Models and Molecular Markers of Spermatogonial Stem Cells in Vertebrates: To Find Models in Nonmammals

Overview

Journal Stem Cells Int

Publisher Wiley

Specialty Cell Biology

Date 2022 Jun 10

PMID 35685306

Authors

Hyuk Song

Hyun-Jung Park

Won-Young Lee

Kyung Hoon Lee

Affiliations

Soon will be listed here.

Abstract

Spermatogonial stem cells (SSCs) are the germline stem cells that are essential for the maintenance of spermatogenesis in the testis. However, it has not been sufficiently understood in amphibians, reptiles, and fish because numerous studies have been focused mainly on mammals. The aim of this review is to discuss scientific ways to elucidate SSC models of nonmammals in the context of the evolution of testicular organization since rodent SSC models. To further understand the SSC models in nonmammals, we point out common markers of an SSC pool (undifferentiated spermatogonia) in various types of testes where the kinetics of the SSC pool appears. This review includes the knowledge of (1) common molecular markers of vertebrate type A spermatogonia including putative SSC markers, (2) localization of the markers on the spermatogonia that have been reported in previous studies, (3) highlighting the most common markers in vertebrates, and (4) suggesting ways of finding SSC models in nonmammals.

Citing Articles

Immunohistochemical Characterization of Spermatogenesis in the Ascidian .

Sakurai H, Shiba K, Takamura K, Inaba K Cells. 2024; 13(22).

PMID: 39594612 PMC: 11592721. DOI: 10.3390/cells13221863.

Spermatogonial stem cell technologies: applications from human medicine to wildlife conservation†.

Damyanova K, Nixon B, Johnston S, Gambini A, Benitez P, Lord T Biol Reprod. 2024; 111(4):757-779.

PMID: 38993049 PMC: 11473898. DOI: 10.1093/biolre/ioae109.

The RNA-binding protein Adad1 is necessary for germ cell maintenance and meiosis in zebrafish.

Islam K, Ajao A, Venkataramani K, Rivera J, Pathania S, Henke K PLoS Genet. 2023; 19(8):e1010589.

PMID: 37552671 PMC: 10437952. DOI: 10.1371/journal.pgen.1010589.

Identification of fish spermatogenic cells through high-throughput immunofluorescence against testis with an antibody set.

Ye D, Liu T, Li Y, Wang Y, Hu W, Zhu Z Front Endocrinol (Lausanne). 2023; 14:1044318.

PMID: 37077350 PMC: 10106697. DOI: 10.3389/fendo.2023.1044318.

A review of the reproductive system in anuran amphibians.

Mendez-Tepepa M, Morales-Cruz C, Garcia-Nieto E, Anaya-Hernandez A Zoological Lett. 2023; 9(1):3.

PMID: 36782341 PMC: 9926845. DOI: 10.1186/s40851-023-00201-0.

References

Clermont Y . Two classes of spermatogonial stem cells in the monkey (Cercopithecus aethiops). Am J Anat. 1969; 126(1):57-71. DOI: 10.1002/aja.1001260106. View

Bosseboeuf A, Gautier A, Auvray P, Mazan S, Sourdaine P . Characterization of spermatogonial markers in the mature testis of the dogfish (Scyliorhinus canicula L.). Reproduction. 2013; 147(1):125-39. DOI: 10.1530/REP-13-0316. View

Zhao Y, Yang Z, Wang Y, Luo Y, Da F, Tao W . Both Gfrα1a and Gfrα1b Are Involved in the Self-renewal and Maintenance of Spermatogonial Stem Cells in Medaka. Stem Cells Dev. 2018; . DOI: 10.1089/scd.2018.0177. View

Shang M, Su B, Lipke E, Perera D, Li C, Qin Z . Spermatogonial stem cells specific marker identification in channel catfish, Ictalurus punctatus and blue catfish, I. furcatus. Fish Physiol Biochem. 2015; 41(6):1545-56. DOI: 10.1007/s10695-015-0106-1. View

Janzen F, Phillips P . Exploring the evolution of environmental sex determination, especially in reptiles. J Evol Biol. 2006; 19(6):1775-84. DOI: 10.1111/j.1420-9101.2006.01138.x. View

Uribe M, Grier H, Mejia-Roa V . Comparative testicular structure and spermatogenesis in bony fishes. Spermatogenesis. 2015; 4(3):e983400. PMC: 4581063. DOI: 10.4161/21565562.2014.983400. View

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

Fayomi A, Orwig K . Spermatogonial stem cells and spermatogenesis in mice, monkeys and men. Stem Cell Res. 2018; 29:207-214. PMC: 6010318. DOI: 10.1016/j.scr.2018.04.009. View

Kawasaki T, Imura F, Nakada A, Kubota H, Sakamaki K, Abe S . Functional demonstration of the ability of a primary spermatogonium as a stem cell by tracing a single cell destiny in Xenopus laevis. Dev Growth Differ. 2006; 48(8):525-35. DOI: 10.1111/j.1440-169X.2006.00890.x. View

10.

Takeuchi Y, Yoshizaki G, Takeuchi T . Biotechnology: surrogate broodstock produces salmonids. Nature. 2004; 430(7000):629-30. DOI: 10.1038/430629a. View

11.

Schartl M, Schmid M, Nanda I . Dynamics of vertebrate sex chromosome evolution: from equal size to giants and dwarfs. Chromosoma. 2015; 125(3):553-71. DOI: 10.1007/s00412-015-0569-y. View

12.

Yoshida S, Sukeno M, Nabeshima Y . A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science. 2007; 317(5845):1722-6. DOI: 10.1126/science.1144885. View

13.

Marshall Graves J . Avian sex, sex chromosomes, and dosage compensation in the age of genomics. Chromosome Res. 2014; 22(1):45-57. DOI: 10.1007/s10577-014-9409-9. View

14.

Bakst M, Akuffo V, Trefil P, Brillard J . Morphological and histochemical characterization of the seminiferous epithelial and Leydig cells of the turkey. Anim Reprod Sci. 2006; 97(3-4):303-13. DOI: 10.1016/j.anireprosci.2006.02.009. View

15.

Karl J, Capel B . Sertoli cells of the mouse testis originate from the coelomic epithelium. Dev Biol. 1998; 203(2):323-33. DOI: 10.1006/dbio.1998.9068. View

16.

Russell L . Genetics of mammalian sex chromosomes. Science. 1961; 133(3467):1795-803. DOI: 10.1126/science.133.3467.1795. View

17.

Shikina S, Yoshizaki G . Improved in vitro culture conditions to enhance the survival, mitotic activity, and transplantability of rainbow trout type a spermatogonia. Biol Reprod. 2010; 83(2):268-76. DOI: 10.1095/biolreprod.109.082123. View

18.

Makela J, Hobbs R . Molecular regulation of spermatogonial stem cell renewal and differentiation. Reproduction. 2019; 158(5):R169-R187. DOI: 10.1530/REP-18-0476. View

19.

Yoshida S . From cyst to tubule: innovations in vertebrate spermatogenesis. Wiley Interdiscip Rev Dev Biol. 2015; 5(1):119-31. PMC: 5049625. DOI: 10.1002/wdev.204. View

20.

Iskandar D, Evans B, McGuire J . A novel reproductive mode in frogs: a new species of fanged frog with internal fertilization and birth of tadpoles. PLoS One. 2015; 9(12):e115884. PMC: 4281041. DOI: 10.1371/journal.pone.0115884. View