Sox3 functions in a cell-autonomous manner to regulate spermatogonial differentiation in mice

Endocrinology

Volumn 152, Issue 4, 2011, Pages 1606-1615

  Laronda, Monica M ^a   Jameson, J Larry ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS ANTIGEN; DNA BINDING PROTEIN; NEUROGENIN 3; PROTEIN RET; STEM CELL FACTOR RECEPTOR; SYNAPTONEMAL COMPLEX PROTEIN 3; TRANSCRIPTION FACTOR SOX3; UNCLASSIFIED DRUG;

AGING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; GENE DELETION; GENE EXPRESSION; GERM CELL; HISTOLOGY; MALE; MEIOSIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA ANALYSIS; SPERMATOGENESIS; SPERMATOGONIUM; SYNAPTONEMAL COMPLEX; TESTIS; TRANSGENE;

ANIMALS; CELL DIFFERENTIATION; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SOXB1 TRANSCRIPTION FACTORS; SPERMATOGENESIS; SPERMATOGONIA; TESTIS;

EID: 79953232003     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-1249     Document Type: Article

References (50)

1. Bowles J, Schepers G, Koopman P 2000 Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol 227:239-255
2. Uchikawa M, Kamachi Y, Kondoh H 1999 Two distinct subgroups of group B Sox genes for transcriptional activators and repressors: their expression during embryonic organogenesis of the chicken. Mech Dev 84:103-120 (Pubitemid 29331657)
3. Pevny LH, Lovell-Badge R 1997 Sox genes find their feet. Curr Opin Genet Dev 7:338-344 (Pubitemid 27292285)
4. Lefebvre V, Huang W, Harley VR, Goodfellow PN, de Crombrugghe B 1997 SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro α1(II) collagen gene. Mol Cell Biol 17:2336-2346 (Pubitemid 27133320)
5. Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, Ling KW, Sham MH, Koopman P, Tam PP, Cheah KS 1997 SOX9 directly regulates the type-II collagen gene. Nat Genet 16:174-178 (Pubitemid 27240616)
6. Bylund M, Andersson E, Novitch BG, Muhr J 2003 Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat Neurosci 6:1162-1168 (Pubitemid 37346036)
7. Koopman P, Münsterberg A, Capel B, Vivian N, Lovell-Badge R 1990 Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 348:450-452 (Pubitemid 120015087)
8. Wood HB, Episkopou V 1999 Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech Dev 86:197-201
9. Weiss J, Meeks JJ, Hurley L, Raverot G, Frassetto A, Jameson JL 2003 Sox3 is required for gonadal function, but not sex determination, in males and females. Mol Cell Biol 23:8084-8091 (Pubitemid 37377500)
10. Rizzoti K, Lovell-Badge R 2007 SOX3 activity during pharyngeal segmentation is required for craniofacial morphogenesis. Development 134:3437-3448 (Pubitemid 350028363)
11. Koyano S, Ito M, Takamatsu N, Takiguchi S, Shiba T 1997 The Xenopus Sox3 gene expressed in oocytes of early stages. Gene 188:101-107 (Pubitemid 27140008)
12. Yao B, Zhou L, Wang Y, Xia W, Gui JF 2007 Differential expression and dynamic changes of SOX3 during gametogenesis and sex reversal in protogynous hermaphroditic fish. J Exp Zool A Ecol Genet Physiol 307:207-219 (Pubitemid 46524363)
13. Raverot G, Weiss J, Park SY, Hurley L, Jameson JL 2005 Sox3 expression in undifferentiated spermatogonia is required for the progression of spermatogenesis. Dev Biol 283:215-225 (Pubitemid 40828853)
14. Bellvé AR, Cavicchia JC, Millette CF, O'Brien DA, Bhatnagar YM, Dym M 1977 Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J Cell Biol 74:68-85 (Pubitemid 8141486)
15. Russell LD, Ettlin RA, Sinha AM, Hikim ED Clegg RA 1990 Histological and histopathological evaluation of the testis. St. Louis, MO: Cache River Press
16. Yoshida S, Takakura A, Ohbo K, Abe K, Wakabayashi J, Yamamoto M, Suda T, Nabeshima Y 2004 Neurogenin3 delineates the earliest stages of spermatogenesis in the mouse testis. Dev Biol 269:447-458 (Pubitemid 38521110)
17. Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukhwani M, Orwig KE, Wolgemuth DJ, Pandolfi PP 2004 Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 36:653-659 (Pubitemid 38715996)
18. Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL, Griswold MD, de Rooij DG, Braun RE 2004 Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 36:647-652 (Pubitemid 38715995)
19. Meng X, Lindahl 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 2000 Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287:1489-1493 (Pubitemid 30127143)
20. 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
21. Filipponi D, Hobbs RM, Ottolenghi S, Rossi P, Jannini EA, Pandolfi PP, Dolci S 2007 Repression of kit expression by Plzf in germ cells. Mol Cell Biol 27:6770-6781 (Pubitemid 47483628)
22. Hao J, Yamamoto M, Richardson TE, Chapman KM, Denard BS, Hammer RE, Zhao GQ, Hamra FK 2008 Sohlh2 knockout mice are male-sterile because of degeneration of differentiating type A spermatogonia. Stem Cells 26:1587-1597
23. Ballow D, Meistrich ML, Matzuk M, Rajkovic A 2006 Sohlh1 is essential for spermatogonial differentiation. Dev Biol 294:161-167
24. Gallardo T, Shirley L, John GB, Castrillon DH 2007 Generation of a germ cell-specific mouse transgenic Cre line, Vasa-Cre. Genesis 45:413-417 (Pubitemid 47015328)
25. Ogawa T, Aréchaga JM, Avarbock MR, Brinster RL 1997 Transplantation of testis germinal cells into mouse seminiferous tubules. Int J Dev Biol 41:111-122 (Pubitemid 27096498)
26. John GB, Gallardo TD, Shirley LJ, Castrillon DH 2008 Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev Biol 321:197-204
27. Nagano R, Tabata S, Nakanishi Y, Ohsako S, Kurohmaru M, Hayashi Y 2000 Reproliferation and relocation of mouse male germ cells (gonocytes) during prespermatogenesis. Anat Rec 258:210-220 (Pubitemid 30082913)
28. Shinohara T, Orwig KE, Avarbock MR, Brinster RL 2000 Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proc Natl Acad Sci USA 97:8346-8351 (Pubitemid 30639675)
29. Saarma M, Sariola H 1999 Other neurotrophic factors: glial cell line-derived neurotrophic factor (GDNF). Microsc Res Tech 45:292-302 (Pubitemid 29264993)
30. Schrans-Stassen BH, van de Kant HJ, de Rooij DG, van Pelt AM 1999 Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology 140:5894-5900 (Pubitemid 30645378)
31. Yoshinaga K, Nishikawa S, Ogawa M, Hayashi S, Kunisada T, Fujimoto T, Nishikawa S 1991 Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Development 113:689-699
32. Tsuda M, Sasaoka Y, Kiso M, Abe K, Haraguchi S, Kobayashi S, Saga Y 2003 Conserved role of nanos proteins in germ cell development. Science 301:1239-1241 (Pubitemid 37052213)
33. Schlesser HN, Simon L, Hofmann MC, Murphy KM, Murphy T, Hess RA, Cooke PS 2008 Effects of ETV5 (ets variant gene 5) on testis and body growth, time course of spermatogonial stem cell loss, and fertility in mice. Biol Reprod 78:483-489 (Pubitemid 351416469)
34. Rizzoti K, Brunelli S, Carmignac D, Thomas PQ, Robinson IC, Lovell-Badge R 2004 SOX3 is required during the formation of the hypothalamo-pituitary axis. Nat Genet 36:247-255 (Pubitemid 38282749)
35. Zhou Q, Nie R, Li Y, Friel P, Mitchell D, Hess RA, Small C, Griswold MD 2008 Expression of stimulated by retinoic acid gene 8 (Stra8) in spermatogenic cells induced by retinoic acid: an in vivo study in vitamin A-sufficient postnatal murine testes. Biol Reprod 79:35-42 (Pubitemid 351931040)
36. van Keulen CJ, de Rooij DG 1975 Spermatogenetic clones developing from repopulating stem cells surviving a high dose of an alkylating agent. Cell Tissue Kinet 8:543-551
37. Shah FJ, Tanaka M, Nielsen JE, Iwamoto T, Kobayashi S, Skakkebaek NE, Leffers H, Almstrup K 2009 Gene expression profiles of mouse spermatogenesis during recovery from irradiation. Reprod Biol Endocrinol 7:130
38. Meistrich ML, Hunter NR, Suzuki N, Trostle PK, Withers HR 1978 Gradual regeneration of mouse testicular stem cells after exposure to ionizing radiation. Radiat Res 74:349-362 (Pubitemid 8369182)
39. Ehmcke J, Joshi B, Hergenrother SD, Schlatt S 2007 Aging does not affect spermatogenic recovery after experimentally induced injury in mice. Reproduction 133:75-83 (Pubitemid 46332157)
40. 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 (Pubitemid 46172906)
41. Jiang FX 1998 Behaviour of spermatogonia following recovery from busulfan treatment in the rat. Anat Embryol (Berl) 198:53-61
42. Kamachi Y, Uchikawa M, Kondoh H 2000 Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet 16:182-187 (Pubitemid 30169154)
43. Koopman P 2005 Sex determination: a tale of two Sox genes. Trends Genet 21:367-370 (Pubitemid 40835718)
44. Hoser M, Potzner MR, Koch JMC, Bosl MR, Wegner M, Sock E 2008 Sox12 deletion in the mouse reveals nonreciprocal redundancy with the related Sox4 and Sox11 transcription factors. Mol Cell Biol 28:4675-4687
45. Kamachi Y, Cheah KS, Kondoh H 1999 Mechanism of regulatory target selection by the SOX high-mobility-group domain proteins as revealed by comparison of SOX1/2/3 and SOX9. Mol Cell Biol 19:107-120 (Pubitemid 29018414)
46. Zhao S, Nichols J, Smith AG, Li M 2004 SoxB transcription factors specify neuroectodermal lineage choice in ES cells. Mol Cell Neurosci 27:332-342 (Pubitemid 39433845)
47. Osaki E, Nishina Y, Inazawa J, Copeland NG, Gilbert DJ, Jenkins NA, Ohsugi M, Tezuka T, Yoshida M, Semba K 1999 Identification of a novel Sry-related gene and its germ cell-specific expression. Nucleic Acids Res 27:2503-2510 (Pubitemid 29271797)
48. Smith JM, Bowles J, Wilson M, Koopman P 2004 HMG box transcription factor gene Hbp1 is expressed in germ cells of the developing mouse testis. Dev Dyn 230:366-370 (Pubitemid 38669597)
49. Zetterström CK, Strand M-L, Söder O 2006 The high mobility group box chromosomal protein 1 is expressed in the human and rat testis where it may function as an antibacterial factor. Hum Reprod 21:2801-2809 (Pubitemid 44566990)
50. Shih Y-H, Kuo C-L, Hirst CS, Dee CT, Liu Y-R, Laghari ZA, Scotting PJ 2010 SoxB1 transcription factors restrict organizer gene expression by repressing multiple events downstream of Wnt signalling. Development 137:2671-2681