Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-24T03:08:50.608Z Has data issue: false hasContentIssue false

Chapter 31 - Spermatogonial Stem Cell Culture and the Future of Germline Gene Editing

from Section 4 - Laboratory Evaluation and Treatment of Male Infertility

Published online by Cambridge University Press:  06 December 2023

By
Xichen Nie ,
Jan-Bernd Stukenborg  and
Jingtao Guo
Edited by
Douglas T. Carrell ,
Alexander W. Pastuszak  and
James M. Hotaling
Douglas T. Carrell
Affiliation:
Utah Center for Reproductive Medicine
Alexander W. Pastuszak
Affiliation:
University of Utah
James M. Hotaling
Affiliation:
Utah Center for Reproductive Medicine
Get access

Summary

Human spermatogonial stem cells (hSSCs), the only type of germline stem cells in adult men, are responsible to ensure lifetime-long sperm production in men after sex maturation. As the starting point of spermatogenesis, this cell type delicately balances its self-renewal and differentiation, which is essential for spermatogenesis to proceed continuously. A deep and systematic understanding of hSSCs is critical for treating testis-related pathology such as male infertility and testicular germ cell tumor. In this chapter, we provide a systematic review of our previous and current understanding of hSSCs, as well as the advancement of ex vivo systems to culture human germline. Ultimately, the successful establishment of an hSSC-based human germline culture system will not only greatly benefit the study of human germ cell biology by serving as a useful platform, but also provide potential therapeutic options to treat male infertility and preserve fertility for childhood cancer patients.

Keywords

spermatogonial stem cellspermatogenesismale infertility
Type
Chapter
Information
Men's Reproductive and Sexual Health Throughout the Lifespan
An Integrated Approach to Fertility, Sexual Function, and Vitality
 , pp. 244 - 250
Publisher: Cambridge University Press
Print publication year: 2023

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agarwal, A, Mulgund, A, Hamada, A, Chyatte, MR. A unique view on male infertility around the globe. Reprod Biol Endocrinol. 2015;13:37.CrossRefGoogle ScholarPubMed
Esteves, SC. Clinical management of infertile men with nonobstructive azoospermia. Asian J Androl. 2015;17(3):459–470.Google Scholar
Foresta, C, Garolla, A, Bartoloni, L, Bettella, A, Ferlin, A. Genetic abnormalities among severely oligospermic men who are candidates for intracytoplasmic sperm injection. J Clin Endocrinol Metab. 2005;90(1):152–156.CrossRefGoogle ScholarPubMed
Georgiou, I, Syrrou, M, Pardalidis, N, et al. Genetic and epigenetic risks of intracytoplasmic sperm injection method. Asian J Androl. 2006;8(6):643–673.Google Scholar
O’Flynn O’Brien, KL, Varghese, AC, Agarwal, A. The genetic causes of male factor infertility: a review. Fertil Steril. 2010;93(1):1–12.CrossRefGoogle ScholarPubMed
Gassei, K, Orwig, KE. Experimental methods to preserve male fertility and treat male infertility. Fertil Steril. 2016;105(2):256–266.Google Scholar
Lim, J, Goriely, A, Turner, GD, et al. OCT2, SSX and SAGE1 reveal the phenotypic heterogeneity of spermatocytic seminoma reflecting distinct subpopulations of spermatogonia. J Pathol. 2011;224(4):473–483.Google Scholar
Looijenga, LHJ, Hersmus, R, Gillis, AJM, et al. Genomic and expression profiling of human spermatocytic seminomas: primary spermatocyte as tumorigenic precursor and DMRT1 as candidate chromosome 9 gene. Cancer Res. 2006;66(1):290–302.CrossRefGoogle ScholarPubMed
Clermont, Y. Renewal of spermatogonia in man. Am J Anat. 1966;118(2):509–524.Google Scholar
Clermont, Y. Spermatogenesis in man: a study of the spermatogonial population. Fertil Steril. 1966;17(6):705–721.Google Scholar
Clermont, Y. Two classes of spermatogonial stem cells in the monkey (Cercopithecus aethiops). Am J Anat. 1969;126(1):57–71.Google Scholar
Grisanti, L, Falciatori, I, Grasso, M, et al. Identification of spermatogonial stem cell subsets by morphological analysis and prospective isolation. Stem Cells. 2009;27(12):3043–3052.Google Scholar
Altman, E, Yango, P, Moustafa, R, Smith, JF, Klatsky, PC, Tran, ND. Characterization of human spermatogonial stem cell markers in fetal, pediatric, and adult testicular tissues. Reproduction. 2014;148(4):417–427.Google Scholar
Kubota, H, Avarbock, MR, Brinster, RL. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A. 2004;101(47):16489–16494.Google Scholar
Brinster, RL, Avarbock, MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci U S A. 1994;91(24):11303–11307.Google Scholar
Brinster, RL, Zimmermann, JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A. 1994;91(24):11298–11302.Google Scholar
Guo, J, Grow, EJ, Mlcochova, H, et al. The adult human testis transcriptional cell atlas. Cell Res. 2018;28(12):1141.Google Scholar
Yoshida, S, Sukeno, M, Nakagawa, T, et al. The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development. 2006;133(8):1495–1505.Google Scholar
Tegelenbosch, RA, de Rooij, DG. A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutat Res. 1993;290(2):193–200.Google Scholar
Hara, K, Nakagawa, T, Enomoto, H, et al. Mouse spermatogenic stem cells continually interconvert between equipotent singly isolated and syncytial states. Cell Stem Cell. 2014;14(5):658–672.Google Scholar
Helsel, AR, Yang, Q-E, Oatley, MJ, Lord, T, Sablitzky, F, Oatley, JM. ID4 levels dictate the stem cell state in mouse spermatogonia. Dev Camb Engl. 2017;144(4):624–634.Google Scholar
Honaramooz, A, Snedaker, A, Boiani, M, Schöler, H, Dobrinski, I, Schlatt, S. Sperm from neonatal mammalian testes grafted in mice. Nature. 2002;418(6899):778–781.Google Scholar
Liu, Z, Nie, Y-H, Zhang, C-C, et al. Generation of macaques with sperm derived from juvenile monkey testicular xenografts. Cell Res. 2016;26(1):139–142.Google Scholar
Wistuba, J, Mundry, M, Luetjens, CM, Schlatt, S. Cografting of hamster (Phodopus sungorus) and marmoset (Callithrix jacchus) testicular tissues into nude mice does not overcome blockade of early spermatogenic differentiation in primate grafts. Biol Reprod. 2004;71(6):2087–2091.Google Scholar
Goossens, E, Geens, M, De Block, G, Tournaye, H. Spermatogonial survival in long-term human prepubertal xenografts. Fertil Steril. 2008;90(5):2019–2022.Google Scholar
Fayomi, AP, Peters, K, Sukhwani, M, et al. Autologous grafting of cryopreserved prepubertal rhesus testis produces sperm and offspring. Science. 2019;363(6433):1314–1319.Google Scholar
Dovey, SL, Valli, H, Hermann, BP, et al. Eliminating malignant contamination from therapeutic human spermatogonial stem cells. J Clin Invest. 2013;123(4):1833–1843.Google Scholar
Hou, M, Andersson, M, Zheng, C, Sundblad, A, Söder, O, Jahnukainen, K. Immunomagnetic separation of normal rat testicular cells from Roser’s T-cell leukaemia cells is ineffective. Int J Androl. 2009;32(1):66–73.Google Scholar
Kanatsu-Shinohara, M, Ogonuki, N, Inoue, K, et al. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod. 2003;69(2):612–616.Google Scholar
Sadri-Ardekani, H, Mizrak, SC, van Daalen, SKM, et al. Propagation of human spermatogonial stem cells in vitro. JAMA. 2009;302(19):2127–2134.Google Scholar
Sadri-Ardekani, H, Akhondi, MA, van der Veen, F, Repping, S, van Pelt, AMM. In vitro propagation of human prepubertal spermatogonial stem cells. JAMA. 2011;305(23):2416–2418.Google Scholar
Dong, L, Kristensen, SG, Hildorf, S, et al. Propagation of spermatogonial stem cell-like cells from infant boys. Front Physiol. 2019;10:1155.Google Scholar
Sato, T, Katagiri, K, Gohbara, A, et al. In vitro production of functional sperm in cultured neonatal mouse testes. Nature. 2011;471(7339):504–507.Google Scholar
Medrano, JV, Vilanova-Pérez, T, Fornés-Ferrer, V, et al. Influence of temperature, serum, and gonadotropin supplementation in short- and long-term organotypic culture of human immature testicular tissue. Fertil Steril. 2018;110(6):1045–1057.e3.Google Scholar
de Michele, F, Poels, J, Vermeulen, M, et al. Haploid germ cells generated in organotypic culture of testicular tissue from prepubertal boys. Front Physiol. 2018;9:1413.CrossRefGoogle ScholarPubMed
Alves-Lopes, JP, Söder, O, Stukenborg, J-B. Testicular organoid generation by a novel in vitro three-layer gradient system. Biomaterials. 2017;130:76–89.CrossRefGoogle ScholarPubMed
Mulder, CL, Zheng, Y, Jan, SZ, et al. Spermatogonial stem cell autotransplantation and germline genomic editing: a future cure for spermatogenic failure and prevention of transmission of genomic diseases. Hum Reprod Update. 2016;22(5):561–573.CrossRefGoogle ScholarPubMed
Shimizu, T, Shiohara, M, Tai, T, Nagao, K, Nakajima, K, Kobayashi, H. Derivation of integration‐free iPSCs from a Klinefelter syndrome patient. Reprod Med Biol. 2015;15(1):35–43.Google Scholar
Zhao, Y, Ye, S, Liang, D, et al. In vitro modeling of human germ cell development using pluripotent stem cells. Stem Cell Rep. 2018;10(2):509–523.CrossRefGoogle ScholarPubMed
Fujimoto, T, Miyayama, Y, Fuyuta, M. The origin, migration and fine morphology of human primordial germ cells. Anat Rec. 1977;188(3):315–330.Google Scholar
Hiller, M, Liu, C, Blumenthal, PD, Gearhart, JD, Kerr, CL. Bone morphogenetic protein 4 mediates human embryonic germ cell derivation. Stem Cells Dev. 2011;20(2):351–361.Google Scholar
Sasaki, K, Yokobayashi, S, Nakamura, T, et al. Robust in vitro induction of human germ cell fate from pluripotent stem cells. Cell Stem Cell. 2015;17(2):178–194.CrossRefGoogle ScholarPubMed
Clark, AT, Bodnar, MS, Fox, M, et al. Spontaneous differentiation of germ cells from human embryonic stem cells in vitro. Hum Mol Genet. 2004;13(7):727–739.CrossRefGoogle ScholarPubMed
Fox, N, Damjanov, I, Martinez-Hernandez, A, Knowles, BB, Solter, D. Immunohistochemical localization of the early embryonic antigen (SSEA-1) in postimplantation mouse embryos and fetal and adult tissues. Dev Biol. 1981;83(2):391–398.CrossRefGoogle ScholarPubMed
Mouka, A, Tachdjian, G, Dupont, J, Drévillon, L, Tosca, L. In vitro gamete differentiation from pluripotent stem cells as a promising therapy for infertility. Stem Cells Dev. 2016;25(7):509–521.Google Scholar
Koopman, P, Münsterberg, A, Capel, B, Vivian, N, Lovell-Badge, R. Expression of a candidate sex-determining gene during mouse testis differentiation. Nature. 1990;348(6300):450–452.Google Scholar
Geens, M, Sermon, KD, Van de Velde, H, Tournaye, H. Sertoli cell-conditioned medium induces germ cell differentiation in human embryonic stem cells. J Assist Reprod Genet. 2011;28(5):471–480.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×