Multi-scale modelling of ovarian follicular development: from follicular morphogenesis to selection for ovulation
Open accessAbstract
In this review, we present multi-scale mathematical models of ovarian follicular development that are based on the embedding of physiological mechanisms into the cell scale. During basal follicular development, follicular growth operates through an increase in the oocyte size concomitant with the proliferation of its surrounding granulosa cells. We have developed a spatio-temporal model of follicular morphogenesis explaining how the interactions between the oocyte and granulosa cells need to be properly balanced to shape the follicle. During terminal follicular development, the ovulatory follicle is selected amongst a cohort of simultaneously growing follicles. To address this process of follicle selection, we have developed a model giving a continuous and deterministic description of follicle development, adapted to high numbers of cells and based on the dynamical and hormonally regulated repartition of granulosa cells into different cell states, namely proliferation, differentiation and apoptosis. This model takes into account the hormonal feedback loop involving the growing ovarian follicles and the pituitary gland, and enables the exploration of mechanisms regulating the number of ovulations at each ovarian cycle. Both models are useful for addressing ovarian physio-pathological situations. Moreover, they can be proposed as generic modelling environments to study various developmental processes and cell interaction mechanisms.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Mathematical modelling has been employed to understand the macroscopic processes involved in follicular development.
“Mathematical modelling has also been employed to understand the macroscopic processes involved in follicular development [67].”
From Mathematical Modelling of Endocrine Systems (2019) · cites this paper as [67]
Cites
Visualizing Spatiotemporal Dynamics of Multicellular Cell-Cycle Progression
Sakaue-Sawano, A., Kurokawa, H., Morimura, T., Hanyu, A., Hama, H., Osawa, H., Kashiwagi, S., Fukami, K., Miyata, T., Miyoshi, H., et al. (2008) · Cell · doi:10.1016/j.cell.2007.12.033 · Cited by 2,123 · see citing works
Initial and cyclic recruitment of ovarian follicles
McGee, E. A., & Hsueh, A. J. W. (2000) · Endocrine Reviews · doi:10.1210/edrv.21.2.0394 · Cited by 1,771 · see citing works
Growth differentiation factor-9 is required during early ovarian folliculogenesis
Dong, J., Albertini, D. F., Nishimori, K., Kumar, T. R., Lu, N., & Matzuk, M. M. (1996) · Nature · doi:10.1038/383531a0 · Cited by 1,650 · see citing works
Regulation of ovarian follicular development in primates: facts and hypotheses
GOUGEON, A. (1996) · Endocrine Reviews · doi:10.1210/edrv-17-2-121 · Cited by 1,497 · see citing works
Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality
Gilchrist, R. B., Lane, M., & Thompson, J. G. (2008) · Human Reproduction Update · doi:10.1093/humupd/dmm040 · Cited by 1,155 · see citing works
Galloway, S., McNatty, K. P., Cambridge, L. M., et al. (2000) · Nature Genetics · doi:10.1038/77033 · Cited by 1,111 · see citing works
Paracrine Actions Of Growth Differentiation Factor-9 in the Mammalian Ovary
Elvin, J. A., Clark, A. T., Wang, P., Wolfman, N. M., & Matzuk, M. M. (1999) · Molecular Endocrinology · doi:10.1210/mend.13.6.0310 · Cited by 650 · see citing works
Wilson, T. M., Wu, X., Juengel, J. L., et al. (2001) · Biology of Reproduction · doi:10.1095/biolreprod64.4.1225 · Cited by 558 · see citing works
Mulsant, P., Lecerf, F., Fabre, S., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091577598 · Cited by 497 · see citing works
Formation of the Ovarian Follicular Antrum and Follicular Fluid1
Rodgers, R. J., & Irving‐Rodgers, H. F. (2010) · Biology of Reproduction · doi:10.1095/biolreprod.109.082941 · Cited by 453 · see citing works
Follicle Selection in Monovular Species
Ginther, O. J., Beg, M. A., Bergfelt, D. R., Donadeu, F. X., & Kot, K. (2001) · Biology of Reproduction · doi:10.1095/biolreprod65.3.638 · Cited by 405 · see citing works
Gap junctions and ovarian folliculogenesis
Kidder, G. M., & Mhawi, A. (2002) · Reproduction · doi:10.1530/rep.0.1230613 · Cited by 347 · see citing works
Regulation of folliculogenesis and the determination of ovulation rate in ruminants
Scaramuzzi, R. J., Baird, D. T., Campbell, B. K., Driancourt, M. A., Dupont, J., Fortune, J. E., Gilchrist, R. B., Martin, G. B., McNatty, K. P., McNeilly, A. S., et al. (2011) · Reproduction Fertility and Development · doi:10.1071/rd09161 · Cited by 310 · see citing works
Self-citationKidder, G. M., & Vanderhyden, B. C. (2010) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y10-009 · Cited by 304 · see citing works
Differentiation of Dominant Versus Subordinate Follicles in Cattle1
Fortune, J. E., Rivera, G. M., Evans, A. C. O., & Turzillo, A. M. (2001) · Biology of Reproduction · doi:10.1095/biolreprod65.3.648 · Cited by 291 · see citing works
Zhang, H., Risal, S., Gorre, N., Busayavalasa, K., Li, X., Shen, Y., Bosbach, B., Brännström, M., & Liu, K. (2014) · Current Biology · doi:10.1016/j.cub.2014.09.023 · Cited by 274 · see citing works
Otsuka, F., & Shimasaki, S. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.122066899 · Cited by 258 · see citing works
Monniaux, D., Clément, F., Dalbiès-Tran, R., Estienne, A., Fabre, S., Mansanet, C., & Monget, P. (2014) · Biology of Reproduction · doi:10.1095/biolreprod.113.117077 · Cited by 233 · see citing works
Self-citationRegulation of ovulation rate in mammals: contribution of sheep genetic models
Fabre, S., Pierre, A., Mulsant, P., et al. (2006) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-4-20 · Cited by 231 · see citing works
Thomas, F. H., & Vanderhyden, B. C. (2006) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-4-19 · Cited by 229 · see citing works
Populations of granulosa cells in small follicles of the sheep ovary
Lundy, T., Smith, P. R., O’Connell, A. R., et al. (1999) · Reproduction · doi:10.1530/jrf.0.1150251 · Cited by 206 · see citing works
The Pattern of Follicular Growth and Atresia in the Ovine Ovary
Turnbull, K., Braden, A., & Mattner, P. E. (1977) · Australian Journal of Biological Sciences · doi:10.1071/bi9770229 · Cited by 167 · see citing works
Oocyte-expressed genes affecting ovulation rate
McNatty, K. P., Smith, P. R., Moore, L. G., et al. (2005) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2004.08.013 · Cited by 146 · see citing works
Ultrasonographic study of ovarian follicular dynamics in ewes during the oestrous cycle
Ravindra, J. P., Rawlings, N. C., Evans, A. C. O., et al. (1994) · Reproduction · doi:10.1530/jrf.0.1010501 · Cited by 139 · see citing works
Ireland, J. J., Mihm, M., Austin, E. J., et al. (2000) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(00)75033-8 · Cited by 136 · see citing works
Stubbs, S. A., Stark, J., Dilworth, S. M., Franks, S., & Hardy, K. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-0729 · Cited by 130 · see citing works
Follicular growth and ovarian dynamics in mammals.
Monniaux, D., Huet, C., Besnard, N., et al. (1997) · PubMed · Cited by 123 · see citing works
Self-citationda Silva‐Buttkus, P., Jayasooriya, G. S., Mora, J. M., Mobberley, M. A., Ryder, T. A., Baithun, M., Stark, J., Franks, S., & Hardy, K. (2008) · Journal of Cell Science · doi:10.1242/jcs.036400 · Cited by 121 · see citing works
Single-cell technologies sharpen up mammalian stem cell research
Hoppe, P. S., Coutu, D. L., & Schroeder, T. (2014) · Nature Cell Biology · doi:10.1038/ncb3042 · Cited by 104 · see citing works
Physiological effects of major genes affecting ovulation rate in sheep
McNatty, K. P., Galloway, S., Wilson, T. M., et al. (2004) · Genetics Selection Evolution · doi:10.1051/gse:2004029 · Cited by 97 · see citing works
Braw-Tal, R., McNatty, K. P., Smith, P. R., et al. (1993) · Biology of Reproduction · doi:10.1095/biolreprod49.5.895 · Cited by 93 · see citing works
Tajima, Y., Moore, M. A. S., Soares, V. C., Ono, M., Kissel, H., & Besmer, P. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.20.11903 · Cited by 88 · see citing works
Myers, M., Middlebrook, B. S., Matzuk, M. M., & Pangas, S. A. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.08.001 · Cited by 82 · see citing works
Effect of follicle size and of the Fec B Booroola gene on oocyte function in sheep
Cognié, Y., Benoit, F., Poulin, N., et al. (1998) · Reproduction · doi:10.1530/jrf.0.1120379 · Cited by 75 · see citing works
Fabre, S., Pierre, A., Pisselet, C., et al. (2003) · Journal of Endocrinology · doi:10.1677/joe.0.1770435 · Cited by 75 · see citing works
The ovarian reserve in mammals: A functional and evolutionary perspective
Monget, P., Bobe, J., Gougeon, A., Fabre, S., Monniaux, D., & Dalbiès‐Tran, R. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.07.046 · Cited by 69 · see citing works
Self-citationEstienne, A., Pierre, A., di Clemente, N., Picard, J., Jarrier-Gaillard, P., Mansanet, C., Monniaux, D., & Fabre, S. (2014) · Endocrinology · doi:10.1210/en.2014-1551 · Cited by 67 · see citing works
Self-citationTsonis, C. G., Carson, R. S., & Findlay, J. K. (1984) · Reproduction · doi:10.1530/jrf.0.0720153 · Cited by 66 · see citing works
Kit Ligand 2 Promotes Murine Oocyte Growth In Vitro1
Thomas, F. H., Ismail, R. S., Jiang, J.-Y., et al. (2007) · Biology of Reproduction · doi:10.1095/biolreprod.106.058529 · Cited by 61 · see citing works
Crawford, J. L., Heath, D. A., Reader, K. L., et al. (2011) · Reproduction · doi:10.1530/rep-10-0485 · Cited by 49 · see citing works
Multi-scale modeling of the follicle selection process in the ovary
Echenim, N., Monniaux, D., Sorine, M., et al. (2005) · Mathematical Biosciences · doi:10.1016/j.mbs.2005.05.003 · Cited by 44 · see citing works
Self-citationMultiscale modelling of ovarian follicular selection
Clément, F., & Monniaux, D. (2012) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2012.12.005 · Cited by 37 · see citing works
Self-citationCleément, F., Gruet, M.-A., Monget, P., et al. (1997) · Cell Proliferation · doi:10.1111/j.1365-2184.1997.tb00939.x · Cited by 33 · see citing works
Mathematical model of FSH-induced cAMP production in ovarian follicles
Clément, F., Monniaux, D., Stark, J., et al. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.281.1.e35 · Cited by 33 · see citing works
Self-citationThe number of clonal precursors of the follicular epithelium in the mouse ovary
Telfer, E. E., Ansell, J., Taylor, H., et al. (1988) · Reproduction · doi:10.1530/jrf.0.0840105 · Cited by 29 · see citing works
Clonal analysis of chimaeric mouse ovaries using DNA in situ hybridization
Boland, N. I., & Gosden, R. G. (1994) · Reproduction · doi:10.1530/jrf.0.1000203 · Cited by 26 · see citing works
Optimal control of the cell dynamics in the granulosa of ovulatory follicles
Clément, F. (1998) · Mathematical Biosciences · doi:10.1016/s0025-5564(98)10026-3 · Cited by 17 · see citing works
Self-citationContribution of a mathematical modelling approach to the understanding of the ovarian function
Clément, F., Monniaux, D., Thalabard, J., et al. (2002) · Comptes Rendus Biologies · doi:10.1016/s1631-0691(02)01457-9 · Cited by 14 · see citing works
Self-citationMultiscale Modeling of Follicular Ovulation as a Mass and Maturity Dynamical System
Michel, P. (2011) · Multiscale Modeling and Simulation · doi:10.1137/090745738 · Cited by 13 · see citing works
Self-citationCauchy problem for multiscale conservation laws: Application to structured cell populations
Shang, P. (2013) · Journal of Mathematical Analysis and Applications · doi:10.1016/j.jmaa.2013.01.001 · Cited by 12 · see citing works
Clément, F., Michel, P., Monniaux, D., et al. (2013) · Multiscale Modeling and Simulation · doi:10.1137/120897249 · Cited by 10 · see citing works
Self-citationPisselet, C., Clément, F., & Monniaux, D. (2000) · annales de biologie animale biochimie biophysique · doi:10.1051/rnd:2000133 · Cited by 10 · see citing works
Self-citationMultiscale Modeling of Follicular Ovulation as a Mass and Maturity Dynamical System
Michel, P. (2011) · HAL (Le Centre pour la Communication Scientifique Directe) · Cited by 9 · see citing works
Self-citationAymard, B., Clément, F., Coquel, F., et al. (2013) · SIAM Journal on Scientific Computing · doi:10.1137/120904238 · Cited by 7 · see citing works
Self-citationNumerical simulation of the selection process of the ovarian follicles
Aymard, B., Clément, F., Coquel, F., et al. (2012) · ESAIM Proceedings · doi:10.1051/proc/201238006 · Cited by 7 · see citing works
Self-citationOptimal Control of Cell Mass and Maturity in a Model of Follicular Ovulation
Clément, F., Coron, J., & Shang, P. (2013) · SIAM Journal on Control and Optimization · doi:10.1137/120862247 · Cited by 6 · see citing works
Self-citationToosi, B. M., Seekallu, S. V., & RAWLINGS, N. C. (2010) · Biology of Reproduction · doi:10.1095/biolreprod.109.082016 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Mathematical Modelling of Endocrine Systems
Zavala, E., Wedgwood, K. C. A., Voliotis, M., Tabak, J., Spiga, F., Lightman, S. L., & Tsaneva-Atanasova, K. (2019) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2019.01.008 · Cited by 81 · see citing works
“Mathematical modelling has also been employed to understand the macroscopic processes involved in follicular development [67].”
Fischer-Holzhausen, S., & Röblitz, S. (2022) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2022.111150 · Cited by 17 · see citing works
Clément, F., Crépieux, P., Yvinec, R., & Monniaux, D. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.110877 · Cited by 16 · see citing works
Self-citationFollicular competition in cows: the selection of dominant follicles as a synergistic effect
Lange, A., Schwieger, R., Plöntzke, J., Schäfer, S., & Röblitz, S. (2019) · Journal of Mathematical Biology · doi:10.1007/s00285-018-1284-0 · Cited by 12 · see citing works
- Authors
- Monniaux, D., Michel, P., Postel, M., & Clément, F.
- Affiliations
- Université de Tours (FR)
- École Centrale de Lyon (FR)
- Laboratoire Jacques-Louis Lions (FR)
- Centre Inria de Paris (FR)
- Corresponding author
- Monniaux, Danielle
- Venue
- Biology of the Cell
- Publisher
- Wiley
- Published
- 2016-02-29
- Volume
- 108
- Issue
- 6
- Pages
- 149-160
- ISSN
- 0248-4900 (ISSN-L)
- 1768-322X
- OpenAlex
- W2260955312
- Cited by
- 36
- References
- 57
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 1 · 2023: 2 · 2022: 4 · 2021: 4 · 2020: 7 · 2019: 4 · 2018: 5 · 2017: 1 · 2016: 1
- FWCI
- 0.54
- Type
- journal article
- Language
- en
- Open access
- green
- inria.hal.science
- Licence
- Locations
- Biology of the Cell (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Reproductive Physiology in Livestock
- Keywords
- ovarian follicle development, granulosa cell proliferation, granulosa cell differentiation, granulosa cell apoptosis, spatio-temporal modeling, ovarian cycle, oocyte size
- MeSH terms
- Animals, Cell Differentiation, Female, Granulosa Cells, Humans, Models, Biological, Ovulation, Apoptosis, Cell Proliferation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
