Current Approach to Spermatogonial Stem Cells in Vitro Maturation

Yıl 2022, Cilt: 12 Sayı: 1, 268 - 273, 30.03.2022

Gülnaz Kervancıoğlu , Zeliha Karadeniz , Elif Kervancıoğlu

https://doi.org/10.33808/clinexphealthsci.918781

Öz

The studies conducted to determine the stage of its usability in prospective fertility restoration of testicular tissues taken from prepubertal patients undergoing oncology treatment were screened. In addition, the current status of spermatogonial stem cell cultures, testicular tissue cultures, and testicular organoid research and their potential in fertility restoration were examined.
Spermatogonial stem cells are only found in prepubertal testicular tissue. Germinal serial cells are not found. Since spermatozoa are not produced in this period, spermatogonial stem cells are stored by freezing in the form of testicular tissue pieces or testicular cell suspension. It is not yet clear how to ensure the maturation of freeze-thawed or fresh spermatogonial stem cells for fertility reconstruction when it is necessary.
The spermatogonial stem cells can be placed in their original niche by maintaining the vitality of the seminiferous tubules in vitro. Then, it can be transplanted to the recipient.
Many hypotheses suggested that that maturation can be achieved via such as two-dimensional, three-dimensional tissue cultures. To ensure differentiation and proliferation of spermatogonial stem cells in three-dimensional cultures, it is necessary to ensure the long-term viability of
the seminiferous tubules in vitro or solve creating an environment similar to the seminiferous tubules niche. In this review article, spermatozoa could be obtained in three-dimensional culture. However, the application of this system in different laboratories and the provision of the setup involves various difficulties. Standard organoids and organoid scaffolds that can be developed for three-dimensional cultures seem to be more preferable.

Anahtar Kelimeler

In vitro maturation, three-dimensional culture, testicular organoid, seminiferous tubules niche

Kaynakça

• [1] Goossens E, Jahnukainen K, Mitchell RT, van Pelt A, Pennings G, Rives N, Poels J, Wyns C, Lane S, Rodriguez-Wallberg KA, Rives A, Valli-Pulaski H, Steimer S, Kliesch S, Braye A, Andres MM, Medrano J, Ramos L, Kristensen SG, Andersen CY, Bjarnason R, Orwig KE, Neuhaus N, Stukenborg JB. Fertility preservation in boys: recent developments and new insights. Hum Reprod Open 2020; 6 (3):1-18.
• [2] Romao RL, Lorenzo AJ. Fertility preservation options for children and adolescents with cancer. Can Uro Assoc J. 2017;11 (1-2Suppl1):97–102.
• [3] Hermann BP, Sukhwani M, Winkler F, Pascarella JN, Peters KA, Sheng Y, Valli H, Rodriguez M, Ezzelarab M, Dargo G, Peterson K, Masterson K, Ramsey C, Ward T, Lienesch M, Volk A, Cooper DK, Thomson AW, Kiss JE, Penedo MC, Schatten GP, Mitalipov S, Orwig KE. Spermatogonial stem cell transplantation into Rhesus testes regenerates spermatogenesis producing functional sperm. Cell Stem Cell 2012; 11 (5):715-726.
• [4] Jahnukainen K, Stukenborg JB. Present and future prospects of male fertility preservation for children and adolescents. J Clin Endocrinol Metab. 2012; 97 (12):4341–4351.
• [5] Kanatsu-Shinohara M, Morimoto H, Shinohara T. Fertility of male germline stem cells following spermatogonial transplantation in infertile mouse models. Biol Reprod. 2016; 94 (5):112.
• [6] Sato T, Katagiri K, Kubota Y, Ogawa T. In vitro sperm production from mouse spermatogonial stem cell lines using an organ culture method. Nat Protoc. 2013; 8(11): 2098-2104.
• [7] Lancaster MA, Knoblich JA. Organogenesis in a dish: modeling development and disease using organoid technologies. Science 2014; 345 (6194).
• [8] Alves-Lopes JP, Söder O, Stukenborg JB. Testicular organoid generation by a novel in vitro threelayer gradient system. Biomaterials 2017; 130 (2017):76-89.
• [9] Drumond AL, Meistrich ML, Chiarini-Garcia H. Spermatogonial morphology and kinetics during testis development in mice: a high-resolution light microscopy approach. Reproduction 2011; 142(1):145–155.
• [10] Kervancioglu G, Demirci EK. Transformation of primordial stem cells into spermatozoa in male gonad. Tıp Fak Klinikleri 2018;1 (3):11-16.
• [11] McGuinness MP, Orth JM. Reinitiation of gonocyte mitosis and movement of gonocytes to the basement membrane in testes of newborn rats in vivo and in vitro. Anat Rec. 1992; 233 (4): 527–537.
• [12] Potter SJ, DeFalco T. Role of the testis interstitial compartment in spermatogonial stem cell function. Reproduction 2017;153 (4):151-162.
• [13] Wang X. Stem cells in tissues, organoids, and cancers. Cell Mol Life Sci. 2019; 76 (20):4043-4070.
• [14] Tung PS, Skinner MK, Fritz IB. Cooperativity between Sertoli cells and peritubuler myoid cells in the formation of the basal lamina in the seminiferous tubule. Ann NY Acad Sci. 1984; 438 (1): 435-446.
• [15] Oatley JM, Brinster RL. The germline stem cell niche unit in mammalian testes. Physiol Rev. 2012; 92 (2):577–595.
• [16] Kanatsu-Shinohara M, Ogonuki N, Inoue K, Ogura A, Toyokuni S, Shinohara T. Restoration of fertility in infertile mice by transplantation of cryopreserved male germline stem cells. Hum Reprod. 2003; 18 (12):2660–2667.
• [17] Kanatsu-Shinohara M, Miki H, Inoue K, Ogonuki N, Toyokuni S, Ogura A, Shinohara T. Germline niche transplantation restores fertility in infertile mice. Hum Reprod. 2005; 20 (9):2376–2382.
• [18] Oatley MJ, Racicot KE, Oatley JM. Sertoli cells dictate spermatogonial stem cell niches in the mouse testis. Biol Reprod. 2011; 84 (4): 639–645.
• [19] Meng X, Indahl M, Hyvönen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, Pichel JG, Westphal H, Saarma M, Sariola H. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 2000; 287 (5457):1489-1493.
• [20] Tadokoro Y, Yomogida K, Ohta H, Tohda A, Nishimune Y. Homeostatic regulation of germinal stem cell proliferation by the GDNF/FSH pathway. Mech Dev. 2002; 113 (1):29–39.
• [21] Spinnler K, Köhn FM, Schwarzer U, Mayerhofer A. Glial cell line-derived neurotrophic factor is constitutively produced by human testicular peritubular cells and may contribute to the spermatogonial stem cell niche in man. Hum Reprod. 2010; 25 (9):2181–2187.
• [22] Oatley JM, Oatley MJ, Avarbock MR, Tobias JW, Brinster RL. Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal. Development 2009; 136 (7):1191-1199.
• [23] Phillips BT, Gassei K, Orwig KE. Spermatogonial stem cell regulation and spermatogenesis. Phil Trans R Soc Lond B Biol Sci. 2010; 365 (1546):1663-1678.
• [24] Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation. Proc Nati Acad Sci USA 1994; 91 (24):11298-11302.
• [25] Brinster RL, Avarbock MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci USA 1994; 91 (24):11303-11307.
• [26] Avarbock MR, Brinster CJ, Brinster RL. Reconstitution of spermatogenesis from frozen spermatogonial stem cells. Nat Med. 1996; 2(6): 693–696.
• [27] Shinora T, Orwig KE, Avarbock MR, Brinster RL. Remodeling of the postnatal mouse testis is accompained by dramatic changes in stem cell number and niche accessibility. Proc. Natl Acad Sci USA 2001; 98 (11): 6186-6191.
• [28] Kanatsu-Shinohara M, Inoue K, Miki H, Ogonuki N, Takehashi M, Morimoto T, Ogura A, Shinohara T. Clonal origin of germ cell colonies after spermatogonial transplantasyon in mice. Biol Reprod. 2006; 75 (1):68-74.
• [29] Honaramooz A, Behboodi E, Megee SO, Overton SA, Galantino-Homer H, Echelard Y, Dobrinski I. Fertility and germline transmission of donor haplotype following germ cell tranplantation in immunocompetent goats. Biol Reprod 2003; 69 (4):1260-1264.
• [30] Lee YM, Jung JG, Kim JN, Park TS, Kim TM, Shin SS, Kang DK, Lim JM, Han JY. A testis-mediated germline chimera production based on transfer of chicken testicular cells directly into heterologous testis. Biol Reprod 2006; 75 (3): 380-386.
• [31] Yeh JR, Zhang X, Nagano M.M.C. Establishment of a shorttherm in vitro assay for Mouse spermatogonial stem cells. Biol Reprod 2007; 77 (5):897-904.
• [32] Russell LD, Ettlin RA, Hikim AP. Histological and Histopathological Evaluation of the Testis. 1st Ed. Cache River Press: Clearwater Florida; 1990;1-40.
• [33] Zhang X, Ebata KT, Nagano M. Genetic analysis of the clonal origin of regenerating spermatogenesis following transplantation. Biol Reprod 2003; 69 (6):1872-1878.
• [34] Takashima S, Shinohara T. Culture and transplantation of spermatogonial stem cells. Stem Cell Res 2018; 29 (2018): 46- 55.
• [35] Steinberger A, Steinberger E, Perloff WH. Mammalian testes in organ culture. Exp Cell Res 1964;36 (1964): 19–27.
• [36] Tesarik J, Bahceci M, Ozcan C, Greco E, Mendoza C. Restoration of fertility by in vitro spermatogenesis. Lancet 1999; 353 (9152): 555–556.
• [37] Sousa M, Cremades N, Alves C, Silva J, Barros A. Developmental potential of human spermatogenic cells co-cultured with Sertoli cells. Hum Reprod. 2002; 17 (1): 161–172.
• [38] Lee DR, Kim KS, Yang YH, Oh HS, Lee SH, Chung TG, Cho JH, Kim HJ, Yoon TK, Cha KY. Isolation of male germ stem cell-like cells from testicular tissue of non-obstructive azoospermic patients and differentiation into haploid male germ cells in vitro. Hum Reprod. 2006;21(2):471–476.
• [39] Riboldi M, Rubio C, Pellicer A, Gil-Salom M, Simón C. In vitro production of haploid cells after coculture of CD49fþ with Sertoli cells from testicular sperm extraction in nonobstructive azoospermic patients. Fertil Steril. 2012; 98 (3):580–590.
• [40] Gholamia K, Pourmand G, Koruji M, Sadighigilani M, Navid S, Izadyar F, Abbasi M. Efficiency of colony formation and differentiation of human spermatogenic cells in two different culture systems. Reprod Biol. 2018; 18 (4): 397–403.
• [41] Kanatsu-Shinohara M, Inoue K, Takashima S, Takehashi M, Ogonuki N, Morimoto H, Nagasawa T, Ogura A, Shinohara T. Reconstitution of Mouse spermatogonial stem cell niches in culture. Cell Stem Cell 2012;11(4): 567-578.
• [42] Lee JH, Gye MC, Choi KW, Hong JY, Lee YB, Park DW, Lee SJ, Min CK. In vitro differentiation of germ cells from nonobstructive azoospermic patients using threedimensional culture in a collagen gel matrix. Fertil Steril. 2006; 87 (4): 824-33.
• [43] Sato T, Katagiri K, Gohbara A, Inoue K, Ogonuki N, Ogura A, Kubota Y, Ogawa T. In vitro production of functional sperm in cultured neonatal mouse testes. Nature 2011; 471 (7339):504– 507.
• [44] Sato T, Katagiri K, Yokonishi T, Kubota Y, Inoue K, Ogonuki N, Matoba S, Ogura A, Ogawa T. In vitro production of fertile sperm from murine spermatogonial stem cell lines. Nat Commun. 2011;13 (2): 1-7
• [45] Sato T, Katagiri K, Kubota Y, Ogawa T. In vitro sperm production from mouse spermatogonial stem cell lines using an organ culture method. Nat Protoc. 2013;8 (11):2098-2104. [46] Yokonishi T, Sato T, Katagiri K, Ogawa T. In vitro spermatogenesis using an organ culture technique. Methods Mol Biol. 2013; 927 (2013): 479–488.
• [47] Yokonishi T, Sato T, Komeya M, Katagiri K, Kubota Y, Nakabayashi K, Hata K, Inoue K, Ogonuki N, Ogura A, Ogawa T. Offspring production with sperm grown in vitro from cryopreserved testis tissues. Nat Commun. 2014; 5: 4320.
• [48] Komeya M, Kimura H, Nakamura H, et al. Long-term ex vivo maintenance of testis tissues producing fertile sperm in a microfluidic device. Sci Rep. 2016; 6: 21472.
• [49] de Michele F, Poels J, Weerens L, Petit C, Evrard Z, Ambroise J, Gruson D, Wyns C. Preserved seminiferous tubule integrity with spermatogonial survival and induction of Sertoli and Leydig cell maturation after long-term organotypic culture of prepubertal human testicular tissue. Hum Reprod. 2017; 32 (1):32–45.
• [50] Potter SJ, de Falco T. Role of the testis interstitial compartment in spermatogonial stem cell function. Reproduction 2017;153(4):151-162.
• [51] Zhang J, Hatakeyama H, Eto K, Abe SI. Reconstruction of a seminiferous tubule-like structurein a 3 dimensional culture system of re-aggregated mouseneonatal testicular cells within a collagen matrix. Gen Comp Endocrinol. 2014;205 (2014):121–132.
• [52] Mincheva M, Sandhowe-Klaverkamp R, Wistuba J, Redmann K, Stukenborg JB, Kliesch S, Schlatt S. Reassembly of adult human testicular cells: can testis cord-like structures be created in vitro?. Mol Hum Reprod. 2018; 24 (2):55-63.
• [53] Wang X. Stem cells in tissues, organoids, and cancers. Cell Mol Life Sci. 2019; 76 (20): 4043–4070.
• [54] Alves-Lopes JP, Söder O, Stukenborg JB. Use of a three-layer gradient system of cells for rat testicular organoid generation. Nat Protoc. 2018;13 (2):248-259.
• [55] Pendergraft SS, Sadri-Ardekani H, Atala A, Piskopos CE. Three – dimensional testicular organoid: a novel tool for the study of human spermatogenesis and gonadotoxicity in vitro. Biol Reprod. 2017; 96 (3):720–732.
• [56] Sakib S, Uchida A, Valenzuela-Leon P, Yu Y, Valli-Pulaski H, Orwig K, Ungrin M, Dobrinski I. Formation of organotypic testicular organoids in microwell culture. Biol Reprod. 2019;100 (6):1648-1660.
• [57] Sakib S, Yu Y, Voigt A, Ungrin M, Dobrinski I. Generation of Porcine Testicular Organoids with Testis Specific Architecture using Microwell Culture. J Vis Exp. 2019;(152):10.3791/60387.
• [58] Topraggaleh TR , Valojerdi MR , Montazeri L, zaei Topraggaleh T, Baharvand H. A testis-derived macroporous 3D scaffold as a platform for the generation of mouse testicular organoids. Biomater Sci. 2019;7 (4):1422-1436.