Advanced 3Dimentional Engineered Microenvironment to Improve of in Vitro Spermatogenesis: Narrative Review

Overview

Journal JBRA Assist Reprod

Date 2025 Jan 21

PMID 39835797

Authors

Masoud Ghorbani

Roya Hassani

Mohammad Reza Nourani

Vahabodin Goodarzi

Affiliations

Soon will be listed here.

Abstract

Induction of in vitro spermatogenesis may be helpful in the treatment of infertility in azoospermic individuals and those undergoing chemotherapy. Different cultivation systems have been implemented to achieve this aim. This review study aimed to investigate the application of three-dimensional culture in the induction of in vitro spermatogenesis. Relevant studies published in English were identified using PubMed using a range of search terms related to the core focus on tissue engineering of male reproductive systems, in vitro spermatogenesis, germ cell preservation, 3D culture systems for in vitro spermatogenesis, a 3D culture of testis tissue with were last updated in end of 2023. Searches were not restricted to a particular time frame or species, although the emphasis within the review is on regenerative medicine in mammalian male fertility preservation and in vitro spermatogenesis. Spermatogenesis is one of the most complicated cellular differentiation processes in the body. Significant attempts have been made to control spermatogenesis to drive differentiation of male germ stem cells toward mature sperm. Current research efforts focus on providing appropriate microenvironmental conditions to support the process of in vitro spermatogenesis by applying the principles of cell transplantation, material science, and bioengineering. Regenerative medicine may open a new avenue to patients for restoration and maintenance of normal function in spermatogenesis. The techniques reviewed are still in development, and this paper can become the primary reference for a large body of scientists developing advanced tissue engineering for male germ cells or developing the next generation of reproductive medicine.

References

Hermann B, Sukhwani M, Winkler F, Pascarella J, Peters K, Sheng Y . Spermatogonial stem cell transplantation into rhesus testes regenerates spermatogenesis producing functional sperm. Cell Stem Cell. 2012; 11(5):715-26. PMC: 3580057. DOI: 10.1016/j.stem.2012.07.017. View

Movassagh S, Banitalebi Dehkordi M, Koruji M, Pourmand G, Farzaneh P, Ashouri Movassagh S . In Vitro Spermatogenesis by Three-dimensional Culture of Spermatogonial Stem Cells on Decellularized Testicular Matrix. Galen Med J. 2021; 8:e1565. PMC: 8344169. DOI: 10.31661/gmj.v8i0.1565. View

AbuMadighem A, Shuchat S, Lunenfeld E, Yossifon G, Huleihel M . Testis on a chip-a microfluidic three-dimensional culture system for the development of spermatogenesis. Biofabrication. 2022; 14(3). DOI: 10.1088/1758-5090/ac6126. View

Congrains A, Bianco J, Rosa R, Mancuso R, Saad S . 3D Scaffolds to Model the Hematopoietic Stem Cell Niche: Applications and Perspectives. Materials (Basel). 2021; 14(3). PMC: 7865713. DOI: 10.3390/ma14030569. View

Kulibin A, Malolina E . spermatogenesis: In search of fully defined conditions. Front Cell Dev Biol. 2023; 11:1106111. PMC: 9998899. DOI: 10.3389/fcell.2023.1106111. View

Shams A, Eslahi N, Movahedin M, Izadyar F, Asgari H, Koruji M . Future of Spermatogonial Stem Cell Culture: Application of Nanofiber Scaffolds. Curr Stem Cell Res Ther. 2017; 12(7):544-553. DOI: 10.2174/1574888X12666170623095457. View

Johnston J, Stone Jr T, Wang Y . Biomaterial-enabled 3D cell culture technologies for extracellular vesicle manufacturing. Biomater Sci. 2023; 11(12):4055-4072. DOI: 10.1039/d3bm00469d. View

Park Y, Huh K, Kang S . Applications of Biomaterials in 3D Cell Culture and Contributions of 3D Cell Culture to Drug Development and Basic Biomedical Research. Int J Mol Sci. 2021; 22(5). PMC: 7958286. DOI: 10.3390/ijms22052491. View

Stukenborg J, Wistuba J, Luetjens C, Abu Elhija M, Huleihel M, Lunenfeld E . Coculture of spermatogonia with somatic cells in a novel three-dimensional soft-agar-culture-system. J Androl. 2007; 29(3):312-29. DOI: 10.2164/jandrol.107.002857. View

10.

Sayde T, Hamoui O, Alies B, Gaudin K, Lespes G, Battu S . Biomaterials for Three-Dimensional Cell Culture: From Applications in Oncology to Nanotechnology. Nanomaterials (Basel). 2021; 11(2). PMC: 7917665. DOI: 10.3390/nano11020481. View

11.

Ungewitter E, Yao H . How to make a gonad: cellular mechanisms governing formation of the testes and ovaries. Sex Dev. 2012; 7(1-3):7-20. PMC: 3474884. DOI: 10.1159/000338612. View

12.

Ganjibakhsh M, Mehraein F, Koruji M, Aflatoonian R, Farzaneh P . Three-dimensional decellularized amnion membrane scaffold promotes the efficiency of male germ cells generation from human induced pluripotent stem cells. Exp Cell Res. 2019; 384(1):111544. DOI: 10.1016/j.yexcr.2019.111544. View

13.

Guo J, Nie X, Giebler M, Mlcochova H, Wang Y, Grow E . The Dynamic Transcriptional Cell Atlas of Testis Development during Human Puberty. Cell Stem Cell. 2020; 26(2):262-276.e4. PMC: 7298616. DOI: 10.1016/j.stem.2019.12.005. View

14.

Di Persio S, Neuhaus N . Human spermatogonial stem cells and their niche in male (in)fertility: novel concepts from single-cell RNA-sequencing. Hum Reprod. 2022; 38(1):1-13. PMC: 9825264. DOI: 10.1093/humrep/deac245. View

15.

Zmrhal V, Svoradova A, Batik A, Slama P . Three-Dimensional Avian Hematopoietic Stem Cell Cultures as a Model for Studying Disease Pathogenesis. Front Cell Dev Biol. 2022; 9:730804. PMC: 8811169. DOI: 10.3389/fcell.2021.730804. View

16.

Sakib S, Voigt A, Goldsmith T, Dobrinski I . Three-dimensional testicular organoids as novel models of testicular biology and toxicology. Environ Epigenet. 2019; 5(3):dvz011. PMC: 6705190. DOI: 10.1093/eep/dvz011. View

17.

Mohaqiq M, Movahedin M, Mazaheri Z, Amirjannati N . In vitro transplantation of spermatogonial stem cells isolated from human frozen-thawed testis tissue can induce spermatogenesis under 3-dimensional tissue culture conditions. Biol Res. 2019; 52(1):16. PMC: 6438003. DOI: 10.1186/s40659-019-0223-x. View

18.

Galdon G, Atala A, Sadri-Ardekani H . In Vitro Spermatogenesis: How Far from Clinical Application?. Curr Urol Rep. 2016; 17(7):49. DOI: 10.1007/s11934-016-0605-3. View

19.

Alrahel A, Movahedin M, Mazaheri Z, Amidi F . Study of Tnp1, Tekt1, and Plzf Genes Expression During an in vitro Three-Dimensional Neonatal Male Mice Testis Culture. Iran Biomed J. 2018; 22(4):258-63. PMC: 5949128. DOI: 10.22034/ibj.22.4.258. View

20.

de Rooij D . The nature and dynamics of spermatogonial stem cells. Development. 2017; 144(17):3022-3030. DOI: 10.1242/dev.146571. View