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Fath-Bayati, L., Naserpour, L., Khoshandam, M., Jannatifar, R., & Fazaeli, H. (2023). Recent advances in developing 3D culture systems of spermatogonial stem cell preservation and differentiation: A narrative review. International Journal of Reproductive BioMedicine (IJRM), 21(9), 681–696. https://doi.org/10.18502/ijrm.v21i9.14397
https://doi.org/10.18502/ijrm.v21i9.14397
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authors
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Leyla Fath-Bayati
Leyla Fath-Bayati
Department of Tissue Engineering and Applied Cell Sciences, School of Medicine, Qom University of Medical Sciences, Qom, Iran.
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Leila Naserpour
Leila Naserpour
Department of Tissue Engineering and Applied Cell Sciences, School of Medicine, Qom University of Medical Sciences, Qom, Iran.
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Mohadeseh Khoshandam
Mohadeseh Khoshandam
Department of Reproductive Biology, Academic Center for Education, Culture and Research, Qom Branch, Qom, Iran.
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Rahil Jannatifar
Rahil Jannatifar
Department of Reproductive Biology, Academic Center for Education, Culture and Research, Qom Branch, Qom, Iran.
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Hoda Fazaeli
Hoda Fazaeli
Department of Mesenchymal Stem Cells, Academic Center for Education, Culture and Research, Qom Branch, Qom, Iran.
Published Date
- Oct 26, 2023
Recent advances in developing 3D culture systems of spermatogonial stem cell preservation and differentiation: A narrative review
Abstract
Male infertility has received vast attention in recent years and has no clear etiology in almost 40% of cases. Several methods have been suggested for preserving sperm and spermatogonial stem cells (SSCs) in both in vivo and in vitro conditions. The efficacy of these methods is related to their abilities, including providing an optimal environment for sperm preservation and long-term SSC culture for in vivo and in vitro differentiation of these cells. In this review article, a full MEDLINE/PubMed search was performed using the following search terms: "Spermatogonial Progenitor Cells, Stem Cells, Fertility Preservations, Sperm Freezing, Cell Differentiations, Tissue Scaffold, 3-Dimensional Cell Culture", which retrieved results from 1973-2022. Related articles were added to the bibliography of selected articles. Exclusion criteria included non-English language, abstract only, and unrelated articles. The production of functioning male germ cells is suggested by introducing modern bioengineered systems as a new hope for the maintenance of male fertility. Till now, few in vitro spermatogenesis investigations have provided appreciable amounts of mature gametes. Each method had benefits and disadvantages, but the 3-dimensional culture method had the greatest impact on the differentiation and preservation of SSCs. One of the critical elements of research is the preservation of sperm and the differentiation of SSCs. Several methods have been employed in this area. Various scaffolds providing an environment similar to an extracellular matrix and conditions for germ cell development and survival have been employed in recent research.
Key words: Tissue engineering, Male infertility, Scaffold, Stem cells, 3D cell culture, Differentiation.
References
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[4] Ilacqua A, Izzo G, Emerenziani GP, Baldari C, Aversa A. Lifestyle and fertility: The influence of stress and quality of life on male fertility. Reprod Biol Endocrinol 2018; 16: 115.
[5] Dolmans M-M, Manavella DD. Recent advances in fertility preservation. J Obstet Gynaecol Res 2019; 45: 266–279.
[6] Abdel-Naser MB, Zouboulis CC. Male fertility and skin diseases. Rev Endocr Metab Disord 2016; 17: 353–365.
[7] Das S, Roychoudhury Sh, Roychoudhury Sh, Agarwal A, Henkel R. Role of infection and leukocytes in male infertility. Adv Exp Med Biol 2022; 1358: 115–140.
[8] Abdel-Naser MB, Altenburg A, Zouboulis CC, Wollina U. Schistosomiasis (bilharziasis) and male infertility. Andrologia 2019; 51: e13165.
[9] Micol LA, Adenubi F, Williamson E, Lane Sh, Mitchell RT, Sangster P. The importance of the urologist in male oncology fertility preservation. BJU Int 2022; 130: 637– 645.
[10] Beveridge T. Anatomy of the infrarenal aortic plexus: Implications for nerve-sparing retroperitoneal lymph node dissection [Ph.D. thesis]. Canada: The University of Western Ontario; 2018.
[11] van Wolff M, Nawroth F. Indications for and against fertility preservation. In: van Wolff M, Nawroth F. Fertility preservation in oncological and non-oncological diseases. Switzerland: Springer; 2020. 25–29.
[12] Klitzman R. How much is a child worth? Providers’ and patients’ views and responses concerning ethical and policy challenges in paying for ART. PLoS One 2017; 12: e0171939.
[13] Sanner C, Coleman M. (Re) constructing family images: Stepmotherhood before biological motherhood. J Marriage Fam 2017; 79: 1462–1477.
[14] Zapzalka DM, Redmon JB, Pryor JL. A survey of oncologists regarding sperm cryopreservation and assisted reproductive techniques for male cancer patients. Cancer 1999; 86: 1812–1817.
[15] Redig AJ, Brannigan R, Stryker SJ, Woodruff TK, Jeruss JS. Incorporating fertility preservation into the care of young oncology patients. Cancer 2011; 117: 4–10.
[16] Yokonishi T, Ogawa T. Cryopreservation of testis tissues and in vitro spermatogenesis. Reprod Med Biol 2016; 15: 21–28.
[17] Sharma S, Wistuba J, Pock T, Schlatt S, Neuhaus N. Spermatogonial stem cells: Updates from specification to clinical relevance. Hum Reprod Update 2019; 25: 275– 297.
[18] Kubota H, Brinster RL. Spermatogonial stem cells. Biol Reprod 2018; 99: 52–74.
[19] Ibtisham F, Honaramooz A. Spermatogonial stem cells for in vitro spermatogenesis and in vivo restoration of fertility. Cells 2020; 9: 745.
[20] Seki Y, Yamaji M, Yabuta Y, Sano M, Shigeta M, Matsui Y, et al. Cellular dynamics associated with the genomewide epigenetic reprogramming in migrating primordial germ cells in mice. Development 2007; 134: 2627–2638.
[21] Wang P, Miao Y, Li X-H, Zhang N, Wang Q, Yue W, et al. Proteome landscape and spatial map of mouse primordial germ cells. Sci China Life Sci 2021; 64: 966– 981.
[22] Akyash F, Aflatoonian R, Yazd EF, Golzadeh J, Tahajjodi SS, Moore H, et al. Testicular sperm extraction derived cells conditioned medium as an in vitro niche supports germ cells development from human embryonic stem cells. In: Proceedings of the 35th Annual Meeting of the European Society for Human Reproduction and Embryology. Viena, Austria; 2019.
[23] Nikolic A, Volarevic V, Armstrong L, Lako M, Stojkovic M. Primordial germ cells: Current knowledge and perspectives. Stem Cells Int 2016; 2016: 1741072.
[24] Hayashi K, Saitou M. Perspectives of germ cell development in vitro in mammals. Anim Sci J 2014; 85: 617–626.
[25] Zhu Y, Hu H-L, Li P, Yang Sh, Zhang W, Ding H, et al. Generation of male germ cells from induced pluripotent stem cells (iPS cells): An in vitro and in vivo study. Asian J Androl 2012; 14: 574–579.
[26] Li L, Yang R, Yin C, Kee K. Studying human reproductive biology through single-cell analysis and in vitro differentiation of stem cells into germ cell-like cells. Hum Reprod Update 2020; 26: 670–688.
[27] Pirouz M, Klimke A, Kessel M. The reciprocal relationship between primordial germ cells and pluripotent stem cells. J Mol Med 2012; 90: 753–761.
[28] Wainwright EN, Wilhelm D. The game plan: Cellular and molecular mechanisms of mammalian testis development. Curr Top Dev Biol 2010; 90: 231–262.
[29] Piprek RP. Molecular and cellular machinery of gonadal differentiation in mammals. Int J Dev Biol 2010; 54: 779– 786.
[30] Mackay S. Gonadal development in mammals at the cellular and molecular levels. Int Rev Cytol 2000; 200: 47–99.
[31] Brennan J, Capel B. One tissue, two fates: Molecular genetic events that underlie testis versus ovary development. Nat Rev Genet 2004; 5: 509–521.
[32] Nef S, Stevant I, Greenfield A. Characterizing the bipotential mammalian gonad. Curr Top Dev Biol 2019; 134: 167–194.
[33] Chen L-Y, Willis WD, Eddy EM. Targeting the Gdnf gene in peritubular myoid cells disrupts undifferentiated spermatogonial cell development. Proc Natl Acad Sci USA 2016; 113: 1829–1834.
[34] Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukhwani M, et al. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 2004; 36: 653– 659.
[35] Kashfi A, Narenji Sani R, Ahmadi-hamedani M. The beneficial effect of equine chorionic gonadotropin hormone (eCG) on the in vitro co-culture of bovine spermatogonial stem cell with Sertoli cells. Comparat Clin Pathol 2019; 28: 701–704.
[36] Davis JC, Snyder EM, Hogarth CA, Small Ch, Griswold MD. Induction of spermatogenic synchrony by retinoic acid in neonatal mice. Spermatogenesis 2013; 3: e23180.
[37] Dovere L, Fera S, Grasso M, Lamberti D, Gargioli C, Muciaccia B, et al. The niche-derived glial cell linederived neurotrophic factor (GDNF) induces migration of mouse spermatogonial stem/progenitor cells. PLoS One 2013; 8: e59431.
[38] Kitadate Y, Jorg DJ, Tokue M, Maruyama A, Ichikawa R, Tsuchiya S, et al. Competition for mitogens regulates spermatogenic stem cell homeostasis in an open niche. Cell Stem Cell 2019; 24: 79–92.
[39] Masaki K, Sakai M, Kuroki Sh, Jo J-I, Hoshina K, Fujimori Y, et al. FGF2 has distinct molecular functions from GDNF in the mouse germline niche. Stem Cell Reports 2018; 10: 1782–1792.
[40] Salaritabar A, Berindan-Neagoe I, Darvish B, Hadjiakhoondi F, Manayi A, Devi KP, et al. Targeting Hedgehog signaling pathway: Paving the road for cancer therapy. Pharmacol Res 2019; 141: 466–480.
[41] Goossens E, Van Saen D, Tournaye H. Spermatogonial stem cell preservation and transplantation: From research to clinic. Hum Reprod 2013; 28: 897–907.
[42] Gies I, De Schepper J, Goossens E, Van Saen D, Pennings G, Tournaye H. Spermatogonial stem cell preservation in boys with Klinefelter syndrome: To bank or not to bank, that’s the question. Fertil Steril 2012; 98: 284–289.
[43] Pourhabibi Zarandi N, Galdon G, Kogan S, Atala A, Sadri-Ardekani H. Cryostorage of immature and mature human testis tissue to preserve spermatogonial stem cells (SSCs): A systematic review of current experiences toward clinical applications. Stem Cells Cloning 2018; 11: 23–38.
[44] Mohammadzadeh E, Mirzapour T, Nowroozi MR, Nazarian H, Piryaei A, Alipour F, et al. Differentiation of spermatogonial stem cells by soft agar threedimensional culture system. Artif Cells Nanomed Biotechnol 2019; 47: 1772–1781.
[45] Ashouri Movassagh S, Banitalebi Dehkordi M, Koruji M, Pourmand GhR, Farzaneh P, Ashouri Movassagh S, et al. In vitro spermatogenesis by three-dimensional culture of spermatogonial stem cells on decellularized testicular matrix. Galen Med J 2019; 8: e1565.
[46] Sen Ch, Freund D, Gomperts BN. Three-dimensional models of the lung: Past, present and future: A mini review. Biochem Soc Trans 2022; 50: 1045–1056.
[47] Sato T, Katagiri K, Kojima K, Komeya M, Yao M, Ogawa T. In vitro spermatogenesis in explanted adult mouse testis tissues. PloS One 2015; 10: e0130171.
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