Abstract
In vitro culture of ovarian follicles isolated or enclosed in ovarian tissue fragments and grafting of isolated ovarian follicles represent a potential alternative to restore fertility in cancer patients who cannot undergo cryopreservation of embryos or oocytes or transplantation of frozen-thawed ovarian tissue. In this regard, respecting the three-dimensional (3D) architecture of isolated follicles is crucial to maintaining their proper follicular physiology. To this end, alginate hydrogel has been widely investigated using follicles from numerous animal species, yielding promising results. The goal of this review is therefore to provide an overview of alginate applications utilizing the biomaterial as a scaffold for 3D encapsulation of isolated ovarian follicles. Different methods of isolated follicle encapsulation in alginate are discussed in this review, as its use of 3D alginate culture systems as a tool for in vitro follicle analysis. Possible improvements of this matrix, namely modification with arginine-glycine-aspartic acid peptide or combination with fibrin, are also summarized. Encouraging results have been obtained in different animal models, and particularly with isolated follicles encapsulated in alginate matrices and grafted to mice. This summary is designed to guide the reader towards development of next-generation alginate scaffolds, with enhanced properties for follicle encapsulation.
Similar content being viewed by others
Abbreviations
- 2D:
-
Two-dimensional
- 3D:
-
Three-dimensional
- AMH:
-
Anti-Müllerian hormone
- ANGPT-1:
-
Angiopoietin-1
- ANGPT-2:
-
Angiopoietin-2
- boECM:
-
Bovine decellularized ovarian extracellular matrix
- ECM:
-
Extracellular matrix
- FSH:
-
Follicle-stimulating hormone
- GC:
-
Granulosa cell
- LH:
-
Luteinizing hormone
- MEF:
-
Mouse embryonic fibroblast
- RGD:
-
Arginine-glycine-aspartic acid
- VEGF:
-
Vascular endothelial growth factor
References
Abir, R., S. Franks, M. A. Mobberley, P. A. Moore, R. A. Margara, and R. M. Winston. Mechanical isolation and in vitro growth of preantral and small antral human follicles. Fertil. Steril. 68:682–688, 1997.
Agarwal, P., J. K. Choi, H. Huang, S. Zhao, J. Dumbleton, J. Li, and X. He. A biomimetic core-shell platform for miniaturized 3D cell and tissue engineering. Part. Part. Syst. Charact. 32:809–816, 2015.
Al-Shamkhani, A., and R. Duncan. Radioiodination of alginate via covalently-bound tyrosinamide allows monitoring of its fate in vivo. J. Bioact. Compat. Polym. 10:4–13, 1995.
Amorim, C. A. Artificial ovary. In: Gonadal Tissue Cryopreservation in Fertility, edited by N. Suzuki, and J. Donnez. New York: Springer, 2016, pp. 175–192.
Amorim, C. A., D. Rondina, C. M. Lucci, A. Giorgetti, J. R. de Figueiredo, and P. B. Goncalves. Cryopreservation of sheep primordial follicles. Reprod. Domest. Anim. 42:53–57, 2007.
Amorim, C. A., and A. Shikanov. The artificial ovary: current status and future perspectives. Future Oncol. 12:2323–2332, 2016.
Amorim, C. A., A. Van Langendonckt, A. David, M. M. Dolmans, and J. Donnez. Survival of human pre-antral follicles after cryopreservation of ovarian tissue, follicular isolation and in vitro culture in a calcium alginate matrix. Hum. Reprod. 24:92–99, 2009.
Andersen, T., P. Auk-Emblem, and M. Dornish. 3D cell culture in alginate hydrogels. Microarrays (Basel) 4:133–161, 2015.
Andersen, T., C. Markussen, M. Dornish, H. Heier-Baardson, J. E. Melvik, E. Alsberg, and B. E. Christensen. In situ gelation for cell immobilization and culture in alginate foam scaffolds. Tissue Eng. A 20:600–610, 2014.
Andreu, N., D. Thomas, L. Saraiva, N. Ward, K. Gustafsson, S. N. Jayasinghe, and B. D. Robertson. In vitro and in vivo interrogation of bio-sprayed cells. Small 8:2495–2500, 2012.
Araújo, V. R., M. O. Gastal, A. Wischral, J. R. Figueiredo, and E. R. Gastal. In vitro development of bovine secondary follicles in two- and three-dimensional culture systems using vascular endothelial growth factor, insulin-like growth factor-1, and growth hormone. Theriogenology 82:1246–1253, 2014.
Asgari, F., M. R. Valojerdi, B. Ebrahimi, and R. Fatehi. Three dimensional in vitro culture of preantral follicles following slow-freezing and vitrification of mouse ovarian tissue. Cryobiology 71:529–536, 2015.
Barrett, S. L., L. D. Shea, and T. K. Woodruff. Noninvasive index of cryorecovery and growth potential for human follicles in vitro. Biol. Reprod. 82:1180–1189, 2010.
Bhakta, G., K. H. Lee, R. Magalhães, F. Wen, S. S. Gouk, D. W. Hutmacher, and L. L. Kuleshova. Cryopreservation of alginate-fibrin beads involving bone marrow derived mesenchymal stromal cells by vitrification. Biomaterials 30:336–343, 2009.
Bian, J., T. Li, C. Ding, W. Xin, B. Zhu, and C. Zhou. Vitreous cryopreservation of human preantral follicles encapsulated in alginate beads with mini mesh cups. J. Reprod. Dev. 59:288–295, 2013.
Bible, E., F. Dell’Acqua, B. Solanky, A. Balducci, P. M. Crapo, S. F. Badylak, E. T. Ahrens, and M. Modo. Non-invasive imaging of transplanted human neural stem cells and ECM scaffold remodeling in the stroke-damaged rat brain by (19)F- and diffusion-MRI. Biomaterials 33:2858–2871, 2012.
Bidarra, S. J., C. C. Barrias, K. B. Fonseca, M. A. Barbosa, R. A. Soares, and P. L. Granja. Injectable in situ crosslinkable RGD-modified alginate matrix for endothelial cells delivery. Biomaterials 32:7897–7904, 2011.
Brito, I. R., C. M. Silva, A. B. Duarte, I. M. Lima, G. Q. Rodrigues, R. Rossetto, A. D. Sales, C. H. Lobo, M. P. Bernuci, A. C. Rosa-E-Silva, C. C. Campello, M. Xu, and J. R. Figueiredo. Alginate hydrogel matrix stiffness influences the in vitro development of caprine preantral follicles. Mol. Reprod. Dev. 81:636–645, 2014.
Brito, I. R., G. M. Silva, A. D. Sales, C. H. Lobo, G. Q. Rodrigues, R. F. Sousa, A. Moura, C. Calderón, M. Bertolini, C. C. Campello, J. Smitz, and J. R. Figueiredo. Fibrin-alginate hydrogel supports steroidogenesis, in vitro maturation of oocytes and parthenotes production from caprine preantral follicles cultured in group. Reprod. Domest. Anim. 51:997–1009, 2016.
Butcher, L., and S. L. Ullmann. Culture of preantral ovarian follicles in the grey, short-tailed opossum, Monodelphis domestica. Reprod. Fertil. Dev. 8:535–539, 1996.
Camboni, A., A. Van Langendonckt, J. Donnez, J. Vanacker, M. M. Dolmans, and C. A. Amorim. Alginate beads as a tool to handle, cryopreserve and culture isolated human primordial/primary follicles. Cryobiology 67:64–69, 2013.
Chiti, C., A. Viswanath, J. Vanacker, L. Germain, L. J. White, M. M. Dolmans, A. Des Rieux and C. A. Amorim. Hydrogel from bovine decellularized ovarian extracellular matrix supports mouse follicle survival in vitro. Front. Bioeng. Biotechnol. Conference Abstract: 10th World Biomaterials Congress. doi: 10.3389/conf.FBIOE.2016.01.00014.
Choi, J. K., P. Agarwal, H. Huang, S. Zhao, and X. He. The crucial role of mechanical heterogeneity in regulating follicle development and ovulation with engineered ovarian microtissue. Biomaterials 35:5122–5128, 2014.
Cortvrindt, R. G., and J. E. Smitz. Follicle culture in reproductive toxicology: a tool for in vitro testing of ovarian function? Hum. Reprod. Update 8:243–254, 2002.
Crapo, P. M., S. Tottey, P. F. Slivka, and S. F. Badylak. Effects of biologic scaffolds on human stem cells and implications for CNS tissue engineering. Tissue Eng. A 20:313–323, 2014.
Dalheim, M. Ø., J. Vanacker, M. A. Najmi, F. L. Aachmann, B. L. Strand, and B. E. Christensen. Efficient functionalization of alginate biomaterials. Biomaterials 80:146–156, 2016.
Desai, N., F. Abdelhafez, A. Calabro, and T. Falcone. 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. 10:29, 2012.
Desai, B. J., H. E. Gruber, and E. N. Hanley, Jr. The influence of Matrigel or growth factor reduced Matrigel on human intervertebral disc cell growth and proliferation. Histol. Histopathol. 14:359–368, 1999.
Dhoot, N. O., C. A. Tobias, I. Fischer, and M. A. Wheatley. Peptide-modified alginate surfaces as a growth permissive substrate for neurite outgrowth. J. Biomed. Mater. Res. A. 71:191–200, 2004.
Donati, I., Y. A. Mørch, B. L. Strand, G. Skjåk-Braek, and S. Paoletti. Effect of elongation of alternating sequences on swelling behavior and large deformation properties of natural alginate gels. J. Phys. Chem. B. 113:12916–12922, 2009.
Dong, F. L., L. Ma, S. L. Shi, S. J. Dai, X. G. Liu, Y. C. Su, Y. H. Guo, F. Wang, and Y. P. Sun. An research on the isolation methods of frozen-thawed human ovarian preantral follicles. Int. J. Clin. Exp. Med. 7:2298–2303, 2014.
Donnez, J., and M. M. Dolmans. Fertility preservation in women. Nat. Rev. Endocrinol. 9:735–749, 2013.
Draget, K. I., G. Skjåk Bræk, and O. Smidsrød. Alginic acid gels: the effect of alginate chemical composition and molecular weight. Carbohydr. Polym. 25:31–38, 1994.
Drury, J. L., and D. J. Mooney. Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24:4337–4351, 2003.
Eppig, J. J., and M. J. O’Brien. Development in vitro of mouse oocytes from primordial follicles. Biol. Reprod. 54:197–207, 1996.
Evron, A., Z. Blumenfeld, and E. Y. Adashi. The role of growth factors in ovarian function and development. Glob. Libr. Women’s Med., (ISSN: 1756-2228) 2015; DOI 10.3843/GLOWM.10288.
Filicori, M. The role of luteinizing hormone in folliculogenesis and ovulation induction. Fertil. Steril. 71:405–414, 1999.
Fisher, T. E., T. A. Molskness, A. Villeda, M. B. Zelinski, R. L. Stouffer, and J. Xu. Vascular endothelial growth factor and angiopoietin production by primate follicles during culture is a function of growth rate, gonadotrophin exposure and oxygen milieu. Hum. Reprod. 28:3263–3270, 2013.
Fonseca, K. B., S. J. Bidarra, M. J. Oliveira, P. L. Granja, and C. C. Barrias. Molecularly designed alginate hydrogels susceptible to local proteolysis as three-dimensional cellular microenvironments. Acta Biomater. 7:1674–1682, 2011.
Formo, K., C. H. Cho, L. Vallier, and B. L. Strand. Culture of hESC-derived pancreatic progenitors in alginate-based scaffolds. J. Biomed. Mater. Res. A 103:3717–3726, 2015.
Gigli, I., D. D. Byrd, and J. E. Fortune. Effects of oxygen tension and supplements to the culture medium on activation and development of bovine follicles in vitro. Theriogenology 66:344–353, 2006.
Gupta, P. S. P., H. S. Ramesh, B. M. Manjunatha, S. Nandi, and J. P. Ravindra. Production of buffalo embryos using oocytes from in vitro grown preantral follicles. Zygote 16:57–63, 2008.
Gutierrez, C. G., J. H. Ralph, E. E. Telfer, I. Wilmut, and R. Webb. Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biol. Reprod. 62:1322–1328, 2000.
Harris, S. E., H. J. Leese, R. G. Gosden, and H. M. Picton. Pyruvate and oxygen consumption throughout the growth and development of murine oocytes. Mol. Reprod. Dev. 76:231–238, 2009.
Haug, A., and B. Larsen. Quantitative determination of the uronic acid composition of alginates. Acta Chem. Scand. 16:1908–1918, 1962.
Haug, A., B. Larsen, and O. Smidsrod. Studies of the sequence of uronic acid residues in alginic acid. Acta Chem. Scand. 21:691–704, 1967.
Haug, A., and O. Smidsrod. Strontium-calcium selectivity of alginates. Nature 215:757, 1967.
Heise, M., R. Koepsel, A. J. Russell, and E. A. McGee. Calcium alginate microencapsulation of ovarian follicles impacts FSH delivery and follicle morphology. Reprod. Biol. Endocrinol. 3:47, 2005.
Hemamalini, N. C., B. S. Rao, G. Tamilmani, D. Amarnath, R. Vagdevi, K. S. Naidu, K. K. Reddy, and V. H. Rao. Influence of transforming growth factor-α, insulin-like growth factor-II, epidermal growth factor or follicle stimulating hormone on in vitro development of preantral follicles in sheep. Small Rumin. Res. 50:11–22, 2003.
Hirao, Y., T. Nagai, M. Kubo, T. Miyano, M. Miyake, and S. Kato. In vitro growth and maturation of pig oocytes. J. Reprod. Fertil. 100:333–339, 1994.
Hornick, J. E., F. E. Duncan, L. D. Shea, and T. K. Woodruff. Isolated primate primordial follicles require a rigid physical environment to survive and grow in vitro. Hum. Reprod. 27:1801–1810, 2012.
Hornick, J. E., F. E. Duncan, L. D. Shea, and T. K. Woodruff. Multiple follicle culture supports primary follicle growth through paracrine-acting signals. Reproduction 145:19–32, 2013.
Irving-Rodgers, H. F., and R. J. Rodgers. Extracellular matrix of the developing ovarian follicle. Semin. Reprod. Med. 24:195–203, 2006.
Itoh, T., M. Kacchi, H. Abe, Y. Sendai, and H. Hoshi. Growth, antrum formation, and estradiol production of bovine preantral follicles cultured in a serum-free medium. Biol. Reprod. 67:1099–1105, 2002.
Jayasinghe, S. N. Cell electrospinning: a novel tool for functionalising fibres, scaffolds and membranes with living cells and other advanced materials for regenerative biology and medicine. Analyst 138:2215–2223, 2013.
Jewgenow, K. Impact of peptide growth factors on the culture of preantral follicles of domestic cats. Theriogenology 45:889–895, 1998.
Ji, L., J. J. de Pablo, and S. P. Palecek. Cryopreservation of adherent human embryonic stem cells. Biotechnol. Bioeng. 88:299–312, 2004.
Jiao, Z. X., and T. K. Woodruff. Follicle microenvironment-associated alterations in gene expression in the mouse oocyte and its polar body. Fertil. Steril. 99:1453–1459, 2013.
Jin, S. Y., L. Lei, A. Shikanov, L. D. Shea, and T. K. Woodruff. A novel two-step strategy for in vitro culture of early-stage ovarian follicles in the mouse. Fertil. Steril. 93:2633–2639, 2010.
Kreeger, P. K., J. W. Deck, T. K. Woodruff, and L. D. Shea. The in vitro regulation of ovarian follicle development using alginate-extracellular matrix gels. Biomaterials 27:714–723, 2006.
Kreeger, P. K., N. N. Fernandes, T. K. Woodruff, and L. D. Shea. Regulation of mouse follicle development by follicle-stimulating hormone in a three-dimensional in vitro culture system is dependent on follicle stage and dose. Biol. Reprod. 73:942–950, 2005.
Kreeger, P. K., T. K. Woodruff, and L. D. Shea. Murine granulosa cell morphology and function are regulated by a synthetic Arg-Gly-Asp matrix. Mol. Cell Endocrinol. 205:1–10, 2003.
Laronda, M. M., F. E. Duncan, J. E. Hornick, M. Xu, J. E. Pahnke, K. A. Whelan, L. D. Shea, and T. K. Woodruff. Alginate encapsulation supports the growth and differentiation of human primordial follicles within ovarian cortical tissue. J. Assist. Reprod. Genet. 31:1013–1028, 2014.
Lee, K. Y., and D. J. Mooney. Hydrogels for tissue engineering. Chem. Rev. 101:1869–1879, 2001.
Lenie, S., R. Cortvrindt, U. Eichenlaub-Ritter, and J. Smitz. Continuous exposure to bisphenol A during in vitro follicular development induces meiotic abnormalities. Mutat. Res. 651:71–81, 2008.
Mainigi, M. A., T. Ord, and R. M. Schultz. Meiotic and developmental competence in mice are compromised following follicle development in vitro using an alginate-based culture system. Biol. Reprod. 85:269–276, 2011.
Makanji, Y., D. Tagler, J. Pahnke, L. D. Shea, and T. K. Woodruff. Hypoxia-mediated carbohydrate metabolism and transport promote early-stage murine follicle growth and survival. Am. J. Physiol. Endocrinol. Metab. 306:893–903, 2014.
Merz, C., S. Saller, L. Kunz, J. Xu, R. R. Yeoman, A. Y. Ting, M. S. Lawson, R. L. Stouffer, J. D. Hennebold, F. Pau, G. A. Dissen, S. R. Ojeda, M. B. Zelinski, and A. Mayerhofer. Expression of the beta-2 adrenergic receptor (ADRB-2) in human and monkey ovarian follicles: a marker of growing follicles? J. Ovarian Res. 7:8, 2015.
Nagashima, J., D. E. Wildt, A. J. Travis, and N. Songsasen. Follicular size and stage and gonadotropin concentration affect alginate-encapsulated in vitro growth and survival of pre- and early antral dog follicles. Reprod. Fertil. Dev. 2015. doi:10.1071/RD15004.
Ouwerx, C., N. Velings, M. M. Mestdagh, and M. A. V. Axelos. Physico-chemical properties and rheology of alginate gel beads formed with various divalent cations. Polym. Gel Netw. 6:393–408, 1998.
Pangas, S. A., H. Saudye, L. D. Shea, and T. K. Woodruff. Novel approach for the three-dimensional culture of granulosa cell-oocyte complexes. Tissue Eng. 9:1013–1021, 2003.
Park, K. E., Y. Y. Kim, S. Y. Ku, S. M. Baek, Y. Huh, Y. J. Kim, S. H. Kim, Y. M. Choi, and S. Y. Moon. Effects of alginate hydrogels on in vitro maturation outcome of mouse preantral follicles. Tissue Eng. Regen. Med. 9:170–174, 2012.
Peretz, J., Z. R. Craig, and J. A. Flaws. Bisphenol A inhibits follicle growth and induces atresia in cultured mouse antral follicles independently of the genomic estrogenic pathway. Biol. Reprod. 87:63, 2012.
Pessoa, A. F. C., R. M. P. Rocha, I. R. Brito, G. M. Silva, R. N. Chaves, D. M. Magalhães-Padilha, C. C. Campello, A. P. R. Rodrigues, D. C. S. Nunes-Pinheiro, and J. R. Figueiredo. Effect of morphological integrity, period, and type of culture system on the in vitro development of isolated caprine preantral follicles. Theriogenology 82:312–317, 2014.
Picton, H. M., and R. G. Gosden. In vitro growth of human primordial follicles from frozen-banked ovarian tissue. Mol. Cell. Endocrinol. 166:27–35, 2000.
Rodrigues, J. K., P. A. Navarro, M. B. Zelinski, R. L. Stouffer, and J. Xu. Direct actions of androgens on the survival, growth and secretion of steroids and anti-Müllerian hormone by individual macaque follicles during three-dimensional culture. Hum. Reprod. 30:664–674, 2015.
Rossetto, R., M. V. A. Saraiva, M. P. Bernuci, G. M. Silva, I. R. Brito, A. M. C. V. Alves, D. M. Magalhães-Padilha, S. N. Báo, C. C. Campello, A. P. R. Rodrigues, and J. R. Figueiredo. Impact of insulin concentration and mode of FSH addition on the in vitro survival and development of isolated bovine preantral follicles. Theriogenology 86:1137–1145, 2016.
Rowley, J. A., G. Madlambayan, and D. J. Mooney. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials 20:45–53, 1999.
Rowley, J. A., and D. J. Mooney. Alginate type and RGD density control myoblast phenotype. J. Biomed. Mater. Res. 60:217–223, 2002.
Roy, S. K., and G. S. Greenwald. Methods of separation and in vitro culture of pre-antral follicles from mammalian ovaries. Hum. Reprod. Update 2:236–245, 1996.
Roy, S. K., and G. S. Greenwald. In vitro effects of follicle-stimulating hormone, luteinizing hormone and prolactine on follicular deoxyribonucleic acid synthesis in the hamster. Endocrinology 122:952–958, 1998.
Roy, S. K., and B. J. Treacy. Isolation and long-term culture of human preantral follicles. Fertil. Steril. 59:783–790, 1993.
Ruoslahti, E. RGD and other recognition sequences for integrins. Annu. Rev. Cell Dev. Biol. 12:697–715, 1996.
Sadeghnia, S., M. M. Akhondi, G. Hossein, S. Mobini, L. Hosseini, M. M. Naderi, S. B. Boroujeni, A. Sarvari, B. Behzadi, and A. Shirazi. Development of sheep primordial follicles encapsulated in alginate or in ovarian tissue in fresh and vitrified samples. Cryobiology 72:100–105, 2016.
Sadr, S. Z., B. Ebrahimi, M. Shahhoseini, R. Fatehi, and R. Favaedi. Mouse preantral follicle development in two-dimensional and three-dimensional culture systems after ovarian tissue vitrification. Eur. J. Obstet. Gynecol. Reprod. Biol. 194:206–211, 2015.
Sandvig, I., K. Karstensen, A. M. Rokstad, F. L. Aachmann, K. Formo, A. Sandvig, G. Skjåk-Bræk, and B. L. Strand. RGD-peptide modified alginate by a chemoenzymatic strategy for tissue engineering applications. J. Biomed. Mater. Res. A. 103:896–906, 2015.
Serra, M., C. Correia, R. Malpique, C. Brito, J. Jensen, P. Bjorquist, M. J. Carrondo, and P. M. Alves. Microencapsulation technology: a powerful tool for integrating expansion and cryopreservation of human embryonic stem cells. PLoS ONE 6:e23212, 2011.
Sharma, G. T., P. K. Dubey, and S. K. Meur. Survival and developmental competence of buffalo preantral follicles using three-dimensional collagen gel culture system. Anim. Reprod. Sci. 114:115–124, 2009.
Shaw, J. M., S. L. Cox, A. O. Trounson, and G. Jenkin. Evaluation of the long-term function of cryopreserved ovarian grafts in the mouse, implications for human applications. Mol. Cell. Endocrinol. 161:103–110, 2000.
Shikanov, A., M. Xu, T. K. Woodruff and L. D. Shea. A method for ovarian follicle encapsulation and culture in a proteolytically degradable 3 dimensional system. J. Vis. Exp. 49, 2011.
Shikanov, A., M. Xu, T. K. Woodruff, and L. D. Shea. Interpenetrating fibrin-alginate matrices for in vitro ovarian follicle development. Biomaterials 30:5476–5485, 2009.
Silva, G. M., R. Rossetto, R. N. Chaves, A. B. G. Duarte, V. R. Araújo, C. Feltrin, M. P. Bernuci, J. A. Anselmo-Franci, M. Xu, T. K. Woodruff, C. C. Campello, and J. R. Figueiredo. In vitro development of secondary follicles from pre-pubertal and adult goats cultured in two-dimensional or three-dimensional systems. Zygote 23:475–484, 2015.
Singelyn, J. M., P. Sundaramurthy, T. D. Johnson, P. J. Schup-Magoffin, D. P. Hu, D. M. Faulk, J. Wang, K. M. Mayle, K. Bartels, M. Salvatore, A. M. Kinsey, A. N. Demaria, N. Dib, and K. L. Christman. Catheter-deliverable hydrogel derived from decellularized ventricular extracellular matrix increases endogenous cardiomyocytes and preserves cardiac function post-myocardial infarction. J. Am. Coll. Cardiol. 59:751–763, 2012.
Skory, R. M., Y. Xu, L. D. Shea, and T. K. Woodruff. Engineering the ovarain cylce unsing in vitro follicle culture. Hum. Reprod. 30:1386–1395, 2015.
Songsasen, N., P. Comizzoli, J. Nagashima, M. Fujihara, and D. E. Wildt. The domestic dog and cat as models for understanding the regulation of ovarian follicle development in vitro. Reprod. Domest. Anim. 47:13–18, 2012.
Songsasen, N., C. Guzy, and D. E. Wildt. Alginate-fibrin gel matrix promotes in vitro growth of dog secondary follicles. Reprod. Fertil. Dev. 24:173, 2011.
Songsasen, N., T. K. Woodruff, and D. E. Wildt. In vitro growth and steroidogenesis of dog follicles as influenced by the physical and hormonal microenvironment. Reproduction 142:113–122, 2011.
Sun, J., and X. Li. Growth and antrum formation of bovine primary follicles in long-term culture in vitro. Reprod. Biol. 13:221–228, 2013.
Tagler, D., Y. Makanji, N. R. Anderson, T. K. Woodruff, and L. D. Shea. Supplemented αMEM/F12-based medium enables the survival and growth of primary ovarian follicles encapsulated in alginate hydrogels. Biotechnol. Bioeng. 110:3258–3268, 2012.
Tagler, D., Y. Makanji, T. Tu, B. P. Bernabé, R. Lee, J. Zhu, E. Kniazeva, J. E. Hornick, T. K. Woodruff, and L. D. Shea. Promoting extracellular matrix remodeling via ascorbic acid enhances the survival of primary ovarian follicles encapsulated in alginate hydrogels. Biotechnol. Bioeng. 111:1417–1429, 2014.
Tagler, D., T. Tu, R. M. Smith, N. R. Anderson, C. M. Tingen, T. K. Woodruff, and L. D. Shea. Embryonic fibroblasts enable the culture of primary ovarian follicles within alginate hydrogels. Tissue Eng. A 18:1229–1238, 2012.
Tambe, S. S., and T. D. Nandedkar. Steroidogenesis in sheep ovarian antral follicles in culture: time course study and supplementation with a precursor. Steroids 58:379–383, 1993.
Telfer, E. E., and M. B. Zelinski. Ovarian Follicle Culture: Advances and Challenges for Human and Non-human Primates. Fertil. Steril. 99:1523–1533, 2013.
Ting, A. Y., J. Xu, and R. L. Stouffer. Differential effects of estrogen and progesterone on development of primate secondary follicles in a steroid-depleted milieu in vitro. Hum. Reprod. 30:1907–1917, 2015.
Ting, A. Y., R. R. Yeoman, J. R. Campos, M. S. Lawson, S. F. Mullen, G. M. Fahy, and M. B. Zelinski. Morphological and functional preservation of pre-antral follicles after vitrification of macaque ovarian tissue in a closed system. Hum. Reprod. 28:1267–1279, 2013.
Ting, A. Y., R. R. Yeoman, M. S. Lawson, and M. B. Zelinski. In vitro development of secondary follicles from cryopreserved rhesus macaque ovarian tissue after slow-rate freeze or vitrification. Hum. Reprod. 26:2461–2472, 2011.
Ting, A. Y., R. R. Yeoman, M. S. Lawson, and M. B. Zelinski. Synthetic polymers improve vitrification outcomes of macaque ovarian tissue as assessed by histological integrity and the in vitro development of secondary follicles. Cryobiology 65:1–11, 2012.
Tingen, C. M., S. E. Kiesewetter, J. Jozefik, C. Thomas, D. Tagler, L. Shea, and T. K. Woodruff. A macrophage and theca cell-enriched stromal cell population influences growth and survival of immature murine follicles in vitro. Reproduction 141:809–820, 2011.
Townsend-Nicholson, A., and S. N. Jayasinghe. Cell electrospinning: a unique biotechnique for encapsulating living organisms for generating active biological microthreads/scaffolds. Biomacromolecules 7:3364–3369, 2006.
Vanacker, J., A. Camboni, C. Dath, A. Van Langendonckt, M. M. Dolmans, J. Donnez, and C. A. Amorim. Enzymatic isolation of human primordial and primary ovarian follicles with Liberase DH: protocol for application in a clinical setting. Fertil. Steril. 96:379–383, 2011.
Vanacker, J., M. M. Dolmans, V. Luyckx, J. Donnez, and C. A. Amorim. First transplantation of isolated murine follicles in alginate. Regen. Med. 9:609–619, 2014.
Vanacker, J., V. Luyckx, C. Amorim, M. M. Dolmans, A. Van Langendonckt, J. Donnez, and A. Camboni. Should we isolate human preantral follicles before or after cryopreservation of ovarian tissue? Fertil. Steril. 99:1363–1368, 2013.
Vanacker, J., V. Luyckx, M. M. Dolmans, A. Des Rieux, J. Jaeger, A. Van Langendonckt, J. Donnez, and C. A. Amorim. Transplantation of an alginate-matrigel matrix containing isolated ovarian cells: first step in developing a biodegradable scaffold to transplant isolated preantral follicles and ovarian cells. Biomaterials 33:6079–6085, 2012.
Vegetti, W., and F. Alagna. FSH and folliculogenesis: from physiology to ovarian stimulation. Reprod. Biomed. 12:684–694, 2006.
Vilela, J. M. V., E. C. R. Leonel, L. D’Oliveira, R. E. G. Paiva, A. L. Miranda-Vilela, C. A. Amorim, A. Pic-Taylor, and C. M. Lucci. Culture of domestic cat ovarian tissue in vitro and in the chick embryo chorioallantoic membrane. Theriogenology 86:1774–1781, 2016.
Viswanath, A., J. Vanacker, L. Germain, J. G. Leprince, A. Diogenes, K. M. Shakesheff, L. J. White and A. des Rieux. Extracellular matrix-derived hydrogels for dental stem cell delivery. J. Biomed. Mater. Res. A. 105: 319-328, 2017.
Wang, R. M., and K. L. Christman. Decellularized myocardial matrix hydrogels: In basic research and preclinical studies. Adv. Drug Deliv. Rev. 96:77–82, 2016.
Wang, T., J. Yan, C. Lu, X. Xia, T. Yin, X. Zhi, X. Zhu, T. Ding, W. Hu, H. Guo, R. Li, L. Yan, and J. Qiao. Human single follicle growth in vitro from cryopreserved ovarian tissue after slow freezing or vitrification. Hum. Reprod. 31:763–773, 2016.
Wang, T. R., L. Y. Yan, J. Yan, C. L. Lu, X. Xia, T. L. Yin, X. H. Zhu, J. M. Gao, T. Ding, W. H. Hu, H. Y. Guo, R. Li, and J. Qiao. Basic fibroblast growth factor promotes the development of human ovarian early follicles during growth in vitro. Hum. Reprod. 29:568–576, 2014.
West, E. R., L. D. Shea, and T. K. Woodruff. Engineering the follicle microenvironment. Semin. Reprod. Med. 25:287–299, 2007.
West, E. R., M. Xu, T. K. Woodruff, and L. D. Shea. Physical properties of alginate hydrogels and their effects on in vitro follicle development. Biomaterials 28:4439–4448, 2007.
West-Farrell, E. R., M. Xu, M. A. Gomberg, Y. H. Chow, T. K. Woodruff, and L. D. Shea. The mouse follicle microenvironment regulates antrum formation and steroid production: alterations in gene expression profiles. Biol. Reprod. 80:432–439, 2009.
Xiao, S., F. E. Duncan, L. Bai, C. T. Nguyen, L. D. Shea, and T. K. Woodruff. Size-specific follicle selection improves mouse oocyte reproductive outcomes. Reproduction 150:183–192, 2015.
Xu, M., A. Banc, T. K. Woodruff, and L. D. Shea. Secondary follicle growth and oocyte maturation by culture in alginate hydrogel following cryopreservation of the ovary or individual follicles. Biotechnol. Bioeng. 103:378–386, 2009.
Xu, M., S. L. Barrett, E. West-Farrell, L. A. Kondapalli, S. E. Kiesewetter, L. D. Shea, and T. K. Woodruff. In vitro grown human ovarian follicles from cancer patients support oocyte growth. Hum. Reprod. 24:2531–2540, 2009.
Xu, J., M. P. Bernuci, M. S. Lawson, R. R. Yeoman, T. E. Fisher, M. B. Zelinski, and R. L. Stouffer. Survival, growth, and maturation of secondary follicles from prepubertal, young, and older adult rhesus monkeys during encapsulated three-dimensional culture: effects of gonadotropins and insulin. Reproduction 140:685–697, 2010.
Xu, M., A. T. Fazleabas, A. Shikanov, E. Jackson, S. L. Barrett, J. Hirshfeld-Cytron, S. E. Kiesewetter, L. D. Shea, and T. K. Woodruff. In vitro oocyte maturation and preantral follicle culture from the luteal-phase baboon ovary produce mature oocytes. Biol. Reprod. 84:689–697, 2011.
Xu, J., J. D. Hennebold and D. B. Seifer. Direct vitamin D3 actions on rhesus macaque follicles in three-dimensional culture: assessment of follicle survival, growth, steroid, and antimüllerian hormone production. Fertil. Steril. 106:1815-1820.e1, 2016.
Xu, M., P. K. Kreeger, L. D. Shea, and T. K. Woodruff. Tissue-engineered follicles produce live, fertile offspring. Tissue Eng. 12:2739–2746, 2006.
Xu, J., M. S. Lawson, R. R. Yeoman, T. A. Molskness, A. Y. Ting, R. L. Stouffer, and M. B. Zelinski. Fibrin promotes development and function of macaque primary follicles during encapsulated three-dimensional culture. Hum. Reprod. 28:2187–2200, 2013.
Xu, J., M. S. Lawson, R. R. Yeoman, K. Y. Pau, S. L. Barrett, M. B. Zelinski, and R. L. Stouffer. Secondary follicle growth and oocyte maturation during encapsulated three-dimensional culture in rhesus monkeys: effects of gonadotrophins, oxygen and fetuin. Hum. Reprod. 26:1061–1072, 2011.
Xu, J., W. K. McGee, C. V. Bishop, B. S. Park, J. L. Cameron, M. B. Zelinski, and R. L. Stouffer. Exposure of female macaques to western-style diet with or without chronic T in vivo alters secondary follicle function during encapsulated 3-dimensional culture. Endocrinology 156:1133–1142, 2015.
Xu, M., E. West, L. S. Shea, and T. K. Woodruff. Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development. Biol. Reprod. 75:916–923, 2006.
Xu, M., E. R. West-Farrell, R. L. Stouffer, L. D. Shea, T. K. Woodruff, and M. B. Zelinski. Encapsulated three-dimensional culture supports development of nonhuman primate secondary follicles. Biol. Reprod. 81:587–594, 2009.
Yamamoto, K., T. Otoi, N. Koyama, N. Horikita, S. Tachikawa, and T. Miyano. Development to live young from bovine small oocytes after growth, maturation and fertilization in vitro. Theriogenology 52:81–89, 1999.
Yin, H., S. G. Kristensen, H. Jiang, A. Rasmussen, and C. Y. Andersen. Survival and growth of isolated pre-antral follicles from human ovarian medulla tissue during long-term 3D culture. Hum. Reprod. 31:1531–1539, 2016.
Zhou, H., M. A. Malik, A. Arab, M. T. Hill, and A. Shikanov. Hydrogel based 3-dimensional (3D) system for toxicity and high-throughput (HTP) analysis for cultured murine ovarian follicles. PLoS ONE 10:e0140205, 2015.
Acknowledgments
J. Vanacker is an FRS-FNRS postdoctoral researcher and C.A. Amorim is an FRS-FNRS research associate. The authors thank Mira Hryniuk, BA, for reviewing the English language of the manuscript.
Conflict of Interest
The authors have no conflict of interest to declare.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Associate Editor Debra T. Auguste oversaw the review of this article.
Rights and permissions
About this article
Cite this article
Vanacker, J., Amorim, C.A. Alginate: A Versatile Biomaterial to Encapsulate Isolated Ovarian Follicles. Ann Biomed Eng 45, 1633–1649 (2017). https://doi.org/10.1007/s10439-017-1816-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10439-017-1816-6