Species-specific differences in follicular antral sizes result from diffusion-based limitations on the thickness of the granulosa cell layer

Molecular Human Reproduction

Volumn 20, Issue 3, 2014, Pages 208-221

  Bachler M ^a   Menshykau, D ^a,b   De Geyter, Ch ^c   Iber, D ^a,b  

^a ETH ZURICH   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Computational modelling; Gonadotrophins; Gradients; Human follicle development; Scaling

Indexed keywords

COMPUTATIONAL MODELLING; GONADOTROPHINS; GRADIENTS; HUMAN FOLLICLE DEVELOPMENT; SCALING;

ADULT; ANIMALS; BODY SIZE; CELL SIZE; COMPUTER SIMULATION; DIFFUSION; ESTRADIOL; FEMALE; FOLLICLE STIMULATING HORMONE; FOLLICULAR FLUID; GONADOTROPINS; GRANULOSA CELLS; HUMANS; MAMMALS; MODELS, BIOLOGICAL; OOCYTES; SPECIES SPECIFICITY;

EID: 84894322862     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gat078     Document Type: Article

References (71)

1. AdamsGP, Singh J, Baerwald AR. Large animal models for the study of ovarian follicular dynamics in women. Theriogenology 2012;78:1733-1748.
2. Aerts JMJ, Bols PEJ. Ovarian follicular dynamics: a review with emphasis on the bovine species. Part I: Folliculogenesis and pre-antral follicle development. Reprod Domest Anim 2010;45:171-179.
3. Aittomäki K, Lucena JL, Pakarinen P, Sistonen P, Tapanainen J, Gromoll J, Kaskikari R, Sankila EM, Lehväslaiho H, Engel AR et al. Mutation in the follicle-stimulating hormone receptor gene causes hereditary hypergonadotropic ovarian failure. Cell 1995;82:959-968.
4. Assou S, Anahory T, Pantesco V, Le Carrour T, Pellestor F, Klein B, Reyftmann L, Dechaud H, De Vos J, Hamamah S. The human cumulus- oocyte complex gene-expression profile. Hum Reprod 2006;21: 1705-1719.
5. Attaran M, Frasor J, Mascha E, Radwanska E, Rawlins RG. The relationship of human granulosa-lutein cell proliferative index to follicular diameter and serum estradiol. Obstet Gynecol 1998;91:449-453.
6. Aurich C. Reproductive cycles of horses. AnimReprod Sci 2011;124:220-228.
7. Bao B, Garverick HA. Expression of steroidogenic enzyme and gonadotropin receptor genes in bovine follicles during ovarian follicular waves: a review. J Anim Sci 1998;76:1903-1921.
8. Bravo PW, Stabenfeldt GH, Lasley BL, FowlerME. The effect of ovarian follicle size on pituitary and ovarian responses to copulation in domesticated South American camelids. Biol Reprod 1991;45:553-559.
9. Brindle E, Miller RC, Shofer JB, Klein NA, Soules MR, O'Connor KA. Urinary beta-luteinizing hormone and beta-follicle stimulating hormone immunoenzymometric assays for population research. Clin Biochem 2006;39: 1071-1079.
10. Carin M. Numerical simulation of moving boundary problems with the ALE method: validation in the case of a free surface and a moving solidification front. In: Excert from the Proceedings of the COMSOL Conference, 2006.
11. Chiou CM, Yang TS, Yeh SP, Tsai MZ, Cheng SP, Huang MC. Changes in number of granulosa cells, follicular fluid levels and diameter of oocytes during folliculogenesis in pre-pubertal gilts at marketing weight. Asian- Australasian J Anim Sci 2004;17:1647-1651.
12. Christin-Maitre S, Hugues JN; Recombinant FSH Study Group. A comparative randomized multicentric study comparing the step-up versus step-down protocol in polycystic ovary syndrome. Hum Reprod 2003;18:1626-1631.
13. Couse JF, Yates MM, Deroo BJ, Korach KS. Estrogen receptor-beta is critical to granulosa cell differentiation and the ovulatory response to gonadotropins. Endocrinology 2005;146:3247-3262.
14. Cutress IJ, Dickinson EJF, Compton RG. Analysis of commercial general engineering finite element software in electrochemical simulations. J Electroanal Chem 2010;638:76-83.
15. D'Angelo A, Brown J, Amso MN. Coasting (withholding gonadotrophins) for preventing ovarian hyperstimulation syndrome. Cochrane Database Syst Rev 2011;CD002811.
16. De Geyter C, De Geyter M, Schneider HP, Nieschlag E. Interdependent influence of follicular fluid estradiol concentration and motility characteristics of spermatozoa on in-vitro fertilization results. Hum Reprod 1992;7:665-670.
17. Dhar A, Dockery P, O WS, Turner K, Lenton EA, Cooke ID. The human ovarian granulosa cell: a stereological approach. J Anat 1996;188: 671-676.
18. Eppig JJ, Wigglesworth K, Pendola F, Hirao Y. Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells. Biol Reprod 1997;56:976-984.
19. Erickson GF, Wang C, Hsueh AJ. FSH induction of functional LH receptors in granulosa cells cultured in a chemically defined medium. Nature 1979; 279:336-338.
20. Evans ACO. Characteristics of ovarian follicle development in domestic animals. Reprod Domest Anim 2003;38:240-246.
21. Germann P, Menshykau D, Tanaka S, Iber D. Simulating organogensis in COMSOL. In: Proceedings of COMSOL Conference, Stuttgart, 2011.
22. Gloaguen P, Crépieux P, Heitzler D, Poupon A, Reiter E. Mapping the follicle-stimulating hormone-induced signaling networks. Front Endocrinol 2011;2:45.
23. Gosden RG, Telfer E. Scaling of follicular sizes in mammalian ovaries. J Zool 1987;211:157-168.
24. Gougeon A. Dynamics of follicular growth in the human: a model from preliminary results. Hum Reprod (Oxford, England) 1986;1:81-87.
25. Griffin J, Emery BR, Huang I, Peterson CM, Carrell DT. Comparative analysis of follicle morphology and oocyte diameter in four mammalian species (mouse, hamster, pig, and human). J Exp Clin Assist Reprod 2006;3:2.
26. Gupta C, Chapekar T, Chhabra Y, Singh P, Sinha S, Luthra K. Differential response to sustained stimulation by hCG & LH on goat ovarian granulosa cells. Ind J Med Res 2012;135:331.
27. Hermes R, Göritz F, Streich WJ. Assisted reproduction in female rhinoceros and elephants-current status and future perspective. Reprod Domest Anim 2007;(Suppl. 2):33-44.
28. Hirakawa T, Minegishi T, Abe K, Kishi H, Ibuki Y, Miyamoto K. A role of insulin-like growth factor I in luteinizing hormone receptor expression in granulosa cells. Endocrinology 1999;140:4965-4971.
29. Iber D, De Geyter C. Computational modelling of bovine ovarian follicle development. Bmc Syst Biol 2013;7:60.
30. Iber D, Zeller R. Making sense-data-based simulations of vertebrate limb development. Curr Opin Genet Dev 2012;22:570-577.
31. Inzunza J, Morani A, Cheng G, Warner M, Hreinsson J, Gustafsson J-A, Hovatta O. Ovarian wedge resection restores fertility in estrogen receptor beta knockout (ERbeta-/-) mice. Proc Natl Acad Sci USA 2007; 104:600-605.
32. IzumiT, Sakakida S, MuranishiY, NagaiT. Allometric studyon the relationship between the growth of ovarian follicles and oocytes in domestic cats. J Reprod Dev 2012;58:484-489.
33. Jeppesen JV, Kristensen SG, Nielsen ME, Humaidan P, Dal Canto M, Fadini R, Schmidt KT, Ernst E, Yding Andersen C. LH-receptor gene expression in human granulosa and cumulus cells from antral and preovulatory follicles. J Clin Endocrinol Metab 2012;97:E1524-E1531.
34. Kumar TR, Wang Y, Lu N, Matzuk MM. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet 1997;15:201-204.
35. Lueders I, Taya K, Watanabe G, Yamamoto Y, Yamamoto T, Kaewmanee S, Niemuller C, Gray C, Streich WJ, Hildebrandt TB. Role of the double luteinizing hormone peak, luteinizing follicles, and the secretion of inhibin for dominant follicle selection in Asian elephants (Elephas maximus). Biol Reprod 2011;85:714-720.
36. Manjunatha BM, Pratap N, Al-Bulushi S, Hago BE. Characterization of ovarian follicular dynamics in dromedary camels (Camelus dromedarius). Theriogenology 2012;78:965-973.
37. McNatty KP. Hormonal correlates of follicular development in the human ovary. Aust J Biol Sci 1981;34:249-268.
38. Menshykau D, Iber D. Simulating organogenesis with comsol: interacting and deforming domains. In: Proceedings of COMSOL Conference, Milano, 2012.
39. Menshykau D, Kraemer C, Iber D. Branch mode selection during early lung development. Plos Comput Biol 2012;8:e1002377.
40. Minegishi T, Hirakawa T, Kishi H, Abe K, Abe Y, Mizutani T, Miyamoto K. A role of insulin-like growth factor I for follicle-stimulating hormone receptor expression in rat granulosa cells. Biol Reprod 2000;62:325-333.
41. Mohammadpour AA. Comparative histomorphological study of ovary and ovarian follicles in Iranian Lori-Bakhtiari sheep and native goat. Pak J Biol Sci 2007;10:673-675.
42. M'rabet N, Moffat R, Helbling S, Kaech A, Zhang H, de Geyter C. The CC-allele of the PvuII polymorphic variant in intron 1 of the a-estrogen receptor gene is significantly more prevalent among infertile women at risk of premature ovarian aging. Fertil Steril 2012;98:965-972.
43. Nair AK, Kash JC, Peegel H, Menon KMJ. Post-transcriptional regulation of luteinizing hormone receptor mRNA in the ovary by a novel mRNA-binding protein. J Biol Chem 2002;277:21468-21473.
44. Nakamura K, Liu X, Ascoli M. Seven non-contiguous intracellular residues of the lutropin/choriogonadotropin receptor dictate the rate of agonistinduced internalization and its sensitivity to non-visual arrestins. J Biol Chem 2000;275:241-247.
45. Olivares A, Cárdenas M, Timossi C, Zariñán T, Díaz-Sánchez V, Ulloa-Aguirre A. Reactivity of different LH and FSH standards and preparations in the world health organization matched reagents for enzyme-linked immunoassays of gonadotrophins. Hum Reprod 2000;15:2285-2291.
46. Osteen KG, Mills TM. Changes in the size, distribution and steroid content of rabbit ovarian follicles during early pseudopregnancy. Biol Reprod 1980; 22:1040-1046.
47. Perez Mayorga M, Gromoll J, Behre HM, Gassner C, Nieschlag E, Simoni M. Ovarian response to follicle-stimulating hormone (FSH) stimulation depends on the FSH receptor genotype. J Clin Endocrinol Metab 2000; 85:3365-3369.
48. Reynaud K, de Lesegno CV, Chebrout M, Thoumire S, Chastant-Maillard S. Follicle population, cumulus mucification, and oocyte chromatin configuration during the periovulatory period in the female dog. Theriogenology 2009;72:1120-1131.
49. Rhind SM, Bramley TA, Wright IA, McMillen SR. FSH and LH receptor concentrations in large ovarian follicles of beef cows in high and low levels of body condition at nine weeks post partum. Reprod Fertil Dev 1992;4:515-522.
50. Richards JS. Estradiol receptor content in rat granulosa cells during follicular development: modification by estradiol and gonadotropins. Endocrinology 1975;97:1174-1184.
51. Richards JS, Pangas SA. The ovary: basic biology and clinical implications. J Clin Invest 2010;120:963-972.
52. Richards JS, Russell DL, Ochsner S, Hsieh M, Doyle KH, Falender AE, Lo YK, Sharma SC. Novel signaling pathways that control ovarian follicular development, ovulation, and luteinization. Recent Prog Horm Res 2002; 57:195-220.
53. Rodgers RJ, Irving-RodgersHF. Formation of the ovarian follicular antrum and follicular fluid. Biol Reprod 2010;82:1021-1029.
54. Rodgers RJ, Irving-Rodgers HF, van Wezel IL, Krupa M, Lavranos TC. Dynamics of the membrana granulosa during expansion of the ovarian follicular antrum. Mol Cell Endocrinol 2001;171:41-48.
55. Sangha GK, Guraya SS. DNA, RNA and protein changes in rat ovarian follicles. In Proc Indian Natn' Sci Acad B55 No 1989.
56. Schwall RH, Erickson GF. Inhibition of synthesis of luteinizing hormone (LH) receptors by a down-regulating dose of LH. Endocrinology 1984; 114:1114-1123.
57. Sharma SC, Clemens JW, Pisarska MD, Richards JS. Expression and function of estrogen receptor subtypes in granulosa cells: regulation by estradiol and forskolin. Endocrinology 1999;140:4320-4334.
58. Silva JM, Price CA. Insulin and IGF-I are necessary for FSH-induced cytochrome P450 aromatase but not cytochrome P450 side-chain cleavage gene expression in oestrogenic bovine granulosa cells in vitro. J Endocrinol 2002;174:499-507.
59. Simões J, Almeida JC, Valentim R, Baril G, Azevedo J, Fontes P, Mascarenhas R. Follicular dynamics in Serrana goats. Anim Reprod Sci 2006;95:16-26.
60. Singh J, Adams GP. Histomorphometry of dominant and subordinate bovine ovarian follicles. Anat Rec 2000;258:58-70.
61. Stenman U-H. Standardization of assays for human chorionic gonadotropin. Clin Chem 2004;50:798-800.
62. Stone BA, Serafini PC, Batzofin JH, Quinn P, Kerin JF, Marrs RP. Interrelationships between plasma hormone levels and the content of total protein, gonadotropins and steroid hormones in antral fluids of women undergoing in vitro fertilization. Fertil Steril 1988;50:102-109.
63. Taneja M, Ali A, Singh G. Ovarian follicular dynamics in water buffalo. Theriogenology 1996;46:121-130.
64. Themmen AP, Blok LJ, Post M, Baarends WM, Hoogerbrugge JW, Parmentier M, Vassart G, Grootegoed JA. Follitropin receptor downregulation involves a cAMP-dependent post-transcriptional decrease of receptor mRNA expression. Mol Cell Endocrinol 1991;78:R7-13.
65. Thummler V, Weddemann A. Computation of Space-Time Patterns via ALE Methods. In: Proceedings of COMSOL Conference, Grenoble, 2007.
66. van Wezel IL, Krupa M, Rodgers RJ. Development of the membrana granulosa of bovine antral follicles: structure, location of mitosis and pyknosis, and immunolocalization of involucrin and vimentin. Reprod Fertil Dev 1999;11:37-48.
67. Vetharaniam I, Peterson A, McNatty K. Modelling female reproductive function in farmed animals. Anim Reprod 2010;122:164-173.
68. Weddemann A, Thummler V. Stability analysis of ALE-methods for advectiondiffusion problems. In: Excert fromthe Proceedings of the COMSOL Conference, Hannover, 2008.
69. Wood JR, Strauss JF. Multiple signal transduction pathways regulate ovarian steroidogenesis. Rev Endocr Metab Disord 2002;3:33-46.
70. Xu Z, Garverick HA, Smith GW, Smith MF, Hamilton SA, Youngquist RS. Expression of follicle-stimulating hormone and luteinizing hormone receptor messenger ribonucleic acids in bovine follicles during the first follicular wave. Bio Reprod 1995;53:951-957.
71. Zhou J, Kumar TR, Matzuk MM, Bondy C. Insulin-like growth factor I regulates gonadotropin responsiveness in the murine ovary. Mol Endocrinol 1997; 11:1924-1933.