
, Caicedo
D
. The role of growth hormone on ovarian functioning and ovarian angiogenesis
. Front Endocrinol (Lausanne)
. 2019
Jul
;10
:450
.
[PubMed]
1664-239215.
Ducolomb
Y
, González-Márquez
H
, Fierro
R
, Jiménez
I
, Casas
E
, Flores
D
, et al Effect of porcine follicular fluid proteins and peptides on oocyte maturation and their subsequent effect on in vitro fertilization
. Theriogenology
. 2013
Apr
;79
(6
):896
–904
.
[PubMed]
0093-691X16.
Herta
AC
, Lolicato
F
, Smitz
JE
. In vitro follicle culture in the context of IVF
. Reproduction
. 2018
Jul
;156
(1
):F59
–73
.
[PubMed]
1470-162617.
Higuchi
CM
, Maeda
Y
, Horiuchi
T
, Yamazaki
Y
. A simplified method for three-dimensional (3-D) ovarian tissue culture yielding oocytes competent to produce full-term offspring in mice
. PLoS One
. 2015
Nov
;10
(11
):e0143114
.
[PubMed]
1932-620318.
Hsueh
AJ
, Kawamura
K
, Cheng
Y
, Fauser
BC
. Intraovarian control of early folliculogenesis
. Endocr Rev
. 2015
Feb
;36
(1
):1
–24
.
[PubMed]
0163-769X19.
Hung
WT
, Hong
X
, Christenson
LK
, McGinnis
LK
. Extracellular vesicles from bovine follicular fluid support cumulus expansion
. Biol Reprod
. 2015
Nov
;93
(5
):117
.
[PubMed]
0006-336320.
Hung
WT
, Navakanitworakul
R
, Khan
T
, Zhang
P
, Davis
JS
, McGinnis
LK
, et al Stage-specific follicular extracellular vesicle uptake and regulation of bovine granulosa cell proliferation
. Biol Reprod
. 2017
Oct
;97
(4
):644
–55
.
[PubMed]
0006-336321.
Ito
M
, Iwata
H
, Kitagawa
M
, Kon
Y
, Kuwayama
T
, Monji
Y
. Effect of follicular fluid collected from various diameter follicles on the progression of nuclear maturation and developmental competence of pig oocytes
. Anim Reprod Sci
. 2008
Jul
;106
(3-4
):421
–30
.
[PubMed]
0378-432022.
Kim
K
, Mitsumizo
N
, Fujita
K
, Utsumi
K
. The effects of follicular fluid on in vitro maturation, oocyte fertilization and the development of bovine embryos
. Theriogenology
. 1996
Mar
;45
(4
):787
–99
.
[PubMed]
0093-691X23.
Ksiazkiewicz
LK
. Recent achievements in in vitro culture and preservation of ovarian follicles in mammals
. Reprod Biol
. 2006
Mar
;6
(1
):3
–16
.
[PubMed]
1642-431X24.
Larocca C, Kmaid S, Calvo J, Viqueira M. Effect of follicular fluid and estrus cow serum on in vitro production of bovine embryos. Agro-Ciencia (Chile). 1995.
25.
Lin
JX
, Jia
YD
, Zhang
CQ
. Effect of epidermal growth factor on follicle-stimulating hormone-induced proliferation of granulosa cells from chicken prehierarchical follicles
. J Zhejiang Univ Sci B
. 2011
Nov
;12
(11
):875
–83
.
[PubMed]
1673-158126.
Malekshah
AK
, Moghaddam
AE
. Follicular fluid and cumulus cells synergistically improve mouse early embryo development in vitro
. J Reprod Dev
. 2005
Apr
;51
(2
):195
–9
.
[PubMed]
0916-881827.
Mendoza
C
, Ruiz-Requena
E
, Ortega
E
, Cremades
N
, Martinez
F
, Bernabeu
R
, et al Follicular fluid markers of oocyte developmental potential
. Hum Reprod
. 2002
Apr
;17
(4
):1017
–22
.
[PubMed]
0268-116128.
Metoki T, Iwata H, Itoh M, Kasai M, Takajyo A, Suzuki A, Kuwayama T, Monji Y. Effects of follicular fluids on the growth of porcine preantral follicle and oocyte. Zygote. 2008 Aug;16(3):239.
29.
Morohaku
K
, Hirao
Y
, Obata
Y
. Developmental competence of oocytes grown in vitro: has it peaked already?
J Reprod Dev
. 2015
.
[PubMed]
0916-881830.
Naito K, Fukuda Y, Ishibashi I. Developmental ability of porcine ova matured in porcine follicular fluid in vitro and fertilized in vitro. Theriogenology. 1989 May;31(5):1049–57.
31.
Nandi
S
, Girish Kumar
V
. Effect of a partially purified 30.1 kDa ovine follicular fluid protein on ovine follicle and ovarian somatic cell growth, and oocyte maturation in vitro
. Acta Physiol (Oxf)
. 2008
Aug
;193
(4
):341
–55
.
[PubMed]
1748-170832.
Oktay
K
, Schenken
RS
, Nelson
JF
. Proliferating cell nuclear antigen marks the initiation of follicular growth in the rat
. Biol Reprod
. 1995
Aug
;53
(2
):295
–301
.
[PubMed]
0006-336333.
Revelli
A
, Delle Piane
L
, Casano
S
, Molinari
E
, Massobrio
M
, Rinaudo
P
. Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics
. Reprod Biol Endocrinol
. 2009
May
;7
(1
):40
.
[PubMed]
1477-782734.
Shoorei
H
, Salehnia
M
, Abdi
S
. The Effects of Different Concentrations of Ovarian Tissue Extract on Preantral Mouse Follicle Development after Three-dimensional Culture
. Pathobiology Research
. 2017
;19
:41
–53
.35.
Skory
RM
, Xu
Y
, Shea
LD
, Woodruff
TK
. Engineering the ovarian cycle using in vitro follicle culture
. Hum Reprod
. 2015
Jun
;30
(6
):1386
–95
.
[PubMed]
0268-116136.
Sluss PM, Schneyer AL, Franke MA, Reichert Jr LE. Porcine follicular fluid contains both follicle-stimulating hormone agonist and antagonist activities. Endocrinology. 1987 Apr;120(4):1477–81.
37.
Smitz
JE
, Cortvrindt
RG
. The earliest stages of folliculogenesis in vitro
. Reproduction
. 2002
Feb
;123
(2
):185
–202
.
[PubMed]
1470-162638.
Telfer
EE
, McLaughlin
M
, Ding
C
, Thong
KJ
. A two-step serum-free culture system supports development of human oocytes from primordial follicles in the presence of activin
. Hum Reprod
. 2008
May
;23
(5
):1151
–8
.
[PubMed]
0268-116139.
Telfer
EE
, Zelinski
MB
. Ovarian follicle culture: advances and challenges for human and nonhuman primates
. Fertil Steril
. 2013
May
;99
(6
):1523
–33
.
[PubMed]
0015-028240.
Xiao
S
, Zhang
J
, Romero
MM
, Smith
KN
, Shea
LD
, Woodruff
TK
. In vitro follicle growth supports human oocyte meiotic maturation
. Sci Rep
. 2015
Nov
;5
(1
):17323
.
[PubMed]
2045-2322© 2020 S. Karger AG, Basel
2020
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.
