Functional and molecular features of the Id4+ germline stem cell population in mouse testes

Genes and Development

Volumn 28, Issue 12, 2014, Pages 1351-1362

  Chan, Frieda ^a   Oatley, Melissa J ^a   Kaucher, Amy V ^a   Yang, Qi En ^a   Bieberich, Charles J ^b   Shashikant, Cooduvalli S ^c   Oatley, Jon M ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Germline stem cell; Id4; Spermatogonia; Spermatogonial stem cell; Transcriptome

Indexed keywords

GREEN FLUORESCENT PROTEIN; INHIBITOR OF DIFFERENTIATION 4; INHIBITOR OF DIFFERENTIATION PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; GENE; GERMLINE STEM CELL; MALE; MOUSE; NONHUMAN; PERINATAL DEVELOPMENT; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RNA SEQUENCE; SEMINIFEROUS TUBULE; SPERMATOGONIUM; TESTIS;

GERMLINE STEM CELL; ID4; SPERMATOGONIA; SPERMATOGONIAL STEM CELL; TRANSCRIPTOME;

ANIMALS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; GREEN FLUORESCENT PROTEINS; INHIBITOR OF DIFFERENTIATION PROTEINS; MALE; MICE; MICE, TRANSGENIC; SPERMATOGENESIS; SPERMATOGONIA; STEM CELLS; TESTIS; TRANSCRIPTOME;

EID: 84902496118     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.240465.114     Document Type: Article

References (45)

1. Arnold K, Sarkar A, Yram MA, Polo JM, Bronson R, Sengupta S, Seandel M, Geijsen N, Hochedlinger K. 2011. Sox2(+) adult stem and progenitor cells are important for tissue regeneration and survival of mice. Cell Stem Cell 9: 317-329.
2. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, et al. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007.
3. Bentley KL, Shashikant CS, Wang W, Ruddle NH, Ruddle FH. 2010. A yeast-based recombinogenic targeting toolset for transgenic analysis of human disease genes. Ann N Y Acad Sci 1207: E58-E68.
4. Brinster RL. 2002. Germline stem cell transplantation and transgenesis. Science 296: 2174-2176.
5. Brinster RL. 2007. Male germline stem cells: from mice to men. Science 316: 404-405.
6. Brinster RL, Avarbock MR. 1994. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci 91: 11303-11307.
7. Brinster RL, Nagano M. 1998. Spermatogonial stem cell transplantation, cryopreservation and culture. Semin Cell Dev Biol 9: 401-409.
8. Brinster RL, Zimmermann JW. 1994. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci 91: 11298-11302.
9. Chiarini-Garcia H, Hornick JR, Griswold MD, Russell LD. 2001. Distribution of type A spermatogonia in the mouse is not random. Biol Reprod 65: 1179-1185.
10. Chiarini-Garcia H, Raymer AM, Russell LD. 2003. Non-random distribution of spermatogonia in rats: evidence of niches in the seminiferous tubules. Reproduction 126: 669-680.
11. de Rooij DG. 1998. Stem cells in the testis. Int J Exp Pathol 79: 67-80.
12. de Rooij DG, Russell LD. 2000. All you wanted to know about spermatogonia but were afraid to ask. J Androl 21: 776-798.
13. Drumond AL, Meistrich ML, Chiarini-Garcia H. 2011. Sper-matogonial morphology and kinetics during testis development in mice: a high-resolution light microscopy approach. Reproduction 142: 145-155.
14. Du Y, Yip HK. 2011. The expression and roles of inhibitor of DNA binding helix-loop-helix proteins in the developing and adult mouse retina. Neuroscience 175: 367-379.
15. Gassei K, Orwig KE. 2013. SALL4 expression in gonocytes and spermatogonial clones of postnatal mouse testes. PLoS ONE 8: e53976.
16. Griswold MD, Oatley JM. 2013. Concise review: defining characteristics of mammalian spermatogenic stem cells. Stem Cells 31: 8-11.
17. Handel MA, Eppig JJ. 1979. Sertoli cell differentiation in the testes of mice genetically deficient in germ cells. Biol Reprod 20: 1031-1038.
18. Huckins C. 1971. The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation and maturation. Anat Rec 169: 533-557.
19. Ishii K, Kanatsu-Shinohara M, Shinohara T. 2014. Cell-cycle-dependent colonization of mouse spermatogonial stem cells after transplantation into seminiferous tubules. J Reprod Dev 60: 37-46.
20. Jeon HM, Jin X, Lee JS, Oh SY, Sohn YW, Park HJ, Joo KM, Park WY, Nam DH, DePinho RA, et al. 2008. Inhibitor of differentiation 4 drives brain tumor-initiating cell genesis through cyclin E and notch signaling. Genes Dev 22: 2028-2033.
21. Kaucher AV, Oatley MJ, Oatley JM. 2012. NEUROG3 is a critical downstream effector for STAT3-regulated differentiation of mammalian stem and progenitor spermatogonia. Biol Reprod 86: 164.
22. Kubota H, Avarbock MR, Brinster RL. 2004. Growth factors essential for self-renewal and expansion of mouse spermato-gonial stem cells. Proc Natl Acad Sci 101: 16489-16494.
23. Kuijk EW, de Gier J, Lopes SM, Chambers I, van Pelt AM, Colenbrander B, Roelen BA. 2010. A distinct expression pattern in mammalian testes indicates a conserved role for NANOG in spermatogenesis. PLoS ONE 5: e10987.
24. Lesch BJ, Page DC. 2012. Genetics of germ cell development. Nat Rev Genet 13: 781-794.
25. Lok D, Jansen MT, de Rooij DG. 1983. Spermatogonial multiplication in the Chinese hamster. II. Cell cycle properties of undifferentiated spermatogonia. Cell Tissue Kinet 16: 19-29.
26. Nagano MC. 2003. Homing efficiency and proliferation kinetics of male germ line stem cells following transplantation in mice. Biol Reprod 69: 701-707.
27. Nakagawa T, Nabeshima Y, Yoshida S. 2007. Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev Cell 12: 195-206.
28. Nakagawa T, Sharma M, Nabeshima Y, Braun RE, Yoshida S. 2010. Functional hierarchy and reversibility within the murine spermatogenic stem cell compartment. Science 328: 62-67.
29. Oakberg EF. 1956. Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat 99: 507-516.
30. Oakberg EF. 1971. Spermatogonial stem-cell renewal in the mouse. Anat Rec 169: 515-531.
31. Oatley JM, Brinster RL. 2008. Regulation of spermatogonial stem cell self-renewal in mammals. Annu Rev Cell Dev Biol 24: 263-286.
32. Oatley JM, Brinster RL. 2012. The germline stem cell niche unit in mammalian testes. Physiol Rev 92: 577-595.
33. Oatley JM, Avarbock MR, Telaranta AI, Fearon DT, Brinster RL. 2006. Identifying genes important for spermatogonial stem cell self-renewal and survival. Proc Natl Acad Sci 103: 9524-9529.
34. Oatley JM, Oatley MJ, Avarbock MR, Tobias JW, Brinster RL. 2009. Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal. Development 136: 1191-1199.
35. Oatley MJ, Kaucher AV, Racicot KE, Oatley JM. 2011a. Inhibitor of DNA binding 4 is expressed selectively by single sper-matogonia in the male germline and regulates the self-renewal of spermatogonial stem cells in mice. Biol Reprod 85: 347-356.
36. Oatley MJ, Racicot KE, Oatley JM. 2011b. Sertoli cells dictate spermatogonial stem cell niches in the mouse testis. Biol Reprod 84: 639-645.
37. Shashikant CS, Bieberich CJ, Belting HG, Wang JC, Borbely MA, Ruddle FH. 1995. Regulation of Hoxc-8 during mouse embryonic development: identification and characterization of critical elements involved in early neural tube expression. Development 121: 4339-4347.
38. Suzuki H, Sada A, Yoshida S, Saga Y. 2009. The heterogeneity of spermatogonia is revealed by their topology and expression of marker proteins including the germ cell-specific proteins Nanos2 and Nanos3. Dev Biol 336: 222-231.
39. Tegelenbosch RA, de Rooij DG. 1993. A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutat Res 290: 193-200.
40. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562-578.
41. van Bragt MP, Roepers-Gajadien HL, Korver CM, Bogerd J, Okuda A, Eggen BJ, de Rooij DG, van Pelt AM. 2008. Expression of the pluripotency marker UTF1 is restricted to a subpopulation of early A spermatogonia in rat testis. Reproduction 136: 33-40.
42. Wang D, Zhuang L, Gao B, Shi CX, Cheung J, Liu M, Jin T, Wen XY. 2008. The Blimp-1 gene regulatory region directs EGFP expression in multiple hematopoietic lineages and testis in mice. Transgenic Res 17: 193-203.
43. Yoshida S, Sukeno M, Nabeshima Y. 2007. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 317: 1722-1726.
44. Yun K, Mantani A, Garel S, Rubenstein J, Israel MA. 2004. Id4 regulates neural progenitor proliferation and differentiation in vivo. Development 131: 5441-5448
45. Zheng K, Wu X, Kaestner KH, Wang PJ. 2009. The pluripotency factor LIN28 marks undifferentiated spermatogonia in mouse. BMC Dev Biol 9: 38.