Skip to main content

Advertisement

SpringerLink
Log in

Biomechanics and mechanical signaling in the ovary: a systematic review

  • Review
  • Published:
Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

Purpose

Mammalian oogenesis and folliculogenesis share a dynamic connection that is critical for gamete development. For maintenance of quiescence or follicular activation, follicles must respond to soluble signals (growth factors and hormones) and physical stresses, including mechanical forces and osmotic shifts. Likewise, mechanical processes are involved in cortical tension and cell polarity in oocytes. Our objective was to examine the contribution and influence of biomechanical signaling in female mammalian gametogenesis.

Methods

We performed a systematic review to assess and summarize the effects of mechanical signaling and mechanotransduction in oocyte maturation and folliculogenesis and to explore possible clinical applications. The review identified 2568 publications of which 122 met the inclusion criteria.

Results

The integration of mechanical and cell signaling pathways in gametogenesis is complex. Follicular activation or quiescence are influenced by mechanical signaling through the Hippo and Akt pathways involving the yes-associated protein (YAP), transcriptional coactivator with PDZ-binding motif (TAZ), phosphatase and tensin homolog deleted from chromosome 10 (PTEN) gene, the mammalian target of rapamycin (mTOR), and forkhead box O3 (FOXO3) gene.

Conclusions

There is overwhelming evidence that mechanical signaling plays a crucial role in development of the ovary, follicle, and oocyte throughout gametogenesis. Emerging data suggest the complexities of mechanotransduction and the biomechanics of oocytes and follicles are integral to understanding of primary ovarian insufficiency, ovarian aging, polycystic ovary syndrome, and applications of fertility preservation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. John GB, Gallardo TD, Shirley LJ, Castrillon DH. Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev Biol. 2008;321:197–204.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Anderson RA, McLaughlin M, Wallace WHB, Albertini DF, Telfer EE. The immature human ovary shows loss of abnormal follicles and increasing follicle developmental competence through childhood and adolescence. Hum Reprod. 2014;29:97–106.

    Article  PubMed  CAS  Google Scholar 

  3. Ingber DE. Cellular mechanotransduction: putting all the pieces together again. FASEB J. 2006;20:1230–2.

    Article  CAS  Google Scholar 

  4. Heisenberg CP, Bellaïche Y. Forces in tissue morphogenesis and patterning. Cell. 2013;153:948–62.

    Article  PubMed  CAS  Google Scholar 

  5. Albertini DF, Barrett SL. The developmental origins of mammalian oocyte polarity. Semin Cell Dev Biol. 2004;15:599–606.

    Article  PubMed  Google Scholar 

  6. Thorne JT, Segal TR, Chang S, Jorge S, Segars JH, Leppert PC. Dynamic reciprocity between cells and their microenvironment in reproduction. Biol Reprod. 2015;92:1–10.

    Article  CAS  Google Scholar 

  7. Moher D, Liberati A, Tetzlaff J, Altman DG, Altman D, Antes G, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Jorge S, Chang S, Barzilai JJ, Leppert P, Segars JH. Mechanical signaling in reproductive tissues: mechanisms and importance. Reprod Sci. 2014;21:1093–107.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Hornick JE, Duncan FE, Shea LD, Woodruff TK. Isolated primate primordial follicles require a rigid physical environment to survive and grow in vitro. Hum Reprod. 2012;27:1801–10.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Shea LD, Woodruff TK, Shikanov A. Bioengineering the ovarian follicle microenvironment. Annu Rev Biomed Eng. 2014;16:29–52.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Xu M, West E, Shea LD, Woodruff TK. Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development. Biol Reprod. 2006;75:916–23.

    Article  PubMed  CAS  Google Scholar 

  12. West ER, Xu M, Woodruff TK, Shea LD. Physical properties of alginate hydrogels and their effects on in vitro follicle development. Biomaterials. 2007;28:4439–48.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. West ER, Shea LD, Woodruff TK. Engineering the follicle microenvironment. Semin Reprod Med. 2007;25:287–99.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Shikanov A, Xu M, Woodruff TK, Shea LD. Interpenetrating fibrin–alginate matrices for in vitro ovarian follicle development. Biomaterials Elsevier Ltd. 2009;30:5476–85.

    Article  CAS  Google Scholar 

  15. Smith RM, Woodruff TK, Shea LD. Designing follicle–environment interactions with biomaterials. Cancer Treat Res. 2010;156:11–24.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Woodruff TK, Shea LD. A new hypothesis regarding ovarian follicle development: ovarian rigidity as a regulator of selection and health. J Assist Reprod Genet. 2011;28:3–6.

    Article  PubMed  Google Scholar 

  17. Abel MH, Wootton AN, Wilkins V, Huhtaniemi I, Knight PG, Charlton HM. The effect of a null mutation in the follicle-stimulating hormone receptor gene on mouse reproduction. Endocrinology. 2000;141:1795–803.

    Article  PubMed  CAS  Google Scholar 

  18. McGee E, Hsueh AJ. Initial and cyclic recruitment of ovarian follicles. Endocr Rev. 2000;21:200–14.

    PubMed  CAS  Google Scholar 

  19. Kawamura K, Cheng Y, Suzuki N, Deguchi M, Sato Y, Takae S, et al. Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proc Natl Acad Sci. 2013;110:17474–9.

    Article  PubMed  Google Scholar 

  20. Cordeiro CN, Christianson MS, Selter JH, Segars JH. In vitro activation: a possible new frontier for treatment of primary ovarian insufficiency. Reprod Sci. 2016;23:429–38.

    Article  PubMed  CAS  Google Scholar 

  21. Xiang C, Li J, Hu L, Huang J, Luo T, Zhong Z, et al. Hippo signaling pathway reveals a spatio-temporal correlation with the size of primordial follicle pool in mice. Cell Physiol Biochem. 2015;35:957–68.

    Article  PubMed  CAS  Google Scholar 

  22. Dupont S. Role of YAP/TAZ in cell–matrix adhesion-mediated signalling and mechanotransduction. Exp Cell Res Elsevier. 2016;343:42–53.

    Article  CAS  Google Scholar 

  23. Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S, Cordenonsi M, et al. Role of YAP/TAZ in mechanotransduction. Nature. 2011;474:179–83.

    Article  PubMed  CAS  Google Scholar 

  24. Provenzano PP, Keely PJ. Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and rho GTPase signaling. J Cell Sci. 2011;124:1195–205.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Kawashima I, Kawamura K. Regulation of follicle growth through hormonal factors and mechanical cues mediated by hippo signaling pathway. Syst Biol Reprod Med. 2017:1–9.

  26. Abbassi L, Malki S, Cockburn K, Macaulay A, Robert C, Rossant J, et al. Multiple mechanisms cooperate to constitutively exclude the transcriptional co-activator YAP from the nucleus during murine oogenesis. Biol Reprod. 2016;94:102.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Cheng Y, Feng Y, Jansson L, Sato Y, Deguchi M, Kawamura K, et al. Actin polymerization-enhancing drugs promote ovarian follicle growth mediated by the hippo signaling effector YAP. FASEB J. 2015;29:2423–30.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Brigstock DR. The connective tissue growth factor/cysteine-rich 61/nephroblastoma overexpressed (CCN) family. Endocr Rev. 1999;20:189–206.

    PubMed  CAS  Google Scholar 

  29. Wada K, Itoga K, Okano T, Yonemura S, Sasaki H. Hippo pathway regulation by cell morphology and stress fibers. Development. 2011;138:3907–14.

    Article  PubMed  CAS  Google Scholar 

  30. Aragona M, Panciera T, Manfrin A, Giulitti S, Michielin F, Elvassore N, et al. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell. 2013;154:1047–59.

    Article  PubMed  CAS  Google Scholar 

  31. Cantley LC, Fruman DA, Meyers RE, Cantley LC, Lawlor MA, Alessi DR, et al. The phosphoinositide 3-kinase pathway. Science. 2002;296:1655–7.

  32. Cecconi S, Mauro A, Cellini V, Patacchiola F. The role of Akt signalling in the mammalian ovary. Int J Dev Biol. 2012;56:809–17.

    Article  PubMed  CAS  Google Scholar 

  33. Li J, Kawamura K, Cheng Y, Liu S, Klein C, Liu S, et al. Activation of dormant ovarian follicles to generate mature eggs. Proc Natl Acad Sci. 2010;107:10280–4.

    Article  PubMed  Google Scholar 

  34. Ernst EH, Grøndahl ML, Grund S, Hardy K, Heuck A, Sunde L, et al. Dormancy and activation of human oocytes from primordial and primary follicles: molecular clues to oocyte regulation. Hum Reprod. 2017;32:1684–700.

    Article  PubMed  CAS  Google Scholar 

  35. Ezzati MM, Baker MD, Saatcioglu HD, Aloisio GM, Pena CG, Nakada Y, et al. Regulation of FOXO3 subcellular localization by kit ligand in the neonatal mouse ovary. J Assist Reprod Genet. 2015;32:1741–7.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Sobinoff AP, Sutherland JM, McLaughlin EA. Intracellular signalling during female gametogenesis. Mol Hum Reprod. 2013;19:265–78.

    Article  PubMed  CAS  Google Scholar 

  37. John GB, Shidler MJ, Besmer P, Castrillon DH. Kit signaling via PI3K promotes ovarian follicle maturation but is dispensable for primordial follicle activation. Dev Biol. 2010;331:292–9.

    Article  CAS  Google Scholar 

  38. Jones RL, Pepling ME. KIT signaling regulates primordial follicle formation in the neonatal mouse ovary. Dev Biol Elsevier. 2013;382:186–97.

    Article  CAS  Google Scholar 

  39. Saatcioglu HD, Cuevas I, Castrillon DH. Control of oocyte reawakening by kit. PLoS Genet. 2016;12:e1006215.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Reddy P, Shen L, Ren C, Boman K, Lundin E, Ottander U, et al. Activation of Akt (PKB) and suppression of FKHRL1 in mouse and rat oocytes by stem cell factor during follicular activation and development. Dev Biol. 2005;281:160–70.

    Article  PubMed  CAS  Google Scholar 

  41. Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science (80-. ). 2003;301:215–8.

  42. Sun HW, Tong SL, He J, Wang Q, Zou L, Ma SJ, et al. RhoA and RhoC-siRNA inhibit the proliferation and invasiveness activity of human gastric carcinoma by rho/PI3K/Akt pathway. World J Gastroenterol. 2007;13:3517–22.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Goto M, Iwase A, Ando H, Kurotsuchi S, Harata T, Kikkawa F. PTEN and Akt expression during growth of human ovarian follicles. J Assist Reprod Genet. 2007;24:541–6.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Kim SY, Ebbert K, Cordeiro MH, Romero M, Zhu J, Serna VA, et al. Cell autonomous phosphoinositide 3-kinase activation in oocytes disrupts normal ovarian function through promoting survival and overgrowth of ovarian follicles. Endocrinology. 2015;156:1464–76.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, et al. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science (80-. ) 2008;319:611–3.

  46. Reddy P, Adhikari D, Zheng W, Liang S, Hamalainen T, Tohonen V, et al. PDK1 signaling in oocytes controls reproductive aging and lifespan by manipulating the survival of primordial follicles. Hum Mol Genet. 2009;18:2813–24.

    Article  PubMed  CAS  Google Scholar 

  47. Jagarlamudi K, Liu L, Adhikari D, Reddy P, Idahl A, Ottander U, et al. Oocyte-specific deletion of Pten in mice reveals a stage-specific function of PTEN/PI3K signaling in oocytes in controlling follicular activation. PLoS One. 2009;4:3–9.

    Article  CAS  Google Scholar 

  48. Cheng Y, Kim J, Li XX, Hsueh AJ. Promotion of ovarian follicle growth following mTOR activation: synergistic effects of AKT stimulators. PLoS One. 2015;10:1–9.

    Google Scholar 

  49. Tong Y, Li F, Lu Y, Cao Y, Gao J, Liu J. Rapamycin-sensitive mTORC1 signaling is involved in physiological primordial follicle activation in mouse ovary. Mol Reprod Dev. 2013;80:1018–34.

    Article  PubMed  CAS  Google Scholar 

  50. Adhikari D, Zheng W, Shen Y, Gorre N, Hämäläinen T, Cooney AJ, et al. Tsc/mTORC1 signaling in oocytes governs the quiescence and activation of primordial follicles. Hum Mol Genet. 2009;19:397–410.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Lu X, Guo S, Cheng Y, Kim JH, Feng Y, Feng Y. Stimulation of ovarian follicle growth after AMPK inhibition. Reproduction. 2017;153:683–94.

    Article  PubMed  CAS  Google Scholar 

  52. Zhao Y, Zhang Y, Li J, Zheng N, Xu X, Yang J, et al. MAPK3/1 participates in the activation of primordial follicles through mTORC1-KITL signaling. J Cell Physiol. 2018;233:226–37.

    Article  PubMed  CAS  Google Scholar 

  53. Adhikari D, Risal S, Liu K, Shen Y. Pharmacological inhibition of mTORC1 prevents over-activation of the primordial follicle pool in response to elevated PI3K signaling. PLoS One. 2013;8:e53810.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Zhang XM, Li L, Xu JJ, Wang N, Liu WJ, Lin XH, et al. Rapamycin preserves the follicle pool reserve and prolongs the ovarian lifespan of female rats via modulating mTOR activation and sirtuin expression. Gene. 2013;523:82–7.

    Article  PubMed  CAS  Google Scholar 

  55. Jiang Z-Z, Hu M-W, Ma X-S, Schatten H, Fan H-Y, Wang Z-B, et al. LKB1 acts as a critical gatekeeper of ovarian primordial follicle pool. Oncotarget. 2016;7:5738–53.

    PubMed  Google Scholar 

  56. Ren Y, Suzuki H, Jagarlamudi K, Golnoski K, McGuire M, Lopes R, et al. Lhx8 regulates primordial follicle activation and postnatal folliculogenesis. BMC Biol. 2015;13:1–12.

    Article  CAS  Google Scholar 

  57. Albertini DF, Combelles CMH, Benecchi E, Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction. 2001;121:647–53.

    Article  PubMed  CAS  Google Scholar 

  58. Da Silva-Buttkus P, Jayasooriya GS, Mora JM, Mobberley M, Ryder TA, Baithun M, et al. Effect of cell shape and packing density on granulosa cell proliferation and formation of multiple layers during early follicle development in the ovary. J Cell Sci. 2008;121:3890–900.

    Article  PubMed  CAS  Google Scholar 

  59. McLaughlin M, Bromfield JJ, Albertini DF, Telfer EE. Activin promotes follicular integrity and oogenesis in cultured pre-antral bovine follicles. Mol Hum Reprod. 2010;16:644–53.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Pangas SA, Rademaker AW, Fishman DA, Woodruff TK. Localization of the activin signal transduction components in normal human ovarian follicles: implications for autocrine and paracrine signaling in the ovary. J Clin Endocrinol Metab. 2002;87:2644–57.

    Article  PubMed  CAS  Google Scholar 

  61. Chang HM, Cheng JC, Liu Y, Klausen C, Xu C, Leung PCK. Activin A-induced increase in LOX activity in human granulosa-lutein cells is mediated by CTGF. Reproduction. 2016;152:293–301.

    Article  PubMed  CAS  Google Scholar 

  62. Chang HM, Fang Y, Liu PP, Cheng JC, Yang X, Leung PC. Connective tissue growth factor mediates growth differentiation factor 8-induced increase of lysyl oxidase activity in human granulosa-lutein cells. MolCell Endocrinol. 2016;434:186–98.

    CAS  Google Scholar 

  63. Fang Y, Chang HM, Cheng JC, Klausen C, Leung PCK, Yang X. Transforming growth factor-β1 increases lysyl oxidase expression by downregulating MIR29A in human granulose lutein cells. Reproduction. 2016;152:205–13.

    Article  PubMed  CAS  Google Scholar 

  64. Yang S, Wang S, Luo A, Ding T, Lai Z, Shen W, et al. Expression patterns and regulatory functions of microRNAs during the initiation of primordial follicle development in the neonatal mouse ovary. Biol Reprod. 2013;89:1–11.

    Google Scholar 

  65. He X, Toth TL. In vitro culture of ovarian follicles from Peromyscus. Semin Cell Dev Biol. 2017;61:140–9.

    Article  PubMed  CAS  Google Scholar 

  66. Zielak-Steciwko AE, Browne JA, McGettigan PA, Gajewska M, Dzieciol M, Szulc T, et al. Expression of microRNAs and their target genes and pathways associated with ovarian follicle development in cattle. Physiol Genomics. 2014;46:735–45.

    Article  PubMed  CAS  Google Scholar 

  67. Plancha CE, Sanfins A, Rodrigues P, Albertini D. Cell polarity during folliculogenesis and oogenesis. Reprod BioMed Online. 2005;10:478–84.

    Article  PubMed  Google Scholar 

  68. Rodgers RJ, Irving-Rodgers HF, Russell DL. Extracellular matrix of the developing ovarian follicle. Reproduction. 2003;126:415–24.

    Article  PubMed  CAS  Google Scholar 

  69. Bernal AL, Mardon H. Focal adhesion proteins in human granulosa cells. Reprod Technol. 2000;10:29–38.

    CAS  Google Scholar 

  70. Rodgers RJ, Irving-Rodgers HF. Formation of the ovarian follicular antrum and follicular fluid. Biol Reprod. 2010;82:1021–9.

    Article  PubMed  CAS  Google Scholar 

  71. Hsueh AJW, Kawamura K, Cheng Y, Fauser BCJM. Intraovarian control of early folliculogenesis. Endocr Rev. 2015;36:1–24.

    Article  PubMed  CAS  Google Scholar 

  72. Kino T, Segars JH, Chrousos GP. The guanine nucleotide exchange factor Brx: a link between osmotic stress, inflammation and organ physiology and pathophysiology. Expert Rev Endocrinol Metab. 2010;5:603–14.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Grive KJ, Freiman RN. The developmental origins of the mammalian ovarian reserve. Development. 2015;142:2554–63.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Bristol SK, Woodruff TK. Follicle-restricted compartmentalization of transforming growth factor beta superfamily ligands in the feline ovary. Biol Reprod. 2004;70:846–59.

    Article  PubMed  CAS  Google Scholar 

  75. Makker A, Goel MM, Mahdi AA. PI3K/PTEN/Akt and TSC/mTOR signaling pathways, ovarian dysfunction, and infertility: an update. J Mol Endocrinol. 2014;53:R103–18.

    Article  PubMed  CAS  Google Scholar 

  76. Ryan KE, Casey SM, Canthy MJ, Crowe MA, Martin F, Evans ACO. Akt and Erk signal transduction pathways are early markers of differentiation in dominant and subordinate ovarian follicles in cattle. Reproduction. 2007;133:617–26.

    Article  PubMed  CAS  Google Scholar 

  77. Evans AC, Martin F. Kinase pathways in dominant and subordinate ovarian follicles during the first wave of follicular development in sheep. Anim Reprod Sci. 2000;64:221–31.

    Article  PubMed  CAS  Google Scholar 

  78. Matousek M, Carati C, Gannon B, Brännström M. Novel method for intrafollicular pressure measurements in the rat ovary: increased intrafollicular pressure after hCG stimulation. Reproduction. 2001;121:307–14.

    Article  PubMed  CAS  Google Scholar 

  79. Richard S, Tartia AP, Boison D, Baltz JM. Mouse oocytes acquire mechanisms that permit independent cell volume regulation at the end of oogenesis. J Cell Physiol. 2016;232:2436–46.

    Article  CAS  Google Scholar 

  80. Curry TE, Smith MF. Impact of extracellular matrix remodeling on ovulation and the folliculo-luteal transition. Semin Reprod Med. 2006;24:228–41.

    Article  PubMed  CAS  Google Scholar 

  81. Gubbay O, Guo W, Rae MT, Niven D, Langdon SP, Hillier SG. Inflammation-associated gene expression is altered between normal human ovarian surface epithelial cells and cell lines derived from ovarian adenocarcinomas. Br J Cancer. 2005;92:1927–33.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Puttabyatappa M, Al-Alem LF, Zakerkish F, Rosewell KL, Brännström M, Curry TE. Induction of tissue factor pathway inhibitor 2 by hCG regulates periovulatory gene expression and plasmin activity. Endocrinology. 2017;158:109–20.

    Article  PubMed  Google Scholar 

  83. Murdoch WJ, Gottsch ML. Proteolytic mechanisms in the ovulatory folliculo-luteal transformation. Connect Tissue Res. 2003;44:50–7.

    Article  PubMed  CAS  Google Scholar 

  84. Murdoch WJ. Regulation of collagenolysis and cell death by plasmin within the formative stigma of preovulatory ovine follicles. J Reprod Fertil. 1998;113:331–6.

    Article  PubMed  CAS  Google Scholar 

  85. Murdoch WJ, Colgin DC, Ellis JA. Role of tumor necrosis factor-a in the ovulatory mechanism of ewes. J Anim Sci. 1997;75:1601–5.

    Article  PubMed  CAS  Google Scholar 

  86. Ko C, Gieske MC, Al-Alem L, Hahn Y, Su W, Gong MC, et al. Endothelin-2 in ovarian follicle rupture. Endocrinology. 2006;147:1770–9.

    Article  PubMed  CAS  Google Scholar 

  87. Bridges PJ, Jo M, Al Alem L, Na G, Su W, Gong MC, et al. Production and binding of endothelin-2 (EDN2) in the rat ovary: endothelin receptor subtype a (EDNRA)-mediated contraction. Reprod Fertil Dev. 2010;22:780–7.

    Article  PubMed  CAS  Google Scholar 

  88. Al-Alem L, Bridges PJ, Su W, Gong MC, Iglarz M, Ko C. Endothelin-2 induces oviductal contraction via endothelin receptor subtype a in rats. J Endocrinol. 2007;193:383–91.

    Article  PubMed  CAS  Google Scholar 

  89. Rolaki A, Drakakis P, Millingos S, Loutradis D, Makrigiannakis A. Novel trends in follicular development, atresia and corpus luteum regression: a role for apoptosis. Reprod BioMed Online. 2005;11:93–103.

    Article  PubMed  Google Scholar 

  90. Evans JP, Robinson DN. The spatial and mechanical challenges of female meiosis. Mol Reprod Dev. 2011;78:769–77.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Larson SM, Lee HJ, Hung PH, Matthews LM, Robinson DN, Evans JP. Cortical mechanics and meiosis II completion in mammalian oocytes are mediated by myosin-II and ezrin–radixin–moesin (ERM) proteins. Mol Biol Cell. 2010;21:3182–92.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Hosseini SM, Moulavi F, Tanhaie-Vash N, Asgari V, Ghanaei HR, Abedi-Dorche M, et al. The principal forces of oocyte polarity are evolutionary conserved but may not affect the contribution of the first two blastomeres to the blastocyst development in mammals. PLoS One. 2016;11:e0148382.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Duan X, Liu J, Zhu CC, Wang QC, Cui XS, Kim NH, et al. RhoA-mediated MLC2 regulates actin dynamics for cytokinesis in meiosis. Cell Cycle. 2016;15:471–7.

    Article  PubMed  CAS  Google Scholar 

  94. Brunet S, Verlhac MH. Positioning to get out of meiosis: the asymmetry of division. Hum Reprod Update. 2011;17:68–75.

    Article  PubMed  Google Scholar 

  95. Sanfins A, Lee GY, Plancha CE, Overstrom EW, Albertini DF. Distinctions in meiotic spindle structure and assembly during in vitro and in vivo maturation of mouse oocytes. Biol Reprod. 2003;69:2059–67.

    Article  PubMed  CAS  Google Scholar 

  96. Barrett SL, Albertini DF. Allocation of gamma-tubulin between oocyte cortex and meiotic spindle influences asymmetric cytokinesis in the mouse oocyte. Biol Reprod. 2007;76:949–57.

    Article  PubMed  CAS  Google Scholar 

  97. Combelles CMH, Albertini DF. Microtubule patterning during meiotic maturation in mouse oocytes is determined by cell cycle-specific sorting and redistribution of gamma-tubulin. Dev Biol. 2001;239:281–94.

    Article  PubMed  CAS  Google Scholar 

  98. Li R, Albertini DF. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat. Rev. Mol. Cell biol. Nat Publ Group. 2013;14:141–52.

    CAS  Google Scholar 

  99. Robinson DN. Cell division: biochemically controlled mechanics. Curr Biol. 2001;11:737–40.

    Article  Google Scholar 

  100. Kloc M, Ghobrial RM, Borsuk E, Kubiak JZ. Polarity and asymmetry during mouse oogenesis and oocyte maturation. Mouse Dev. 2012:23–44.

  101. Jo Y-J, Jang W-I, Namgoong S, Kim N-H. Actin-capping proteins play essential roles in the asymmetric division of maturing mouse oocytes. J Cell Sci. 2015;128:160–70.

    Article  PubMed  CAS  Google Scholar 

  102. Duan X, Zhang H, Pan M, Zhang Y, Sun S. Vesicular transport protein Arf6 modulates cytoskeleton dynamics for polar body extrusion in mouse oocyte meiosis. BBA Mol Cell Res. 2018;1865:455–62.

    CAS  Google Scholar 

  103. Duan X, Liu J, Dai X-X, Liu H-L, Cui X-S, Kim N-H, et al. Rho-GTPase effector ROCK phosphorylates cofilin in actin-meditated cytokinesis during mouse oocyte meiosis. Biol Reprod. 2014;90:1–9.

    Article  CAS  Google Scholar 

  104. Lee SR, Xu YN, Jo YJ, Namgoong S, Kim NH. The rho-GTPase effector ROCK regulates meiotic maturation of the bovine oocyte via myosin light chain phosphorylation and cofilin phosphorylation. Mol Reprod Dev. 2015;82:849–58.

    Article  PubMed  CAS  Google Scholar 

  105. Wang F, Zhang L, Duan X, Zhang GL, Wang ZB, Wang Q, et al. RhoA-mediated FMNL1 regulates GM130 for actin assembly and phosphorylates MAPK for spindle formation in mouse oocyte meiosis. Cell Cycle. 2015;14:2835–43.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. Wang QC, Liu J, Wang ZB, Zhang Y, Duan X, Cui XS, et al. Dynamin 2 regulates actin-mediated spindle migration in mouse oocytes. Biol Cell. 2014;106:193–202.

    Article  PubMed  CAS  Google Scholar 

  107. Jang WI, Jo YJ, Kim HC, Jia JL, Namgoong S, Kim NH. Non-muscle tropomyosin (Tpm3) is crucial for asymmetric cell division and maintenance of cortical integrity in mouse oocytes. Cell Cycle. 2014;13:2359–69.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  108. Pan MH, Wang F, Lu Y, Tang F, Duan X, Zhang Y, et al. FHOD1 regulates cytoplasmic actin-based spindle migration for mouse oocyte asymmetric cell division. J Cell Physiol. 2018;233:2270–8.

    Article  PubMed  CAS  Google Scholar 

  109. Halet G, Carroll J. Rac activity is polarized and regulates meiotic spindle stability and anchoring in mammalian oocytes. Dev Cell. 2007;12:309–17.

    Article  PubMed  CAS  Google Scholar 

  110. De S, Marcinkiewicz JL, Vijayaraghavan S, Kline D. Expression of 14-3-3 protein isoforms in mouse oocytes, eggs and ovarian follicular development. BMC Res Notes. 2012;5:57.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  111. Kolano A, Brunet S, Silk AD, Cleveland DW, Verlhac M-H. Error-prone mammalian female meiosis from silencing the spindle assembly checkpoint without normal interkinetochore tension. Proc Natl Acad Sci. 2012;109:E1858–67.

    Article  PubMed  Google Scholar 

  112. Lee Y, Kim KH, Yoon H, Lee OH, Kim E, Park M, et al. RASD1 knockdown results in failure of oocyte maturation. Cell Physiol Biochem. 2016;40:1289–302.

    Article  PubMed  CAS  Google Scholar 

  113. Hughesdon PE. Morphology and morphogenesis of the Stein–Leventhal ovary and of so-called “hyperthecosis.” Obstet Gynecol Surv 1982;37:59–77.

  114. Hatzirodos N, Bayne RA, Irving-Rodgers HF, Hummitzsch K, Sabatier L, Lee S, et al. Linkage of regulators of TGF-activity in the fetal ovary to polycystic ovary syndrome. FASEB J. 2011;25:2256–65.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. Mukherjee A, Sidis Y, Mahan A, Raher MJ, Xia Y, Rosen ED, et al. FSTL3 deletion reveals roles for TGF-beta family ligands in glucose and fat homeostasis in adults. Proc Natl Acad Sci U S A. 2007;104:1348–53.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  116. Urbanek M, Sam S, Legro RS, Dunaif A. Identification of a polycystic ovary syndrome susceptibility variant in fibrillin-3 and association with a metabolic phenotype. J Clin Endocrinol Metab. 2007;92:4191–8.

    Article  PubMed  CAS  Google Scholar 

  117. D’Ascenzo S, Giusti I, Millimaggi D, Marci R, Tatone C, Colonna RC, et al. Intrafollicular expression of matrix metalloproteinases and their inhibitors in normally ovulating women compared with patients undergoing in vitro fertilization treatment. Eur J Endocrinol. 2004;151:87–91.

    Article  PubMed  Google Scholar 

  118. Tarkun I, Cantürk Z, Arslan BC, Türemen E, Tarkun P. The plasminogen activator system in young and lean women with polycystic ovary syndrome. Endocr J. 2004;51:467–72.

    Article  PubMed  CAS  Google Scholar 

  119. Kort J, Behr B. Biomechanics and developmental potential of oocytes and embryos. Fertil Steril. 2017;108:738–41.

    Article  PubMed  Google Scholar 

  120. Lai D, Takayama S, Smith GD. Recent microfluidic devices for studying gamete and embryo biomechanics. J Biomech Elsevier. 2015;48:1671–8.

    Article  Google Scholar 

  121. Yanez LZ, Camarillo DB. Microfluidic analysis of oocyte and embryo biomechanical properties to improve outcomes in assisted reproductive technologies. Mol Hum Reprod. 2017;23:235–47.

    Article  PubMed  Google Scholar 

  122. He X. Microfluidic encapsulation of ovarian follicles for 3D culture. Ann Biomed Eng. 2017;45:1676–84.

    Article  PubMed  PubMed Central  Google Scholar 

  123. Andolfi L, Masiero E, Giolo E, Martinelli M, Luppi S, dal Zilio S, et al. Investigating the mechanical properties of zona pellucida of whole human oocytes by atomic force spectroscopy. Integr Biol. 2016;8:886–93.

    Article  CAS  Google Scholar 

  124. Kawashima I, Kawamura K. Disorganization of the germ cell pool leads to primary ovarian insufficiency. Reproduction. 2017;153:R205–13.

    Article  PubMed  CAS  Google Scholar 

  125. Yin O, Cayton K, Segars JH. In vitro activation: a dip into the primordial follicle pool? J Clin Endocrinol Metab. 2016;101:3568–70.

    Article  PubMed  CAS  Google Scholar 

  126. Novella-Maestre E, Herraiz S, Rodriguez-Iglesias B, Diaz-Garcia C, Pellicer A. Short-term PTEN inhibition improves in vitro activation of primordial follicles, preserves follicular viability, and restores AMH levels in cryopreserved ovarian tissue from Cancer patients. PLoS One. 2015;10:e0127786.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  127. Suzuki N, Yoshioka N, Takae S, Sugishita Y, Tamura M, Hashimoto S, et al. Successful fertility preservation following ovarian tissue vitrification in patients with primary ovarian insufficiency. Hum Reprod. 2015;30:608–15.

    Article  PubMed  Google Scholar 

  128. Zhai J, Yao G, Dong F, Bu Z, Cheng Y, Sato Y, et al. In vitro activation of follicles and fresh tissue auto-transplantation in primary ovarian insufficiency patients. J Clin Endocrinol Metab. 2016;101:4405–12.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Janice P. Evans, PhD for her suggestions and edits of the manuscript and Jamie Blanck, MLIS, MPA, AHIP for her assistance with the systematic review query.

Funding

In part, by the Howard W. and Georgeanna Seegar Jones Endowment. C.O. was supported by the intramural research program of NICHD, ZIE HD-008737-14.

Author information

Author notes

  1. Jaimin S. Shah and Reem Sabouni contributed equally to this work.

Authors and Affiliations

  1. Department of Obstetrics, Gynecology, and Reproductive Sciences, University of Texas at Houston Health Science Center, Houston, TX, USA

    Jaimin S. Shah

  2. Jones Institute for Reproductive Medicine, Eastern Virginia Medical School, Norfolk, VA, USA

    Reem Sabouni

  3. Howard W. and Georgeanna Seegar Jones Division of Reproductive Sciences and Women’s Health Research, Baltimore, MD, USA

    Kamaria C. Cayton Vaught & James H. Segars

  4. Program in Reproductive and Adult Endocrinology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD, USA

    Carter M. Owen

  5. The Center for Human Reproduction, New York, NY, USA

    David F. Albertini

  6. Gynecology and Obstetrics, 720 Rutland Avenue/Ross 624, Baltimore, MD, 21205, USA

    James H. Segars

Authors
  1. Jaimin S. Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Reem Sabouni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kamaria C. Cayton Vaught
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carter M. Owen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David F. Albertini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. James H. Segars
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to James H. Segars.

Ethics declarations

Conflicts of interest

The authors declare no conflicts of interest.

Electronic supplementary material

ESM 1

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shah, J.S., Sabouni, R., Cayton Vaught, K.C. et al. Biomechanics and mechanical signaling in the ovary: a systematic review. J Assist Reprod Genet 35, 1135–1148 (2018). https://doi.org/10.1007/s10815-018-1180-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10815-018-1180-y

Keywords

Search

Navigation