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Citations to this article

The ovary: basic biology and clinical implications
JoAnne S. Richards, Stephanie A. Pangas
JoAnne S. Richards, Stephanie A. Pangas
Published April 1, 2010
Citation Information: J Clin Invest. 2010;120(4):963-972. https://doi.org/10.1172/JCI41350.
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The ovary: basic biology and clinical implications

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Abstract

The classical view of ovarian follicle development is that it is regulated by the hypothalamic-pituitary-ovarian axis, in which gonadotropin-releasing hormone (GnRH) controls the release of the gonadotropic hormones follicle-stimulating hormone (FSH) and luteinizing hormone (LH), and that ovarian steroids exert both negative and positive regulatory effects on GnRH secretion. More recent studies in mice and humans indicate that many other intra-ovarian signaling cascades affect follicular development and gonadotropin action in a stage- and context-specific manner. As we discuss here, mutant mouse models and clinical evidence indicate that some of the most powerful intra-ovarian regulators of follicular development include the TGF-β/SMAD, WNT/FZD/β-catenin, and RAS/ERK1/2 signaling pathways and the FOXO/FOXL2 transcription factors.

Authors

JoAnne S. Richards, Stephanie A. Pangas

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Total citations by year

Year: 2025 2024 2023 2022 2021 2020 2019 2018 2017 2016 2015 2014 2013 2012 2011 2010 2009 Total
Citations: 9 25 22 21 18 9 16 13 11 12 12 8 13 5 9 3 1 207
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H Yan, J Wen, T Zhang, W Zheng, M He, K Huang, Q Guo, Q Chen, Y Yang, G Deng, J Xu, Z Wei, H Zhang, G Xia, C Wang
Cell Death and Disease 2019
HAS2-AS1 is a novel LH/hCG target gene regulating HAS2 expression and enhancing cumulus cells migration
Y Yung, L Ophir, GM Yerushalmi, M Baum, A Hourvitz, E Maman
Journal of Ovarian Research 2019
VCAM1 Is Induced in Ovarian Theca and Stromal Cells in a Mouse Model of Androgen Excess
NR Candelaria, A Padmanabhan, F Stossi, MC Ljungberg, KE Shelly, BK Pew, M Solis, AM Rossano, JM McAllister, S Wu, JA Richards
Endocrinology 2019
Tyrosine nitrations impaired intracellular trafficking of FSHR to the cell surface and FSH-induced Akt-FoxO3a signaling in human granulosa cells
G Zhou, R Hu, G Xia, S Yan, Q Ren, J Zhao, F Wang, C Huang, Q Yao, Y Tan, N Zhao
Aging 2019
SFRP4 Is a Negative Regulator of Ovarian Follicle Development and Female Fertility
G Zamberlam, E Lapointe, A Abedini, C Rico, P Godin, M Paquet, FJ DeMayo, D Boerboom
Endocrinology 2019
Poor second ovarian stimulation in cynomolgus monkeys (Macaca fascicularis) is associated with the production of antibodies against human follicle-stimulating hormone
Y SEITA, C IWATANI, H TSUCHIYA, S NAKAMURA, F KIMURA, T MURAKAMI, M EMA
Journal of Reproduction and Development 2019
Discovering Science and the Ovary: A Career of Joy
JA Richards
Reproduction 2019
The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates
S Matsubara, A Shiraishi, T Osugi, T Kawada, H Satake
eLife 2019
Ad libitum feeding triggers puberty onset associated with increases in arcuate Kiss1 and Pdyn expression in growth-retarded rats
S MAJARUNE, P Nima, A SUGIMOTO, M NAGAE, N INOUE, H TSUKAMURA, Y UENOYAMA
Journal of Reproduction and Development 2019
Activation of Notch Signaling by Oocytes and Jag1 in Mouse Ovarian Granulosa Cells
N Hubbard, RD Prasasya, KE Mayo
Endocrinology 2019
The transcriptional regulator CBX2 and ovarian function: A whole genome and whole transcriptome approach
L Bouazzi, P Sproll, W Eid, A Biason-Lauber
Scientific Reports 2019
Molecular mechanisms of embryonic implantation in mammals: Lessons from the gene manipulation of mice
T Namiki, J Ito, N Kashiwazaki
Reproductive Medicine and Biology 2018
Fshb Knockout Mouse Model, Two Decades Later and Into The Future
TR Kumar
Endocrinology 2018
Chronic restraint stress induces excessive activation of primordial follicles in mice ovaries
M Xu, J Sun, Q Wang, Q Zhang, C Wei, D Lai, M Zhang
PloS one 2018
Metabolic Effects of FecB Gene on Follicular Fluid and Ovarian Vein Serum in Sheep (Ovis aries)
X Guo, X Wang, R Di, Q Liu, W Hu, X He, J Yu, X Zhang, J Zhang, K Broniowska, W Chen, C Wu, M Chu
International journal of molecular sciences 2018
Ovulatory Induction of SCG2 in Human, Nonhuman Primate, and Rodent Granulosa Cells Stimulates Ovarian Angiogenesis
PR Hannon, DM Duffy, KL Rosewell, M Brännström, JW Akin, TE Curry
Endocrinology 2018
Histone demethylase KDM4A and KDM4B expression in granulosa cells from women undergoing in vitro fertilization
AJ Krieg, SR Mullinax, F Grimstad, K Marquis, E Constance, Y Hong, SA Krieg, KF Roby
Journal of Assisted Reproduction and Genetics 2018
Uterine Foxl2 regulates the adherence of the Trophectoderm cells to the endometrial epithelium
M Elbaz, R Hadas, LM Bilezikjian, E Gershon
Reproductive Biology and Endocrinology 2018
Systematic Analysis of Long Non-Coding RNAs and mRNAs in the Ovaries of Duroc Pigs During Different Follicular Stages Using RNA Sequencing
Y Liu, M Li, X Bo, T Li, L Ma, T Zhai, T Huang
International journal of molecular sciences 2018
Sex- and Age-Specific Impact of ERK Loss Within the Pituitary Gonadotrope in Mice
JL Brown, J Xie, MA Brieño-Enriquez, J Sones, CN Angulo, U Boehm, A Miller, C Toufaily, Y Wang, DJ Bernard, MS Roberson
Endocrinology 2018
At the Crossroads of Fate—Somatic Cell Lineage Specification in the Fetal Gonad
E Rotgers, A Jørgensen, HH Yao
Endocrine reviews 2018
Structure-Function Relationships of the Follicle-Stimulating Hormone Receptor
A Ulloa-Aguirre, T Zariñán, E Jardón-Valadez, R Gutiérrez-Sagal, JA Dias
Frontiers in Endocrinology 2018
Cell Origins of High-Grade Serous Ovarian Cancer
J Kim, E Park, O Kim, J Schilder, D Coffey, CH Cho, R Bast
Cancers 2018
Control of growth and development of preantral follicle: insights from in vitro culture
de Figueiredo JR, de Lima LF, Silva JR, Santos RR
2018
Ovarian Follicular Theca Cell Recruitment, Differentiation, and Impact on Fertility: 2017 Update
JA Richards, YA Ren, N Candelaria, JE Adams, A Rajkovic
Endocrine reviews 2017
GGPP-Mediated Protein Geranylgeranylation in Oocyte Is Essential for the Establishment of Oocyte-Granulosa Cell Communication and Primary-Secondary Follicle Transition in Mouse Ovary
C Jiang, F Diao, YJ Sang, N Xu, RL Zhu, XX Wang, Z Chen, WW Tao, B Yao, HX Sun, XX Huang, B Xue, CJ Li, M Pepling
PLoS genetics 2017
Brain-derived neurotrophic factor promotes human granulosa-like tumor cell steroidogenesis and proliferation by activating the FSH receptor-mediated signaling pathway
M Xie, M Li, J Zhou, X Ding, Y Shao, J Jing, Y Liu, B Yao
Scientific Reports 2017
A novel action of follicle-stimulating hormone in the ovary promotes estradiol production without inducing excessive follicular growth before puberty
CM François, F Petit, F Giton, A Gougeon, C Ravel, S Magre, J Cohen-Tannoudji, CJ Guigon
Scientific Reports 2017
Defining the Role of Estrogen Receptor β in the Regulation of Female Fertility
MA Rumi, P Singh, KF Roby, X Zhao, K Iqbal, A Ratri, T Lei, W Cui, S Borosha, P Dhakal, K Kubota, D Chakraborty, JL Vivian, MW Wolfe, MJ Soares
Endocrinology 2017
Female Fertility: It Takes Two to Tango
LX Chen, PT Jimenez
Endocrinology 2017
Gonadal soma controls ovarian follicle proliferation through Gsdf in zebrafish: GSDF Controls Ovary Development in Zebrafish
YL Yan, T Desvignes, R Bremiller, C Wilson, D Dillon, S High, B Draper, CL Buck, J Postlethwait
Developmental Dynamics 2017
Identification and analysis of differentially expressed long non-coding RNAs between multiparous and uniparous goat (Capra hircus) ovaries
Y Ling, L Xu, L Zhu, M Sui, Q Zheng, W Li, Y Liu, F Fang, X Zhang, M Zhang
PloS one 2017
TGFβ superfamily signaling and uterine decidualization
N Ni, Q Li
Reproductive Biology and Endocrinology 2017
Stress and the HPA Axis: Balancing Homeostasis and Fertility
D Joseph, S Whirledge
International journal of molecular sciences 2017
Extragonadal Actions of FSH: A Critical Need for Novel Genetic Models
TR Kumar
Endocrinology 2017
Induction of Tissue Factor Pathway Inhibitor 2 by hCG regulates Periovulatory Gene Expression and Plasmin Activity
M Puttabyatappa, LF Al-Alem, F Zakerkish, KL Rosewell, M Brännström, TE Curry
Endocrinology 2016
Insulin signalling and glucose transport in the ovary and ovarian function during the ovarian cycle
J Dupont, RJ Scaramuzzi
Biochemical Journal 2016
Growth Arrest Specific-1 (GAS1) Is a C/EBP Target Gene That Functions in Ovulation and Corpus Luteum Formation in Mice
YA Ren, Z Liu, LK Mullany, CM Fan, JS Richards
Biology of reproduction 2016
The transcriptional repressor ICER binds to multiple loci throughout the genome
LC Muñiz, CA Molina
Biochemical and Biophysical Research Communications 2016
Role of Cysteine Residues in the Carboxyl-Terminus of the Follicle-Stimulating Hormone Receptor in Intracellular Traffic and Postendocytic Processing
B Melo-Nava, P Casas-González, MA Pérez-Solís, J Castillo-Badillo, JL Maravillas-Montero, E Jardón-Valadez, T Zariñán, A Aguilar-Rojas, N Gallay, E Reiter, A Ulloa-Aguirre
Frontiers in Cell and Developmental Biology 2016
Comparative profiling of differentially expressed microRNAs between the follicular and luteal phases ovaries of goats
L Zhu, T Chen, M Sui, C Han, F Fang, Y Ma, M Chu, X Zhang, C Liu, Y Ling
SpringerPlus 2016
An endometrial gene expression signature accurately predicts recurrent implantation failure after IVF
YE Koot, SR van Hooff, CM Boomsma, D Leenen, MJ Koerkamp, M Goddijn, MJ Eijkemans, BC Fauser, FC Holstege, NS Macklon
Scientific Reports 2016
Expression of Human NSAID Activated Gene 1 in Mice Leads to Altered Mammary Gland Differentiation and Impaired Lactation
AK Binder, JP Kosak, KS Janhardhan, G Moser, TE Eling, KS Korach, J Pawluski
PloS one 2016
FSH Regulates mRNA Translation in Mouse Oocytes and Promotes Developmental Competence
F Franciosi, S Manandhar, M Conti
Endocrinology 2016
The disparate origins of ovarian cancers: pathogenesis and prevention strategies
AN Karnezis, KR Cho, CB Gilks, CL Pearce, DG Huntsman
Nature Reviews Cancer 2016
Leukemia Inhibitory Factor Is Necessary for Ovulation in Female Rhesus Macaques
MJ Murphy, NG Halow, PA Royer, JD Hennebold
Endocrinology 2016
XCI-escaping gene KDM5C contributes to ovarian development via downregulating miR-320a.
Sun YX, Zhang YX, Zhang D, Xu CM, Chen SC, Zhang JY, Ruan YC, Chen F, Zhang RJ, Qian YQ, Liu YF, Jin LY, Yu TT, Xu HY, Luo YQ, Liu XM, Sun F, Sheng JZ, Huang HF
Human Genetics 2016
Gene expression analysis of pig cumulus-oocyte complexes stimulated in vitro with follicle stimulating hormone or epidermal growth factor-like peptides
M Blaha, L Nemcova, KV Kepkova, P Vodicka, R Prochazka
Reproductive Biology and Endocrinology 2015
Regulation of mitogen-activated protein kinase 3/1 activity during meiosis resumption in mammals
R PROCHAZKA, M BLAHA
Journal of Reproduction and Development 2015
Activation of Gq/11 in the Mouse Corpus Luteum Is Required for Parturition
R Mejia, C Waite, M Ascoli
Molecular Endocrinology 2015
Vertebrate Reproduction
S Kornbluth, R Fissore
Cold Spring Harbor perspectives in biology 2015
Rictor/mTORC2 Pathway in Oocytes Regulates Folliculogenesis, and Its Inactivation Causes Premature Ovarian Failure
Z Chen, X Kang, L Wang, H Dong, C Wang, Z Xiong, W Zhao, C Jia, J Lin, W Zhang, W Yuan, M Zhong, H Du, X Bai
The Journal of biological chemistry 2015
Gonadotropin and kisspeptin gene expression, but not GnRH, are impaired in cFOS deficient mice
C Xie, CR Jonak, AS Kauffman, D Coss
Molecular and Cellular Endocrinology 2015
FOXO1/3 and PTEN Depletion in Granulosa Cells Promotes Ovarian Granulosa Cell Tumor Development
Z Liu, YA Ren, SA Pangas, J Adams, W Zhou, DH Castrillon, D Wilhelm, JA Richards
Molecular Endocrinology 2015
Hypoglycosylated hFSH Has Greater Bioactivity Than Fully Glycosylated Recombinant hFSH in Human Granulosa Cells
C Jiang, X Hou, C Wang, JV May, VY Butnev, GR Bousfield, JS Davis
The Journal of clinical endocrinology and metabolism 2015
Genetic Models for the Study of Luteinizing Hormone Receptor Function
P Narayan
Frontiers in Endocrinology 2015
WNT5a is required for normal ovarian follicle development and antagonizes gonadotropin responsiveness in granulosa cells by suppressing canonical WNT signaling
A Abedini, G Zamberlam, E Lapointe, C Tourigny, A Boyer, M Paquet, K Hayashi, H Honda, A Kikuchi, C Price, D Boerboom
The FASEB Journal 2015
Infertility in Female Mice with a Gain-of-Function Mutation in the Luteinizing Hormone Receptor Is Due to Irregular Estrous Cyclicity, Anovulation, Hormonal Alterations, and Polycystic Ovaries
L Hai, SR McGee, AC Rabideau, M Paquet, P Narayan
Biology of reproduction 2015
Recent advancements in the hormonal stimulation of ovulation in swine
R Knox
2015
Constitutively Active FOXO1 Diminishes Activin Induction of Fshb Transcription in Immortalized Gonadotropes
CH Park, DV Skarra, AJ Rivera, DJ Arriola, VG Thackray, A Wolfe
PloS one 2014
Multiple Pathways Mediate Luteinizing Hormone Regulation of cGMP Signaling in the Mouse Ovarian Follicle
X Liu, F Xie, AM Zamah, B Cao, M Conti
Biology of reproduction 2014
“Been hit twice”: a novel bi-allelic heterozygous mutation in LHCGR
TR Kumar
Journal of Assisted Reproduction and Genetics 2014
Intrauterine factors and risk of nonepithelial ovarian cancers
W Sieh, K Sundquist, J Sundquist, MA Winkleby, C Crump
Gynecologic Oncology 2014
Cytokine (IL16) and tyrphostin actions on ovarian primordial follicle development
A Feeney, E Nilsson, MK Skinner
Reproduction 2014
Identification of sites of STAT3 action in the female reproductive tract through conditional gene deletion
RL Robker, LN Watson, SA Robertson, KR Dunning, EA McLaughlin, DL Russell
PloS one 2014
Extragonadal FSH Receptor: Is It Real?
TR Kumar
Biology of reproduction 2014
Evidence Supporting a Functional Requirement of SMAD4 for Bovine Preimplantation Embryonic Development: A Potential Link to Embryotrophic Actions of Follistatin
KB Lee, K Zhang, JK Folger, JG Knott, GW Smith
Biology of reproduction 2014
Pituitary gland development and disease: from stem cell to hormone production
SW Davis, BS Ellsworth, MI Millan, P Gergics, V Schade, N Foyouzi, ML Brinkmeier, AH Mortensen, SA Camper
Current topics in developmental biology 2013
Ovulation involves the luteinizing hormone-dependent activation of G(q/11) in granulosa cells
SM Breen, N Andric, T Ping, F Xie, S Offermans, JA Gossen, M Ascoli
Molecular Endocrinology 2013
Ontogeny of the ovary in polycystic ovary syndrome
DA Dumesic, JA Richards
Fertility and Sterility 2013
Role of follicle-stimulating hormone on biliary cyst growth in autosomal dominant polycystic kidney disease
P Onori, R Mancinelli, A Franchitto, G Carpino, A Renzi, S Brozzetti, J Venter, H Francis, S Glaser, DM Jefferson, G Alpini, E Gaudio
Liver International 2013
Computational modelling of bovine ovarian follicle development
D Iber, CD Geyter
BMC Systems Biology 2013
Luteinizing hormone and follicle stimulating hormone synergy: A review of role in controlled ovarian hyper-stimulation
GA Raju, R Chavan, M Deenadayal, D Gunasheela, R Gutgutia, G Haripriya, M Govindarajan, NH Patel, AS Patki
Journal of human reproductive sciences 2013
FSH in vitro versus LH in vivo: similar genomic effects on the cumulus
M Assidi, FJ Richard, MA Sirard
Journal of Ovarian Research 2013
Gene bionetworks that regulate ovarian primordial follicle assembly
E Nilsson, B Zhang, MK Skinner
BMC Genomics 2013
The absence of ER-β results in altered gene expression in ovarian granulosa cells isolated from in vivo preovulatory follicles
AK Binder, KF Rodriguez, KJ Hamilton, PS Stockton, CE Reed, KS Korach
Endocrinology 2013
Nano-encapsulation of arsenic trioxide enhances efficacy against murine lymphoma model while minimizing its impact on ovarian reserve in vitro and in vivo
RW Ahn, SL Barrett, MR Raja, JK Jozefik, L Spaho, H Chen, MB Bally, AP Mazar, MJ Avram, JN Winter, LI Gordon, LD Shea, TV O'Halloran, TK Woodruff
PloS one 2013
Gonadal expression of Foxo1, but not Foxo3, is conserved in diverse Mammalian species
ED Tarnawa, MD Baker, GM Aloisio, BR Carr, DH Castrillon
Biology of reproduction 2013
Integrating microRNAs into the complexity of gonadotropin signaling networks
K León, N Gallay, A Poupon, E Reiter, R Dalbies-Tran, P Crepieux
Frontiers in Cell and Developmental Biology 2013
Forkhead Box O1 Is a Repressor of Basal and GnRH-Induced Fshb Transcription in Gonadotropes
DV Skarra, DJ Arriola, CA Benson, VG Thackray
Molecular Endocrinology 2013
Epigenetic Mechanisms in the Actions of Endocrine-disrupting Chemicals: Gonadal Effects and Role in Female Reproduction: Endocrine Disruptors, the Ovary and Female Fertility
M Uzumcu, AM Zama, E Oruc
Reproduction in Domestic Animals 2012
Regulation of the ovarian reserve by members of the transforming growth factor beta family
SA Pangas
Molecular Reproduction and Development 2012
The molecular basis of impaired follicle-stimulating hormone action: evidence from human mutations and mouse models
ET Siegel, HG Kim, HK Nishimoto, LC Layman
Reproductive sciences (Thousand Oaks, Calif.) 2012
FOXL2 is involved in the synergy between activin and progestins on the follicle-stimulating hormone β-subunit promoter
Y Ghochani, JK Saini, PL Mellon, VG Thackray
Endocrinology 2012
Deletion of Tuberous Sclerosis 1 in Somatic Cells of the Murine Reproductive Tract Causes Female Infertility
Y Tanaka, JH Park, PS Tanwar, T Kaneko-Tarui, S Mittal, HJ Lee, JM Teixeira
Endocrinology 2012
Transforming Growth Factor β Receptor Type 1 Is Essential for Female Reproductive Tract Integrity and Function
Q Li, JE Agno, MA Edson, AK Nagaraja, T Nagashima, MM Matzuk
PLoS genetics 2011
Molecular characterization of the human ovulatory cascade—Lesson from the IVF/IVM model
GM Yerushalmi, E Maman, Y Yung, A Kedem, A Hourvitz
Journal of Assisted Reproduction and Genetics 2011
Bone morphogenetic protein signaling transcription factor (SMAD) function in granulosa cells
SA Pangas
Molecular and Cellular Endocrinology 2011
Hematopoietic-Prostaglandin D2 synthase through PGD2 production is involved in the adult ovarian physiology
A Farhat, P Philibert, C Sultan, F Poulat, B Boizet-Bonhoure
Journal of Ovarian Research 2011
Regulation of gene expression in ovarian cancer cells by luteinizing hormone receptor expression and activation
J Cui, BM Miner, JB Eldredge, SW Warrenfeltz, P Dam, Y Xu, D Puett
BMC Cancer 2011
Consequences of RAS and MAPK activation in the ovary: the good, the bad and the ugly
HY Fan, Z Liu, LK Mullany, JA Richards
Molecular and Cellular Endocrinology 2011
Sex differences in kappa opioid pharmacology
K Rasakham, LY Liu-Chen
Life Sciences 2011
The Epigenetics of Normal Pregnancy
JD Best, N Carey
Obstetric Medicine: The Medicine of Pregnancy 2011
Gene Expression Profiling Reveals Cyp26b1 to Be an Activin Regulated Gene Involved in Ovarian Granulosa Cell Proliferation
JL Kipp, A Golebiowski, G Rodriguez, M Demczuk, SM Kilen, KE Mayo
Endocrinology 2011
How we are born?
Sudhansu Dey
Journal of Clinical Investigation 2010
Aromatase is a direct target of FOXL2: C134W in granulosa cell tumors via a single highly conserved binding site in the ovarian specific promoter
NI Fleming, KC Knower, KA Lazarus, PJ Fuller, ER Simpson, CD Clyne
PloS one 2010
CCAAT/Enhancer-Binding Proteins (C/EBP)-α and -β Are Essential for Ovulation, Luteinization, and the Expression of Key Target Genes
HY Fan, Z Liu, PF Johnson, JA Richards
Molecular Endocrinology 2010
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology 2009

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