Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-16T19:20:15.951Z Has data issue: false hasContentIssue false

Chapter 30 - Contributions of Ovarian Stromal Cells to Follicle Culture

from Section 8 - In Vitro Follicle Culture

Published online by Cambridge University Press:  27 March 2021

By
Emma S Gargus  and
Teresa K Woodruff
Edited by
Jacques Donnez  and
S. Samuel Kim
Jacques Donnez
Affiliation:
Catholic University of Louvain, Brussels
S. Samuel Kim
Affiliation:
University of Kansas School of Medicine
Get access

Summary

With the advent of culture models for studying the process of ovarian folliculogenesis some 40 years ago, opportunities arose for the more systematic evaluation of the factors that regulated ovarian function [1]. The initial focus of studies using cultured follicles emphasized two of the then widely recognized roles of the follicle in mammals: the production of ovarian steroid hormones and of viable oocytes during the process of ovulation. As our understanding of the molecular and cellular complexity of this tissue compartment has evolved and deepened, so too has the need to redefine the major functions of the follicle at both local ovarian and systemic levels in the context of reproduction in mammalian species, especially as it relates to the origins and treatments for human infertility [2]. Thus, a shift in the motivation to use cultured follicles in humans has taken place owing primarily to the rapidly evolving field of fertility preservation.

Type
Chapter
Information
Fertility Preservation
Principles and Practice
 , pp. 341 - 354
Publisher: Cambridge University Press
Print publication year: 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

West, ER, Shea, LD, Woodruff, TK. Engineering the follicle microenvironment. Semin Reprod Med, 2007;25(4):287–299.Google Scholar
Woodruff, TK. The emergence of a new interdiscipline: oncofertility. Cancer Treat Res, 2007;138:3–11.Google Scholar
De Vos, M, Smitz, J, Woodruff, TK. Fertility preservation in women with cancer. Lancet (London, England), 2014;384(9950):1302–1310.Google Scholar
Goetsch, AL, Kimelman, D, Woodruff, TK. Fertility Preservation and Restoration for Patients with Complex Medical Conditions. Switzerland: Springer Nature, 2017.Google Scholar
Jeruss, JS, Woodruff, TK. Preservation of fertility in patients with cancer. N Engl J Med, 2009 February 26;360(9):902–911.Google Scholar
Donnez, J, Dolmans, M-M, Diaz, C, Pellicer, A. Ovarian cortex transplantation: time to move on from experimental studies to open clinical application. Fertil Steril, 2015 November;104(5):1097–1098.Google Scholar
Skory, RM, Xu, Y, Shea, LD, Woodruff, TK. Engineering the ovarian cycle using in vitro follicle culture. Hum Reprod, 2015;30(6):1386–1395.Google Scholar
Xiao, S, Zhang, J, Romero, MM et al. In vitro follicle growth supports human oocyte meiotic maturation. Sci Rep, 2015 December 27;5(1):17323.Google Scholar
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(6):1801–1810.Google Scholar
Hornick, JE, Duncan, FE, Shea, LD, Woodruff, TK. Multiple follicle culture supports primary follicle growth through paracrine-acting signals. Reproduction, 2013 January;145(1):19–32.Google Scholar
Tingen, CM, Kiesewetter, SE, Jozefik, J et al. A macrophage and theca cell-enriched stromal cell population influences growth and survival of immature murine follicles in vitro. Reproduction, 2011 June 1;141(6):809–820.CrossRefGoogle ScholarPubMed
Tagler, D, Tu, T, Smith, RM et al. Embryonic fibroblasts enable the culture of primary ovarian follicles within alginate hydrogels. Tissue Eng Part A, 2012 June;18(11–12):1229–1238.Google Scholar
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 1;23(5):1151–1158.Google Scholar
Eppig, JJ. Development in vitro of mouse oocytes from primordial follicles. Biol Reprod, 1996 January 1;54(1):197–207.Google Scholar
Baird, DT, Webb, R, Campbell, BK, Harkness, LM, Gosden, RG. Long-term ovarian function in sheep after ovariectomy and transplantation of autografts Stored at −196 C. Endocrinology, 1999 January;140(1):462–471.Google Scholar
Cushman, RA, Wahl, CM, Fortune, JE. Bovine ovarian cortical pieces grafted to chick embryonic membranes: a model for studies on the activation of primordial follicles. Hum Reprod, 2002 January;17(1):48–54.CrossRefGoogle Scholar
Picton, HM, Gosden, RG. In vitro growth of human primordial follicles from frozen-banked ovarian tissue. Mol Cell Endocrinol, 2000 August;166(1):27–35.Google Scholar
Laronda, MM, Duncan, FE, Hornick, JE et al. Alginate encapsulation supports the growth and differentiation of human primordial follicles within ovarian cortical tissue. J Assist Reprod Genet, 2014;31(8):1013–1028.CrossRefGoogle ScholarPubMed
Jakus, AE, Laronda, MM, Rashedi, AS et al. “Tissue Papers” from organ-specific decellularized extracellular matrices. Adv Funct Mater, 2017;1700992:1–14.Google Scholar
Magoffin, DA, Magarelli, PC. Preantral follicles stimulate luteinizing hormone independent differentiation of ovarian theca-interstitial cells by an intrafollicular paracrine mechanism. Endocrine, 1995;3(2):107–112.Google Scholar
Magoffin, DA. Ovarian theca cell. Int J Biochem Cell Biol, 2005 July;37(7):1344–1349.Google Scholar
Magarelli, PC, Zachow, RJ, Magoffin, DA. Developmental and hormonal regulation of rat theca-cell differentiation factor secretion in ovarian follicles. Biol Reprod, 1996 August;55(2):416–420.Google Scholar
Huang, CTF, Weitsman, SR, Dykes, BN, Magoffin, DA. Stem cell factor and insulin-like growth factor-I stimulate luteinizing hormone-independent differentiation of rat ovarian theca cells. Biol Reprod, 2001 February 1;64(2):451–456.Google Scholar
Erickson, GF, Magoffin, DA, Dyer, CA, Hofeditz, C. The ovarian androgen producing cells: A review of structure/function relationships. Endocr Rev, 1985 July;6(3):371–399.Google Scholar
Dennis, JE, Charbord, P. Origin and differentiation of human and murine stroma. Stem Cells, 2002 May;20(3):205–214.Google Scholar
Reeves, G. Specific stroma in the cortex and medulla of the ovary. Cell types and vascular supply in relation to follicular apparatus and ovulation. Obstet Gynecol, 1971 June;37(6):832–844.Google Scholar
Orisaka, M, Tajima, K, Mizutani, T et al. Granulosa cells promote differentiation of cortical stromal cells into theca cells in the bovine ovary. Biol Reprod, 2006 November 1;75(5):734–740.Google Scholar
Jabara, S, Christenson, LK, Wang, CY et al. Stromal cells of the human postmenopausal ovary display a distinctive biochemical and molecular phenotype. J Clin Endocrinol Metab, 2003 January;88(1):484–492.Google Scholar
Hummitzsch, K, Irving-Rodgers, HF, Hatzirodos, N et al. A new model of development of the mammalian ovary and follicles. PLoS One, 2013;8(2):e55578.CrossRefGoogle ScholarPubMed
Laronda, MM, Rutz, AL, Xiao, S et al. A bioprosthetic ovary created using 3D printed microporous scaffolds restores ovarian function in sterilized mice. Nat Commun, 2017;8(May):1–10.Google Scholar
Knight, PG, Glister, C. TGF superfamily members and ovarian follicle development. Reproduction, 2006 August 1;132(2):191–206.Google Scholar
Lee, W-S, Yoon, S-J, Yoon, T-K et al. Effects of bone morphogenetic protein-7 (BMP-7) on primordial follicular growth in the mouse ovary. Mol Reprod Dev, 2004 October;69(2):159–163.Google Scholar
Dubreuil, G. Sur l’existence d’une substance inductrice a action limitee et locale pour la metaplasie theca des cellules du stroma cortical ovarien. Ann Endocrinol, 1948;434–442.Google Scholar
Gurava, S. Biology of the Ovarian Follicle. New York: Springer-Verlag, 1985.CrossRefGoogle Scholar
Parrott, JA, Skinner, MK. Kit ligand actions on ovarian stromal cells: Effects on theca cell recruitment and steroid production. Mol Reprod Dev, 2000 January;55(1):55–64.Google Scholar
Nilsson, EE, Skinner, MK. Kit ligand and basic fibroblast growth factor interactions in the induction of ovarian primordial to primary follicle transition. Mol Cell Endocrinol, 2004 February 12;214(1–2):19–25.Google Scholar
Hillier, SG, Miró, F. Inhibin, activin, and follistatin. Potential roles in ovarian physiology. Ann N Y Acad Sci, 1993 May 28(687):29–38.Google Scholar
Hayashi, M, McGee, EA, Min, G et al. Recombinant Growth Differentiation Factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology, 1999 March;140(3):1236–1244.Google Scholar
Lee, WS, Otsuka, F, Moore, RK, Shimasaki, S. Effect of bone morphogenetic protein-7 on folliculogenesis and ovulation in the rat. Biol Reprod, 2001 October;65(4):994–999.Google Scholar
Nilsson, EE, Skinner, MK. Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol Reprod, 2003 May 28;69(4):1265–1272.Google Scholar
Cortvrindt, R, Smitz, J, Van Steirteghem, AC. In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simplified culture system. Hum Reprod, 1996 December;11(12):2656–2666.Google Scholar
Picton, HM, Harris, SE, Muruvi, W, Chambers, EL. The in vitro growth and maturation of follicles. Reproduction, 2008 December 1;136(6):703–715.Google Scholar
West, ER, Zelinski, MB, Kondapalli, LA, et al. Preserving female fertility following cancer treatment: current options and future possibilities. Pediatr Blood Cancer. 2009 August;53(2):289–295.Google Scholar
Eppig, JJ. Mouse oocyte development in vitro with various culture systems. Dev Biol, 1977 October 15;60(2):371–388.Google Scholar
O’Brien, MJ, Pendola, JK, Eppig, JJ. A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol Reprod, 2003 May 1;68(5):1682–1686.Google Scholar
Kreeger, PK, Deck, JW, Woodruff, TK, Shea, LD. The in vitro regulation of ovarian follicle development using alginate-extracellular matrix gels. Biomaterials, 2006 February;27(5):714–723.Google Scholar
Eppig, JJ, Schroeder, AC. Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol Reprod, 1989 Aug;41(2):268–276.Google Scholar
Gomes, JE, Correia, SC, Gouveia-Oliveira, A, Cidadão, AJ, Plancha, CE. Three-dimensional environments preserve extracellular matrix compartments of ovarian follicles and increase FSH-dependent growth. Mol Reprod Dev, 1999 October 1;54(2):163–172.Google Scholar
Cain, L, Chatterjee, S, Collins, TJ. In vitro folliculogenesis of rat preantral follicles. Endocrinology, 1995 August;136(8):3369–3377.Google Scholar
Nayudu, PL, Osborn, SM. Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro. Reproduction, 1992 July 1;95(2):349–362.Google Scholar
Rowghani, NM, Heise, MK, McKeel, D et al. Maintenance of morphology and growth of ovarian follicles in suspension culture. Tissue Eng, 2004 March;10(3–4):545–552.Google Scholar
Boland, NI, Humpherson, PG, Leese, HJ, Gosden, RG. Pattern of lactate production and steroidogenesis during growth and maturation of mouse ovarian follicles in vitro. Biol Reprod, 1993 April 1;48(4):798–806.Google Scholar
Nation, A, Selwood, L. The production of mature oocytes from adult ovaries following primary follicle culture in a marsupial. Reproduction, 2009 August 1;138(2):247–255.Google Scholar
Tibbitt, MW, Anseth, KS. Hydrogels as extracellular matrix mimics for 3D cell culture. Biotechnol Bioeng, 2009 July 1;103(4):655–663.Google Scholar
Petersen, OW, Rønnov-Jessen, L, Howlett, AR, Bissell, MJ. Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc Natl Acad Sci U S A, 1992 October 1;89(19):9064–9068.Google Scholar
Weaver, VM, Fischer, AH, Peterson, OW, Bissell, MJ. The importance of the microenvironment in breast cancer progression: recapitulation of mammary tumorigenesis using a unique human mammary epithelial cell model and a three-dimensional culture assay. Biochem Cell Biol, 1996;74(6):833–851.Google Scholar
Tanaka, H, Murphy, CL, Murphy, C et al. Chondrogenic differentiation of murine embryonic stem cells: Effects of culture conditions and dexamethasone. J Cell Biochem, 2004 October 15;93(3):454–462.Google Scholar
Engler, AJ, Sen, S, Sweeney, HL, Discher, DE. Matrix elasticity directs stem cell lineage specification. Cell, 2006 August 25;126(4):677–689.Google Scholar
Joo, S, Oh, SH, Sittadjody, S et al. The effect of collagen hydrogel on 3D culture of ovarian follicles. Biomed Mater, 2016 November 11;11(6):65009.Google Scholar
Xu, J, Lawson, MS, Yeoman, RR et al. Fibrin promotes development and function of macaque primary follicles during encapsulated three-dimensional culture. Hum Reprod, 2013 August 1;28(8):2187–2200.Google Scholar
Desai, N, Abdelhafez, F, Calabro, A, Falcone, T. Three dimensional culture of fresh and vitrified mouse pre-antral follicles in a hyaluronan-based hydrogel: a preliminary investigation of a novel biomaterial for in vitro follicle maturation. Reprod Biol Endocrinol, 2012 June 13;10(1):29.Google Scholar
Shikanov, A, Smith, RM, Xu, M, Woodruff, TK, Shea, LD. Hydrogel network design using multifunctional macromers to coordinate tissue maturation in ovarian follicle culture. Biomaterials, 2011;32(10):2524–2531.Google Scholar
Abir, R, Roizman, P, Fisch, B et al. Pilot study of isolated early human follicles cultured in collagen gels for 24 hours. Hum Reprod, 1999;14(5):1299–1301.CrossRefGoogle ScholarPubMed
Torrance, C, Telfer, E, Gosden, RG. Quantitative study of the development of isolated mouse pre-antral follicles in collagen gel culture. J Reprod Fertil, 1989 September 1;87(1):367–374.Google Scholar
Sharma, GT, Dubey, PK, Meur, SK. Survival and developmental competence of buffalo preantral follicles using three-dimensional collagen gel culture system. Anim Reprod Sci, 2009 August 1;114(1–3):115–124.Google Scholar
Carroll, J, Whittingham, DG, Wood, MJ. Effect of gonadotrophin environment on growth and development of isolated mouse primary ovarian follicles. J Reprod Fertil, 1991 September;93(1):71–79.Google Scholar
Hirao, Y, Nagai, T, Kubo, M et al. In vitro growth and maturation of pig oocytes. J Reprod Fertil, 1994 March;100(2):333–339.Google Scholar
Rodgers, RJ, Irving-Rodgers, HF, Russell, DL. Extracellular matrix of the developing ovarian follicle. Reproduction, 2003 October;126(4):415–424.Google Scholar
Pangas, Sa, Saudye, H, Shea, LD, Woodruff, TK. Novel approach for the three-dimensional culture of granulosa cell-oocyte complexes. Tissue Eng, 2003;9(5):1013–1021.Google Scholar
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 December 1;75(September):916–923.Google Scholar
Erin, R, West Teresa, K, Woodruff, et al. Physical properties of alginate hydrogels and their effects on in vitro follicle development. Biomaterials, 2007;28(30):4439–4448.Google Scholar
Xu, M, West-Farrell, ER, Stouffer, RL et al. Encapsulated three-dimensional culture supports development of nonhuman primate secondary follicles. Biol Reprod, 2009 September 1;81(3):587–594.Google Scholar
Xu, M, Barrett, SL, West-Farrell, E et al. In vitro grown human ovarian follicles from cancer patients support oocyte growth. Hum Reprod, 2009 October 1;24(10):2531–2540.Google Scholar
Xu, M, Kreeger, PK, Shea, LD, Woodruff, TK. Tissue-engineered follicles produce live, fertile offspring. Tissue Eng, 2006 October;12(10):2739–2746.Google Scholar
Shikanov, A, Xu, M, Woodruff, TK, Shea, LD. Interpenetrating fibrin–alginate matrices for in vitro ovarian follicle development. Biomaterials, 2009 October;30(29):5476–5485.Google Scholar
Augst, AD, Kong, HJ, Mooney, DJ. Alginate hydrogels as biomaterials. Macromol Biosci, 2006 August 7;6(8):623–633.Google Scholar
Rowley, JA, Madlambayan, G, Mooney, DJ. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials, 1999 January;20(1):45–53.Google Scholar
Skory, RM, Xu, Y, Shea, LD, Woodruff, TK. Engineering the ovarian cycle using in vitro follicle culture. Hum Reprod, 2015;30(6):1386–1395.Google Scholar
Silva, GM, Rossetto, R, Chaves, RN et al. In vitro development of secondary follicles from pre-pubertal and adult goats cultured in two-dimensional or three-dimensional systems. Zygote, 2015 August 26;23(4):475–484.Google Scholar
Sadeghnia, S, Akhondi, MM, Hossein, G et al. Development of sheep primordial follicles encapsulated in alginate or in ovarian tissue in fresh and vitrified samples. Cryobiology, 2016 April 1;72(2):100–105.Google Scholar
Songsasen, N, Woodruff, TK, Wildt, DE. In vitro growth and steroidogenesis of dog follicles are influenced by the physical and hormonal microenvironment. Reproduction, 2011 July;142(1):113–122.Google Scholar
Jin, SY, Lei, L, Shikanov, A, Shea, LD, Woodruff, TK. A novel two-step strategy for in vitro culture of early-stage ovarian follicles in the mouse. Fertil Steril, 2010 May 15;93(8):2633–2639.Google Scholar
Amorim, CA, Van Langendonckt, A, David, A, Dolmans, M-M, Donnez, J. Survival of human pre-antral follicles after cryopreservation of ovarian tissue, follicular isolation and in vitro culture in a calcium alginate matrix. Hum Reprod, 2008 October 14;24(1):92–99.Google Scholar
Osborn, SM, Gook, DA, Stern, K, Speirs, AL. The isolation and culture of human primordial follicles from fresh ovarian tissue. Hum Reprod, 1997 June 1;12(Suppl 2):192–193.Google Scholar
Itoh, T, Hoshi, H. Efficient isolation and long-term viability of bovine small preantral follicles in vitro. Vitr Cell Dev Biol – Anim, 2000 April;36(4):235.Google Scholar
Wu, MF, Huang, WT, Tsay, C et al. The stage-dependent inhibitory effect of porcine follicular cells on the development of preantral follicles. Anim Reprod Sci, 2002;73(1–2):73–88.Google Scholar
Ramesh, HS, Gupta, PSP, Nandi, S et al. Co-culture of buffalo large preantral follicles with ovarian somatic cells. Adv Biol Res (Rennes), 2007;1(2):29–33.Google Scholar
Laronda, MM, Jakus, AE, Whelan, KA et al. Initiation of puberty in mice following decellularized ovary transplant. Biomaterials, 2015;50:20–29.Google Scholar
Scarrit, ME, Pashos, NC, Bunnell, BA. A review of cellularization strategies for tissue engineering of whole organs. Front Bioeng Biotechnol, 2015;3:43.Google Scholar
Atala, A, Bauer, SB, Soker, S, Yoo, JJ, Retik, AB. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet (London, England), 2006 April 15;367(9518):1241–1246.Google Scholar
Hendriks, J, Riesle, J, van Blitterswijk, CA. Co-culture in cartilage tissue engineering. J Tissue Eng Regen Med, 2007 May;1(3):170–178.Google Scholar
Soto-Gutiérrez, A, Navarro-Álvarez, N, Zhao, D et al. Differentiation of mouse embryonic stem cells to hepatocyte-like cells by co-culture with human liver nonparenchymal cell lines. Nat Protoc, 2007 February 1;2(2):347–356.Google Scholar
Harimoto, M, Yamato, M, Hirose, M et al. Novel approach for achieving double-layered cell sheets co-culture: overlaying endothelial cell sheets onto monolayer hepatocytes utilizing temperature-responsive culture dishes. J Biomed Mater Res, 2002 December 5;62(3):464–470.Google Scholar
Robinson, SN, Ng, J, Niu, T et al. Superior ex vivo cord blood expansion following co-culture with bone marrow-derived mesenchymal stem cells. Bone Marrow Transplant, 2006 February 9;37(4):359–366.Google Scholar
Luk, JM, Wang, PP, Lee, CK, Wang, JH, Fan, ST. Hepatic potential of bone marrow stromal cells: Development of in vitro co-culture and intra-portal transplantation models. J Immunol Methods, 2005 October 20;305(1):39–47.Google Scholar
Houchin-Ray, T, Zelivyanskaya, M, Huang, A, Shea, LD. Non-viral gene delivery transfection profiles influence neuronal architecture in an in vitro co-culture model. Biotechnol Bioeng, 2009 August 1;103(5):1023–1033.Google Scholar
Dominguez, F, Gadea, B, Mercader, A et al. Embryologic outcome and secretome profile of implanted blastocysts obtained after coculture in human endometrial epithelial cells versus the sequential system. Fertil Steril, 2010 February;93(3):774–782.e1.Google Scholar
Godard, NM, Pukazhenthi, BS, Wildt, DE, Comizzoli, P. Paracrine factors from cumulus-enclosed oocytes ensure the successful maturation and fertilization in vitro of denuded oocytes in the cat model. Fertil Steril, 2009 May;91(5):2051–2060.Google Scholar
Reubinoff, BE, Pera, MF, Fong, C-Y, Trounson, A, Bongso, A. Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol, 2000 April 1;18(4):399–404.Google Scholar
Thomson, JA, Itskovitz-Eldor, J, Shapiro, SS et al. Embryonic stem cell lines derived from human blastocysts. Science, 1998 November 6;282(5391):1145–1147.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×