Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2023-0039
Animal Reproduction (AR)
REVIEW ARTICLE

3D culture applied to reproduction in females: possibilities and perspectives

Giuliana de Avila Ferronato; Franciele Flores Vit; Juliano Coelho da Silveira

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Abstract

Abstract: In vitro cell culture is a well-established technique present in numerous laboratories in diverse areas. In reproduction, gametes, embryos, and reproductive tissues, such as the ovary and endometrium, can be cultured. These cultures are essential for embryo development studies, understanding signaling pathways, developing drugs for reproductive diseases, and in vitro embryo production (IVP). Although many culture systems are successful, they still have limitations to overcome. Three-dimensional (3D) culture systems can be close to physiological conditions, allowing greater interaction between cells and cells with the surrounding environment, maintenance of the cells' natural morphology, and expression of genes and proteins such as in vivo. Additionally, three-dimensional culture systems can stimulated extracellular matrix generating responses due to the mechanical force produced. Different techniques can be used to perform 3D culture systems, such as hydrogel matrix, hanging drop, low attachment surface, scaffold, levitation, liquid marble, and 3D printing. These systems demonstrate satisfactory results in follicle culture, allowing the culture from the pre-antral to antral phase, maintaining the follicular morphology, and increasing the development rates of embryos. Here, we review some of the different techniques of 3D culture systems and their applications to the culture of follicles and embryos, bringing new possibilities to the future of assisted reproduction.

Keywords

In vitro embryo, follicles, mechanotransduction, 3D culture system, tissue tension

References

Ahn SI, Sei YJ, Park HJ, Kim J, Ryu Y, Choi JJ, Sung HJ, MacDonald TJ, Levey AI, Kim Y. Microengineered human blood-brain barrier platform for understanding nanoparticle transport mechanisms. Nat Commun. 2020;11(1):175. http://dx.doi.org/10.1038/s41467-019-13896-7. PMid:31924752.

Alexandrova M, Manchorova D, You Y, Mor G, Dimitrova V, Dimova T. Functional HLA-C expressing trophoblast spheroids as a model to study placental-maternal immune interactions during human implantation. Sci Rep. 2022;12(1):10224. http://dx.doi.org/10.1038/s41598-022-12870-6. PMid:35715452.

Alzamil L, Nikolakopoulou K, Turco MY. Organoid systems to study the human female reproductive tract and pregnancy. Cell Death Differ. 2021;28(1):35-51. http://dx.doi.org/10.1038/s41418-020-0565-5. PMid:32494027.

Amorim CA. Special issue devoted to a new field of regenerative medicine: reproductive tissue engineering. Ann Biomed Eng. 2017;45(7):1589-91. http://dx.doi.org/10.1007/s10439-017-1862-0. PMid:28567657.

Antonino DC, Soares MM, Junior JM, de Alvarenga PB, Mohallem RFF, Rocha CD, Vieira LA, de Souza AG, Beletti ME, Alves BG, Jacomini JO, Goulart LR, Alves KA. Three-dimensional levitation culture improves in-vitro growth of secondary follicles in bovine model. Reprod Biomed Online. 2019;38(3):300-11. http://dx.doi.org/10.1016/j.rbmo.2018.11.013. PMid:30639159.

Araújo VR, Gastal MO, Wischral A, Figueiredo JR, Gastal EL. 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. 2014;82(9):1246-53. http://dx.doi.org/10.1016/j.theriogenology.2014.08.004. PMid:25219848.

Arcuri S, Pennarossa G, Ledda S, Gandolfi F, Brevini TAL. Use of epigenetic cues and mechanical stimuli to generate blastocyst-like structures from mammalian skin dermal fibroblasts. Methods Mol Biol. 2024;2767:161-73. http://dx.doi.org/10.1007/7651_2023_486. PMid:37199907.

Avrămescu RE, Ghica MV, Dinu-Pirvu C, Udeanu DI, Popa L. Liquid marbles: from industrial to medical applications. Molecules. 2018;23(5):1120. http://dx.doi.org/10.3390/molecules23051120. PMid:29747389.

Bebbere D, Nieddu SM, Ariu F, Piras D, Ledda S. 3D liquid marble microbioreactors support in vitro maturation of prepubertal ovine oocytes and affect expression of oocyte-specific factors. Biology (Basel). 2021;10(11):1101. http://dx.doi.org/10.3390/biology10111101. PMid:34827093.

Behringer R, Gertsenstein M, Nagy KV, Nagy A. Differentiating mouse embryonic stem cells into embryoid bodies by hanging-drop cultures. Cold Spring Harb Protoc. 2016;2016(12):pdb.prot092429. http://dx.doi.org/10.1101/pdb.prot092429. PMid:27934689.

Berry SM, Strotman LN, Kueck JD, Alarid ET, Beebe DJ. Purification of cell subpopulations via immiscible filtration assisted by surface tension (IFAST). Biomed Microdevices. 2011;13(6):1033-42. http://dx.doi.org/10.1007/s10544-011-9573-z. PMid:21796389.

Bhakta G, Lee KH, Magalhaes R, Wen F, Gouk SS, Hutmacher DW, Kuleshova LL. Cryopreservation of alginate-fibrin beads involving bone marrow derived mesenchymal stromal cells by vitrification. Biomaterials. 2009;30(3):336-43. http://dx.doi.org/10.1016/j.biomaterials.2008.09.030. PMid:18930316.

Bian J, Li T, Ding C, Xin W, Zhu B, Zhou C. Vitreous cryopreservation of human preantral follicles encapsulated in alginate beads with mini mesh cups. J Reprod Dev. 2013;59(3):288-95. http://dx.doi.org/10.1262/jrd.2012-157. PMid:23485957.

BioRender. 2023 [cited 2023 March 20]. Available from: https://app.biorender.com/biorender

Bouillon C, Léandri R, Desch L, Ernst A, Bruno C, Cerf C, Chiron A, Souchay C, Burguet A, Jimenez C, Sagot P, Fauque P. Does embryo culture medium influence the health and development of children born after in vitro fertilization? PLoS One. 2016;11(3):e0150857. http://dx.doi.org/10.1371/journal.pone.0150857. PMid:27008092.

Brito IR, Silva CM, Duarte AB, Lima IM, Rodrigues GQ, Rossetto R, Sales AD, Lobo CH, Bernuci MP, Rosa ESAC, Campello CC, Xu M, Figueiredo JR. Alginate hydrogel matrix stiffness influences the in vitro development of caprine preantral follicles. Mol Reprod Dev. 2014;81(7):636-45. http://dx.doi.org/10.1002/mrd.22330. PMid:24700587.

Burgdorf T, Piersma AH, Landsiedel R, Clewell R, Kleinstreuer N, Oelgeschlager M, Desprez B, Kienhuis A, Bos P, de Vries R, de Wit L, Seidle T, Scheel J, Schonfelder G, van Benthem J, Vinggaard AM, Eskes C, Ezendam J. Workshop on the validation and regulatory acceptance of innovative 3R approaches in regulatory toxicology - Evolution versus revolution. Toxicol In Vitro. 2019;59:1-11. http://dx.doi.org/10.1016/j.tiv.2019.03.039. PMid:30946968.

Bus A, van Hoeck V, Langbeen A, Leroy J, Bols PEJ. Effects of vitrification on the viability of alginate encapsulated isolated bovine pre-antral follicles. J Assist Reprod Genet. 2018;35(7):1187-99. http://dx.doi.org/10.1007/s10815-018-1208-3. PMid:29797286.

Canovas S, Ross PJ, Kelsey G, Coy P. DNA methylation in embryo development: epigenetic impact of ART (Assisted Reproductive Technologies). BioEssays. 2017;39(11):1700106. http://dx.doi.org/10.1002/bies.201700106. PMid:28940661.

Carrel A. The permanent life of tissues outside of the organism. J Exp Med. 1912;15(5):516-28. http://dx.doi.org/10.1084/jem.15.5.516. PMid:19867545.

Chen M, Le DQ, Baatrup A, Nygaard JV, Hein S, Bjerre L, Kassem M, Zou X, Bunger C. Self-assembled composite matrix in a hierarchical 3-D scaffold for bone tissue engineering. Acta Biomater. 2011;7(5):2244-55. http://dx.doi.org/10.1016/j.actbio.2010.12.031. PMid:21195810.

Choi JK, Agarwal P, Huang H, Zhao S, He X. The crucial role of mechanical heterogeneity in regulating follicle development and ovulation with engineered ovarian microtissue. Biomaterials. 2014;35(19):5122-8. http://dx.doi.org/10.1016/j.biomaterials.2014.03.028. PMid:24702961.

Correia HHV, Lima LF, Sousa FGC, Ferreira ACA, Cadenas J, Paes VM, Alves BG, Shikanov A, Figueiredo JR. Activation of goat primordial follicles in vitro: influence of alginate and ovarian tissue. Reprod Domest Anim. 2020;55(1):105-9. http://dx.doi.org/10.1111/rda.13582. PMid:31661715.

Crapo PM, Gilbert TW, Badylak SF. An overview of tissue and whole organ decellularization processes. Biomaterials. 2011;32(12):3233-43. http://dx.doi.org/10.1016/j.biomaterials.2011.01.057. PMid:21296410.

Determan MD, Cox JP, Mallapragada SK. Drug release from pH-responsive thermogelling pentablock copolymers. J Biomed Mater Res A. 2007;81(2):326-33. http://dx.doi.org/10.1002/jbm.a.30991. PMid:17120218.

Di Berardino C, Liverani L, Peserico A, Capacchietti G, Russo V, Bernabo N, Tosi U, Boccaccini AR, Barboni B. When electrospun fiber support matters: in vitro ovine long-term folliculogenesis on Poly (Epsilon Caprolactone) (PCL)-patterned fibers. Cells. 2022;11(12):1968. http://dx.doi.org/10.3390/cells11121968. PMid:35741097.

Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science. 2005;310(5751):1139-43. http://dx.doi.org/10.1126/science.1116995. PMid:16293750.

Do A-V, Khorsand B, Geary SM, Salem AK. 3D printing of scaffolds for tissue regeneration applications. Adv Healthc Mater. 2015;4(12):1742-62. http://dx.doi.org/10.1002/adhm.201500168. PMid:26097108.

Eaton NL, Niemeyer GP, Doody MC. The use of an alginic acid matrix to support in vitro development of isolated murine blastomeres. J In Vitro Fert Embryo Transf. 1990;7(1):28-32. http://dx.doi.org/10.1007/BF01133880. PMid:2338512.

Eder T, Eder IE. 3D hanging drop culture to establish prostate cancer organoids. Methods Mol Biol. 2017;1612:167-75. http://dx.doi.org/10.1007/978-1-4939-7021-6_12. PMid:28634942.

Edmondson R, Broglie JJ, Adcock AF, Yang L. Three-dimensional cell culture systems and their applications in drug discovery and cell-based biosensors. Assay Drug Dev Technol. 2014;12(4):207-18. http://dx.doi.org/10.1089/adt.2014.573. PMid:24831787.

Eissa AM, Barros FSV, Vrljicak P, Brosens JJ, Cameron NR. Enhanced differentiation potential of primary human endometrial cells cultured on 3D scaffolds. Biomacromolecules. 2018;19(8):3343-50. http://dx.doi.org/10.1021/acs.biomac.8b00635. PMid:29928802.

Ferraz MA, Henning HHW, Costa PF, Malda J, Melchels FP, Wubbolts R, Stout TAE, Vos P, Gadella BM. Improved bovine embryo production in an oviduct-on-a-chip system: prevention of poly-spermic fertilization and parthenogenic activation. Lab Chip. 2017;17(5):905-16. http://dx.doi.org/10.1039/C6LC01566B. PMid:28194463.

Ferraz MA, Rho HS, Hemerich D, Henning HHW, van Tol HTA, Holker M, Besenfelder U, Mokry M, Vos P, Stout TAE, Le Gac S, Gadella BM. An oviduct-on-a-chip provides an enhanced in vitro environment for zygote genome reprogramming. Nat Commun. 2018;9(1):4934. http://dx.doi.org/10.1038/s41467-018-07119-8. PMid:30467383.

Ferronato GA, Dos Santos CM, Rosa P, Bridi A, Perecin F, Meirelles FV, Sangalli JR, da Silveira JC. Bovine in vitro oocyte maturation and embryo culture in liquid marbles 3D culture system. PLoS One. 2023;18(4):e0284809. http://dx.doi.org/10.1371/journal.pone.0284809. PMid:37083878.

Filas BA, Bayly PV, Taber LA. Mechanical stress as a regulator of cytoskeletal contractility and nuclear shape in embryonic epithelia. Ann Biomed Eng. 2011;39(1):443-54. http://dx.doi.org/10.1007/s10439-010-0171-7. PMid:20878237.

Fuertes-Recuero M, Gonzalez-Gil A, Perez JCF, Ariati IG, Picazo RA. Determination of the appropriate concentration of sodium alginate used for in vitro culture of cat preantral follicles in a serum-free medium containing FSH, EGF and IGF-I. Reprod Domest Anim. 2023;58(5):670-8. http://dx.doi.org/10.1111/rda.14336. PMid:36862062.

Goodman TT, Ng CP, Pun SH. 3-D tissue culture systems for the evaluation and optimization of nanoparticle-based drug carriers. Bioconjug Chem. 2008;19(10):1951-9. http://dx.doi.org/10.1021/bc800233a. PMid:18788773.

Gu Q, Tomaskovic-Crook E, Wallace GG, Crook JM. 3D bioprinting human induced pluripotent stem cell constructs for in situ cell proliferation and successive multilineage differentiation. Adv Healthc Mater. 2017;6(17):1700175. http://dx.doi.org/10.1002/adhm.201700175. PMid:28544655.

Gutierrez CG, Ralph JH, Telfer EE, Wilmut I, Webb R. Growth and antrum formation of bovine preantral follicles in long-term culture in vitro1. Biol Reprod. 2000;62(5):1322-8. http://dx.doi.org/10.1095/biolreprod62.5.1322. PMid:10775183.

Habanjar O, Diab-Assaf M, Caldefie-Chezet F, Delort L. 3D cell culture systems: tumor application, advantages, and disadvantages. Int J Mol Sci. 2021;22(22):12200. http://dx.doi.org/10.3390/ijms222212200. PMid:34830082.

Haeger JD, Hambruch N, Dilly M, Froehlich R, Pfarrer C. Formation of bovine placental trophoblast spheroids. Cells Tissues Organs. 2011;193(4):274-84. http://dx.doi.org/10.1159/000320544. PMid:20975254.

Haycock JW. 3D cell culture: a review of current approaches and techniques. Methods Mol Biol. 2011;695:1-15. http://dx.doi.org/10.1007/978-1-60761-984-0_1. PMid:21042962.

Hoffman RM. In Memoriam: Joseph Leighton, 1921-1999: father of 3-Dimensional tissue culture. New York: Humana Press; 2018.. http://dx.doi.org/10.1007/978-1-4939-7745-1_1.

Holtfreter J. A study of the mechanics of gastrulation. J Exp Zool. 1944;95(2):171-212. http://dx.doi.org/10.1002/jez.1400950203.

Ishikawa S, Machida R, Hiraga K, Hiradate Y, Suda Y, Tanemura K. Hanging drop monoculture for selection of optimal antioxidants during in vitro maturation of porcine oocytes. Reprod Domest Anim. 2014;49(2):e26-30. http://dx.doi.org/10.1111/rda.12289. PMid:24629146.

Jaguszeski MZ, Pinto Neto A, Oliveira W, Cattelam J, Gregianini HAG. Pregnancy rate of recipient cows after transfer of in vitro-produced nellore embryos. Rev Caatinga. 2019;32(4):1087-91. http://dx.doi.org/10.1590/1983-21252019v32n425rc.

Jalayeri M, Pirnia A, Najafabad EP, Varzi AM, Gholami M. Evaluation of alginate hydrogel cytotoxicity on three-dimensional culture of type A spermatogonial stem cells. Int J Biol Macromol. 2017;95:888-94. http://dx.doi.org/10.1016/j.ijbiomac.2016.10.074. PMid:27984148.

Jensen C, Teng Y. Is it time to start transitioning from 2D to 3D cell culture? Front Mol Biosci. 2020;7(33):33. http://dx.doi.org/10.3389/fmolb.2020.00033. PMid:32211418.

Jones ASK, Shikanov A. Follicle development as an orchestrated signaling network in a 3D organoid. J Biol Eng. 2019;13(1):2-2. http://dx.doi.org/10.1186/s13036-018-0134-3. PMid:30647770.

Jorge S, Chang S, Barzilai JJ, Leppert P, Segars JH. Mechanical signaling in reproductive tissues: mechanisms and importance. Reprod Sci. 2014;21(9):1093-107. http://dx.doi.org/10.1177/1933719114542023. PMid:25001021.

Kaarj K, Yoon JY. Methods of delivering mechanical stimuli to organ-on-a-chip. Micromachines (Basel). 2019;10(10):700. http://dx.doi.org/10.3390/mi10100700. PMid:31615136.

Kessler M, Hoffmann K, Brinkmann V, Thieck O, Jackisch S, Toelle B, Berger H, Mollenkopf HJ, Mangler M, Sehouli J, Fotopoulou C, Meyer TF. The Notch and Wnt pathways regulate stemness and differentiation in human fallopian tube organoids. Nat Commun. 2015;6(1):8989. http://dx.doi.org/10.1038/ncomms9989. PMid:26643275.

Kim EJ, Yang C, Lee J, Youm HW, Lee JR, Suh CS, Kim SH. The new biocompatible material for mouse ovarian follicle development in three-dimensional in vitro culture systems. Theriogenology. 2020;144:33-40. http://dx.doi.org/10.1016/j.theriogenology.2019.12.009. PMid:31895996.

Kim JW, Nam SA, Yi J, Kim JY, Lee JY, Park SY, Sen T, Choi YM, Lee JY, Kim HL, Kim HW, Park J, Cho DW, Kim YK. Kidney decellularized extracellular matrix enhanced the vascularization and maturation of human kidney organoids. Adv Sci (Weinh). 2022;9(15):e2103526. http://dx.doi.org/10.1002/advs.202103526. PMid:35322595.

Knight E, Przyborski S. Advances in 3D cell culture technologies enabling tissue-like structures to be created in vitro. J Anat. 2015;227(6):746-56. http://dx.doi.org/10.1111/joa.12257. PMid:25411113.

Knöspel F, Ban Z, Schonfelder G, Schneider MR. Next milestone in understanding early life-blastoids mimic embryogenesis in vitro. Biol Reprod. 2019;100(1):11-2. http://dx.doi.org/10.1093/biolre/ioy182. PMid:30657896.

Kolahi KS, Donjacour A, Liu X, Lin W, Simbulan RK, Bloise E, Maltepe E, Rinaudo P. Effect of substrate stiffness on early mouse embryo development. PLoS One. 2012;7(7):e41717. http://dx.doi.org/10.1371/journal.pone.0041717. PMid:22860009.

Kopper O, de Witte CJ, Lohmussaar K, Valle-Inclan JE, Hami N, Kester L, Balgobind AV, Korving J, Proost N, Begthel H, van Wijk LM, Revilla SA, Theeuwsen R, van de Ven M, van Roosmalen MJ, Ponsioen B, Ho VWH, Neel BG, Bosse T, Gaarenstroom KN, Vrieling H, Vreeswijk MPG, van Diest PJ, Witteveen PO, Jonges T, Bos JL, van Oudenaarden A, Zweemer RP, Snippert HJG, Kloosterman WP, Clevers H. An organoid platform for ovarian cancer captures intra- and interpatient heterogeneity. Nat Med. 2019;25(5):838-49. http://dx.doi.org/10.1038/s41591-019-0422-6. PMid:31011202.

Langhans SA. Three-dimensional in vitro cell culture models in drug discovery and drug repositioning. Front Pharmacol. 2018;9:6. http://dx.doi.org/10.3389/fphar.2018.00006. PMid:29410625.

Laronda MM, Jakus AE, Whelan KA, Wertheim JA, Shah RN, Woodruff TK. Initiation of puberty in mice following decellularized ovary transplant. Biomaterials. 2015;50:20-9. http://dx.doi.org/10.1016/j.biomaterials.2015.01.051. PMid:25736492.

Laronda MM, Rutz AL, Xiao S, Whelan KA, Duncan FE, Roth EW, Woodruff TK, Shah RN. A bioprosthetic ovary created using 3D printed microporous scaffolds restores ovarian function in sterilized mice. Nat Commun. 2017;8(1):15261. http://dx.doi.org/10.1038/ncomms15261. PMid:28509899.

Laronda MM. Engineering a bioprosthetic ovary for fertility and hormone restoration. Theriogenology. 2020;150:8-14. http://dx.doi.org/10.1016/j.theriogenology.2020.01.021. PMid:31973967.

Ledda S, Idda A, Kelly J, Ariu F, Bogliolo L, Bebbere D. A novel technique for in vitro maturation of sheep oocytes in a liquid marble microbioreactor. J Assist Reprod Genet. 2016;33(4):513-8. http://dx.doi.org/10.1007/s10815-016-0666-8. PMid:26852233.

Lee KY, Mooney DJ. Alginate: properties and biomedical applications. Prog Polym Sci. 2012;37(1):106-26. http://dx.doi.org/10.1016/j.progpolymsci.2011.06.003. PMid:22125349.

Leighton J. A sponge matrix method for tissue culture; formation of organized aggregates of cells in vitro. J Natl Cancer Inst. 1951;12(3):545-61. PMid:14889259.

Li R, Zhong C, Yu Y, Liu H, Sakurai M, Yu L, Min Z, Shi L, Wei Y, Takahashi Y, Liao HK, Qiao J, Deng H, Nunez-Delicado E, Rodriguez Esteban C, Wu J, Izpisua Belmonte JC. Generation of blastocyst-like structures from mouse embryonic and adult cell cultures. Cell. 2019;179(3):687-702.e618. http://dx.doi.org/10.1016/j.cell.2019.09.029. PMid:31626770.

Li S, Winuthayanon W. Oviduct: roles in fertilization and early embryo development. J Endocrinol. 2017;232(1):R1-26. http://dx.doi.org/10.1530/JOE-16-0302. PMid:27875265.

Liverani L, Raffel N, Fattahi A, Preis A, Hoffmann I, Boccaccini AR, Beckmann MW, Dittrich R. Electrospun patterned porous scaffolds for the support of ovarian follicles growth: a feasibility study. Sci Rep. 2019;9(1):1150. http://dx.doi.org/10.1038/s41598-018-37640-1. PMid:30718584.

Lopez-Garcia MD, Beebe DJ, Crone WC. Young’s modulus of collagen at slow displacement rates. Biomed Mater Eng. 2010;20(6):361-9. http://dx.doi.org/10.3233/BME-2010-0649. PMid:21263182.

MacKintosh SB, Serino LP, Iddon PD, Brown R, Conlan RS, Wright CJ, Maffeis TG, Raxworthy MJ, Sheldon IM. A three-dimensional model of primary bovine endometrium using an electrospun scaffold. Biofabrication. 2015;7(2):025010. http://dx.doi.org/10.1088/1758-5090/7/2/025010. PMid:26019144.

Martino F, Perestrelo AR, Vinarsky V, Pagliari S, Forte G. Cellular mechanotransduction: from tension to function. Front Physiol. 2018;9:824. http://dx.doi.org/10.3389/fphys.2018.00824. PMid:30026699.

Matsuura K, Hayashi N, Kuroda Y, Takiue C, Hirata R, Takenami M, Aoi Y, Yoshioka N, Habara T, Mukaida T, Naruse K. Improved development of mouse and human embryos using a tilting embryo culture system. Reprod Biomed Online. 2010;20(3):358-64. http://dx.doi.org/10.1016/j.rbmo.2009.12.002. PMid:20093091.

Montanez-Sauri SI, Beebe DJ, Sung KE. Microscale screening systems for 3D cellular microenvironments: platforms, advances, and challenges. Cell Mol Life Sci. 2015;72(2):237-49. http://dx.doi.org/10.1007/s00018-014-1738-5. PMid:25274061.

Montanez-Sauri SI, Sung KE, Berthier E, Beebe DJ. Enabling screening in 3D microenvironments: probing matrix and stromal effects on the morphology and proliferation of T47D breast carcinoma cells. Integr Biol. 2013;5(3):631-40. http://dx.doi.org/10.1039/c3ib20225a. PMid:23340769.

Nie N, Gong L, Jiang D, Liu Y, Zhang J, Xu J, Yao X, Wu B, Li Y, Zou X. 3D bio-printed endometrial construct restores the full-thickness morphology and fertility of injured uterine endometrium. Acta Biomater. 2023;157:187-99. http://dx.doi.org/10.1016/j.actbio.2022.12.016. PMid:36521675.

Nikolova MP, Chavali MS. Recent advances in biomaterials for 3D scaffolds: a review. Bioact Mater. 2019;4:271-92. http://dx.doi.org/10.1016/j.bioactmat.2019.10.005. PMid:31709311.

Nishiguchi A, Taguchi T. A pH-driven genipin gelator to engineer decellularized extracellular matrix-based tissue adhesives. Acta Biomater. 2021;131:211-21. http://dx.doi.org/10.1016/j.actbio.2021.06.033. PMid:34198010.

Ohnuki Y, Kurosawa H. Effects of hanging drop culture conditions on embryoid body formation and neuronal cell differentiation using mouse embryonic stem cells: optimization of culture conditions for the formation of well-controlled embryoid bodies. J Biosci Bioeng. 2013;115(5):571-4. http://dx.doi.org/10.1016/j.jbiosc.2012.11.016. PMid:23276518.

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):1013-21. http://dx.doi.org/10.1089/107632703322495655. PMid:14633385.

Pennarossa G, Arcuri S, De Iorio T, Ledda S, Gandolfi F, Brevini TAL. Combination of epigenetic erasing and mechanical cues to generate human epiBlastoids from adult dermal fibroblasts. J Assist Reprod Genet. 2023;40(5):1015-27. http://dx.doi.org/10.1007/s10815-023-02773-4. PMid:36933093.

Pennarossa G, De Iorio T, Gandolfi F, Brevini TAL. Ovarian decellularized bioscaffolds provide an optimal microenvironment for cell growth and differentiation in vitro. Cells. 2021;10(8):2126. http://dx.doi.org/10.3390/cells10082126. PMid:34440895.

Pennarossa G, Ghiringhelli M, Gandolfi F, Brevini TAL. Whole-ovary decellularization generates an effective 3D bioscaffold for ovarian bioengineering. J Assist Reprod Genet. 2020a;37(6):1329-39. http://dx.doi.org/10.1007/s10815-020-01784-9. PMid:32361917.

Pennarossa G, Manzoni EFM, Ledda S, deEguileor M, Gandolfi F, Brevini TAL. Use of a PTFE micro-bioreactor to promote 3D cell rearrangement and maintain high plasticity in epigenetically erased fibroblasts. Stem Cell Rev Rep. 2019;15(1):82-92. http://dx.doi.org/10.1007/s12015-018-9862-5. PMid:30397853.

Pereira VM, Pinto PAF, Motta LCB, Almeida MF, de Andrade AFC, Pavaneli APP, Ambrosio CE. Initial characterization of 3D culture of yolk sac tissue. Animals (Basel). 2023;13(9):1435. http://dx.doi.org/10.3390/ani13091435. PMid:37174472.

Peserico A, Di Berardino C, Capacchietti G, Camerano Spelta Rapini C, Liverani L, Boccaccini AR, Russo V, Mauro A, Barboni B. IVM advances for early antral follicle-enclosed oocytes coupling reproductive tissue engineering to inductive influences of human chorionic gonadotropin and ovarian surface epithelium coculture. Int J Mol Sci. 2023;24(7):6626. http://dx.doi.org/10.3390/ijms24076626. PMid:37047595.

Picton HM, Gosden RG. In vitro growth of human primordial follicles from frozen-banked ovarian tissue. Mol Cell Endocrinol. 2000;166(1):27-35. http://dx.doi.org/10.1016/S0303-7207(00)00294-X. PMid:10989205.

Ravi M, Paramesh V, Kaviya SR, Anuradha E, Solomon FD. 3D cell culture systems: advantages and applications. J Cell Physiol. 2015;230(1):16-26. http://dx.doi.org/10.1002/jcp.24683. PMid:24912145.

Ren H, Zhang Y, Zhang Y, Qiu Y, Chang Q, Yu X, Pei X. Optimized study of an in vitro 3D culture of preantral follicles in mice. J Vet Sci. 2023;24(1):e4. http://dx.doi.org/10.4142/jvs.22223. PMid:36560836.

Rossetto R, Saraiva MVA, Bernuci MP, Silva GM, Brito IR, Alves A, Magalhaes-Padilha DM, Bao SN, Campello CC, Rodrigues APR, Figueiredo JR. Impact of insulin concentration and mode of FSH addition on the in vitro survival and development of isolated bovine preantral follicles. Theriogenology. 2016;86(4):1137-45. http://dx.doi.org/10.1016/j.theriogenology.2016.04.003. PMid:27207475.

Sadeghnia S, Akhondi MM, Hossein G, Mobini S, Hosseini L, Naderi MM, Boroujeni SB, Sarvari A, Behzadi B, Shirazi A. Development of sheep primordial follicles encapsulated in alginate or in ovarian tissue in fresh and vitrified samples. Cryobiology. 2016;72(2):100-5. http://dx.doi.org/10.1016/j.cryobiol.2016.03.001. PMid:26968252.

Sadr SZ, Fatehi R, Maroufizadeh S, Amorim CA, Ebrahimi B. Utilizing fibrin-alginate and matrigel-alginate for mouse follicle development in three-dimensional culture systems. Biopreserv Biobank. 2018;16(2):120-7. http://dx.doi.org/10.1089/bio.2017.0087. PMid:29363997.

Sahoo DR, Biswal T. Alginate and its application to tissue engineering. SN Applied Sciences. 2021;3(1):30. http://dx.doi.org/10.1007/s42452-020-04096-w.

Sanches BV, Zangirolamo AF, Silva NC, Morotti F, Seneda MM. Cryopreservation of in vitro-produced embryos: challenges for commercial implementation. Anim Reprod. 2017;14(3):521-7. http://dx.doi.org/10.21451/1984-3143-AR995.

Shen P, Xu J, Wang P, Zhao X, Huang B, Wu F, Wang L, Chen W, Feng Y, Guo Z, Liu X, Deng Y, Jiang J, Shi D, Lu F. A new three-dimensional glass scaffold increases the in vitro maturation efficiency of buffalo (Bubalus bubalis) oocyte via remodelling the extracellular matrix and cell connection of cumulus cells. Reprod Domest Anim. 2020;55(2):170-80. http://dx.doi.org/10.1111/rda.13602. PMid:31816136.

Souza GR, Molina JR, Raphael RM, Ozawa MG, Stark DJ, Levin CS, Bronk LF, Ananta JS, Mandelin J, Georgescu MM, Bankson JA, Gelovani JG, Killian TC, Arap W, Pasqualini R. Three-dimensional tissue culture based on magnetic cell levitation. Nat Nanotechnol. 2010;5(4):291-6. http://dx.doi.org/10.1038/nnano.2010.23. PMid:20228788.

Su G, Zhao Y, Wei J, Han J, Chen L, Xiao Z, Chen B, Dai J. The effect of forced growth of cells into 3D spheres using low attachment surfaces on the acquisition of stemness properties. Biomaterials. 2013;34(13):3215-22. http://dx.doi.org/10.1016/j.biomaterials.2013.01.044. PMid:23439133.

Swift FR. A hanging-drop technique for general laboratory use. Microchem J. 1963;7(1):120-36. http://dx.doi.org/10.1016/0026-265X(63)90016-X.

Tosca EM, Ronchi D, Facciolo D, Magni P. Replacement, reduction, and refinement of animal experiments in anticancer drug development: the contribution of 3D in vitro cancer models in the drug efficacy assessment. Biomedicines. 2023;11(4):1058. http://dx.doi.org/10.3390/biomedicines11041058. PMid:37189676.

Tsai YA, Li T, Torres-Fernández LA, Weise SC, Kolanus W, Takeoka S. Ultra-thin porous PDLLA films promote generation, maintenance, and viability of stem cell spheroids. Front Bioeng Biotechnol. 2021;9:674384. http://dx.doi.org/10.3389/fbioe.2021.674384. PMid:34195179.

Türker E, Demircak N, Arslan-Yildiz A. Scaffold-free three-dimensional cell culturing using magnetic levitation. Biomater Sci. 2018;6(7):1745-53. http://dx.doi.org/10.1039/C8BM00122G. PMid:29700506.

Vanacker J, Amorim CA. Alginate: a versatile biomaterial to encapsulate isolated ovarian follicles. Ann Biomed Eng. 2017;45(7):1633-49. http://dx.doi.org/10.1007/s10439-017-1816-6. PMid:28247039.

Vanacker J, Luyckx V, Dolmans MM, Des Rieux A, Jaeger J, Van Langendonckt A, Donnez J, Amorim CA. 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. 2012;33(26):6079-85. http://dx.doi.org/10.1016/j.biomaterials.2012.05.015. PMid:22658800.

Wang X, Young DJ, Wu YL, Loh XJ. Thermogelling 3D systems towards stem cell-based tissue regeneration therapies. Molecules. 2018;23(3):553. http://dx.doi.org/10.3390/molecules23030553. PMid:29498651.

Wu H-W, Hsiao Y-H, Chen C-C, Yet S-F, Hsu C-H. A PDMS-based microfluidic hanging drop chip for embryoid body formation. Molecules. 2016;21(7):882. http://dx.doi.org/10.3390/molecules21070882. PMid:27399655.

Wu T, Gao YY, Su J, Tang XN, Chen Q, Ma LW, Zhang JJ, Wu JM, Wang SX. Three-dimensional bioprinting of artificial ovaries by an extrusion-based method using gelatin-methacryloyl bioink. Climacteric. 2022;25(2):170-8. http://dx.doi.org/10.1080/13697137.2021.1921726. PMid:33993814.

Xiao S, Coppeta JR, Rogers HB, Isenberg BC, Zhu J, Olalekan SA, McKinnon KE, Dokic D, Rashedi AS, Haisenleder DJ, Malpani SS, Arnold-Murray CA, Chen K, Jiang M, Bai L, Nguyen CT, Zhang J, Laronda MM, Hope TJ, Maniar KP, Pavone ME, Avram MJ, Sefton EC, Getsios S, Burdette JE, Kim JJ, Borenstein JT, Woodruff TK. A microfluidic culture model of the human reproductive tract and 28-day menstrual cycle. Nat Commun. 2017;8(1):14584. http://dx.doi.org/10.1038/ncomms14584. PMid:28350383.

Xu J, Lawson MS, Yeoman RR, Molskness TA, Ting AY, Stouffer RL, Zelinski MB. Fibrin promotes development and function of macaque primary follicles during encapsulated three-dimensional culture. Hum Reprod. 2013;28(8):2187-200. http://dx.doi.org/10.1093/humrep/det093. PMid:23608357.

Xu J, Lawson MS, Yeoman RR, Pau KY, Barrett SL, Zelinski MB, Stouffer RL. Secondary follicle growth and oocyte maturation during encapsulated three-dimensional culture in rhesus monkeys: effects of gonadotrophins, oxygen and fetuin. Hum Reprod. 2011;26(5):1061-72. http://dx.doi.org/10.1093/humrep/der049. PMid:21362681.

Yadav M, Agrawal H, Pandey M, Singh D, Onteru SK. Three-dimensional culture of buffalo granulosa cells in hanging drop mimics the preovulatory follicle stage. J Cell Physiol. 2018;233(3):1959-70. http://dx.doi.org/10.1002/jcp.25909. PMid:28294325.

Yao Q, Zheng YW, Lan QH, Kou L, Xu HL, Zhao YZ. Recent development and biomedical applications of decellularized extracellular matrix biomaterials. Mater Sci Eng C. 2019;104:109942. http://dx.doi.org/10.1016/j.msec.2019.109942. PMid:31499951.

Zhao F, Cheng J, Zhang J, Yu H, Dai W, Yan W, Sun M, Ding G, Li Q, Meng Q, Liu Q, Duan X, Hu X, Ao Y. Comparison of three different acidic solutions in tendon decellularized extracellular matrix bio-ink fabrication for 3D cell printing. Acta Biomater. 2021;131:262-75. http://dx.doi.org/10.1016/j.actbio.2021.06.026. PMid:34157451.

Zhao S, Liu ZX, Gao H, Wu Y, Fang Y, Wu SS, Li MJ, Bai JH, Liu Y, Evans A, Zeng SM. A three-dimensional culture system using alginate hydrogel prolongs hatched cattle embryo development in vitro. Theriogenology. 2015;84(2):184-92. http://dx.doi.org/10.1016/j.theriogenology.2015.03.011. PMid:25881989.

Zhao X, Zhang S, Gao S, Chang HM, Leung PCK, Tan J. A novel three-dimensional follicle culture system decreases oxidative stress and promotes the prolonged culture of human granulosa cells. ACS Appl Mater Interfaces. 2023;15(12):15084-95. http://dx.doi.org/10.1021/acsami.2c18734. PMid:36926803.

Zhou H, Malik MA, Arab A, Hill MT, Shikanov A. Hydrogel based 3-Dimensional (3D) system for toxicity and High-Throughput (HTP) analysis for cultured murine ovarian follicles. PLoS One. 2015;10(10):e0140205. http://dx.doi.org/10.1371/journal.pone.0140205. PMid:26451950.
 


Submitted date:
03/20/2023

Accepted date:
12/13/2023

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