C-kit expression profile and regulatory factors during spermatogonial stem cell differentiation

BMC Developmental Biology

Volumn 13, Issue 1, 2013, Pages

  Zhang, Lei ^a,b,c   Tang, Jiangjing ^a,b,d   Haines, Christopher J ^b   Feng, Huai ^e   Lai, Liangxue ^d   Teng, Xiaoming ^a   Han, Yibing ^a,b  

^a TONGJI UNIVERSITY   (China)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^c Diagnostics and Reproductive Health Center BGI   (China)

^d GUANGZHOU INSTITUTES OF BIOMEDICINE AND HEALTH   (China)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

c kit; Differentiation; Expression profile; Regulatory factor; Spermatogonial stem cells

Indexed keywords

RETINOIC ACID; STEM CELL FACTOR RECEPTOR; TRANSCRIPTOME;

ANIMAL; ARTICLE; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELL LINE; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MALE; METABOLISM; MOUSE; NEWBORN; SPERMATOGONIUM; STEM CELL; TESTIS;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; GENE EXPRESSION REGULATION; HUMANS; MALE; MICE; MICE, INBRED C57BL; PROTO-ONCOGENE PROTEINS C-KIT; SPERMATOGONIA; STEM CELLS; TESTIS; TRANSCRIPTOME; TRETINOIN;

EID: 84886222475     PISSN: None     EISSN: 1471213X     Source Type: Journal    
DOI: 10.1186/1471-213X-13-38     Document Type: Article

References (45)

1. Mouse differentiating spermatogonia can generate germinal stem cells in vivo. Barroca V, Lassalle B, Coureuil M, Louis JP, Le PF, Testart J, Allemand I, Riou L, Fouchet P, Nat Cell Biol 2009 11 190 196 10.1038/ncb1826 19098901
2. Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Schrans Stassen BH, De Kant HJ V, De Rooij DG, Van PAM, Endocrinology 1999 140 5894 5900 10.1210/en.140.12.5894 10579355 (Pubitemid 30645378)
3. The proto-oncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Chabot B, Stephenson DA, Chapman VM, Besmer P, Bernstein A, Nature 1988 335 88 89 10.1038/335088a0 2457811
4. Human proto-oncogene c-kit: a new cell surface receptor tyrosine kinase for an unidentified ligand. Yarden Y, Kuang WJ, Yang Feng T, Coussens L, Munemitsu S, Dull TJ, Chen E, Schlessinger J, Francke U, Ullrich A, EMBO J 1987 6 3341 3351 2448137
5. The fourth immunoglobulin domain of the stem cell factor receptor couples ligand binding to signal transduction. Blechman JM, Lev S, Barg J, Eisenstein M, Vaks B, Vogel Z, Givol D, Yarden Y, Cell 1995 80 103 113 10.1016/0092- 8674(95)90455-7 7529140
6. Structure-function analyses of the kit receptor for the steel factor. Blechman JM, Lev S, Givol D, Yarden Y, Stem Cells 1993 11 Suppl 2 12 21 7691317 (Pubitemid 23331548)
7. A cell- and developmental stage-specific promoter drives the expression of a truncated c-kit protein during mouse spermatid elongation. Albanesi C, Geremia R, Giorgio M, Dolci S, Sette C, Rossi P, Development 1996 122 1291 1302 8620856 (Pubitemid 26124454)
8. Expression of c-kit receptor and its autophosphorylation in immature rat type A spermatogonia. Dym M, Jia MC, Dirami G, et al. Biol Reprod 1995 52 1 8 19 10.1095/biolreprod52.1.8 7536046
9. Steel factor controls primordial germ cell survival and motility from the time of their specification in the allantois, and provides a continuous niche throughout their migration. Gu Y, Runyan C, Shoemaker A, Surani A, Wylie C, Development 2009 136 8 1295 1303 10.1242/dev.030619 19279135
10. Apoptosis, onset and maintenance of spermatogenesis: evidence for the involvement of Kit in Kit-haplodeficient mice. Guerif F, Cadoret V, Rahal-Perola V, et al. Biol Reprod 2002 67 1 70 79 10.1095/biolreprod67.1.70 12080001 (Pubitemid 34680637)
11. Regulation of proliferation and differentiation in spermatogonial stem cells: the role of c-kit and its ligand SCF. Ohta H, Yomogida K, Dohmae K, Nishimune Y, Development 2000 127 10 2125 2131 10769236 (Pubitemid 30386676)
12. Expression of the c-kit gene is critical for migration of neonatal rat gonocytes in vitro. Orth JM, Qiu J, Jester WF Jr, Pilder S, Biol Reprod 1997 57 3 676 683 10.1095/biolreprod57.3.676 9283007 (Pubitemid 27349932)
13. Kit ligand mediates survival of type A spermatogonia and dividing spermatocytes in postnatal mouse testes. Packer AI, Besmer P, Bachvarova RF, Mol Reprod Dev 1995 42 3 303 310 10.1002/mrd.1080420307 8579844
14. Expression of c-Kit receptor mRNA and protein in the developing, adult and irradiated rodent testis. Prabhu SM, Meistrich ML, McLaughlin EA, Roman SD, Warne S, Mendis S, Itman C, Loveland KL, Reproduction 2006 131 489 499 10.1530/rep.1.00968 16514192
15. Steel factor controls midline cell death of primordial germ cells and is essential for their normal proliferation and migration. Runyan C, Schaible K, Molyneaux K, Wang Z, Levin L, Wylie C, Development 2006 133 24 4861 4869 10.1242/dev.02688 17107997 (Pubitemid 46085052)
16. Exposure to Retinoic Acid in the Neonatal but Not Adult Mouse Results in Synchronous Spermatogenesis. Snyder EM, Davis JC, Zhou Q, Evanoff R, Griswold MD, Biol Reprod 2011 84 5 886 893 10.1095/biolreprod.110.089755 21228214
17. Stem cell factor protects germ cells from apoptosis in vitro. Yan W, Suominen J, Toppari J, J Cell Sci 2000 113 Pt 1 161 168 10591635 (Pubitemid 30066343)
18. Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Yoshinaga K, Nishikawa S, Ogawa M, Hayashi S, Kunisada T, Fujimoto T, Nishikawa S, Development 1991 113 689 699 1723681
19. Expression of the c-kit proto-oncogene in the murine male germ cells. Sorrentino V, Giorgi M, Geremia R, Besmer P, Rossi P, Oncogene 1991 6 149 151 1704118 (Pubitemid 21923995)
20. A novel c-kit transcript, potentially encoding a truncated receptor, originates within a kit gene intron in mouse spermatids. Rossi P, Marziali G, Albanesi C, Charlesworth A, Geremia R, Sorrentino V, Dev Biol 1992 152 203 207 10.1016/0012-1606(92)90172-D 1378413
21. Parthenogenetic activation of mouse eggs by microinjection of a truncated c-kit tyrosine kinase present in spermatozoa. Sette C, Bevilacqua A, Bianchini A, Mangia F, Geremia R, Rossi P, Development 1997 124 2267 2274 9187152 (Pubitemid 27283247)
22. The role of stem cell factor and of alternative c-kit gene products in the establishment, maintenance and function of germ cells. Sette C, Dolci S, Geremia R, Rossi P, Int J Dev Biol 2000 44 599 608 11061423
23. Spermatogonial stem cells derived from infertile Wv/Wv mice self-renew in vitro and generate progeny following transplantation. Kubota H, Avarbock MR, Schmidt JA, Brinster RL, Biol Reprod 2009 81 293 301 10.1095/biolreprod.109. 075960 19369648
24. Phenotypic plasticity of mouse spermatogonial stem cells. Morimoto H, Kanatsu Shinohara M, Takashima S, Chuma S, Nakatsuji N, Takehashi M, Shinohara T, PLoS One 2009 4 7909 10.1371/journal.pone.0007909 19936070
25. Functional hierarchy and reversibility within the murine spermatogenic stem cell compartment. Nakagawa T, Sharma M, Nabeshima Y, Braun RE, Yoshida S, Science 2010 328 62 67 10.1126/science.1182868 20299552
26. Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Shinohara T, Orwig KE, Avarbock MR, Brinster RL, Proc Natl Acad Sci U S A 2000 97 8346 8351 10.1073/pnas.97.15.8346 10900001 (Pubitemid 30639675)
27. The heterogeneity of spermatogonia is revealed by their topology and expression of marker proteins including the germ cell-specific proteins Nanos2 and Nanos3. Suzuki H, Sada A, Yoshida S, Saga Y, Dev Biol 2009 336 222 231 10.1016/j.ydbio.2009.10.002 19818747
28. The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Yoshida S, Sukeno M, Nakagawa T, Ohbo K, Nagamatsu G, Suda T, Nabeshima Y, Development 2006 133 1495 1505 10.1242/dev.02316 16540512 (Pubitemid 43732963)
29. Imatinib has deleterious effects on differentiating spermatogonia while sparing spermatogonial stem cell self renewal. Heim C, Minniear K, Dann CT, Reprod Toxicol 2011 31 454 463 10.1016/j.reprotox.2010.12.056 21295132
30. Restoration of spermatogenesis after transplantation of c-Kit positive testicular cells in the fowl. Trefil P, Bakst MR, Yan H, Hejnar J, Kalina J, Mucksova J, Theriogenology 2010 74 1670 1676 10.1016/j.theriogenology.2010.07. 002 20833414
31. Generation of multipotent cell lines from a distinct population of male germ line stem cells. Izadyar F, Pau F, Marh J, Slepko N, Wang T, Gonzalez R, Ramos T, Howerton K, Sayre C, Silva F, Reproduction 2008 135 771 784 10.1530/REP-07-0479 18502893 (Pubitemid 351837390)
32. Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. Jones Villeneuve EM, McBurney MW, Rogers KA, Kalnins VI, J Cell Biol 1982 94 253 262 10.1083/jcb.94.2.253 7107698 (Pubitemid 12026774)
33. Regulation and perturbation of testicular functions by vitamin A. Livera G, Rouiller-Fabre V, Pairault C, Levacher C, Habert R, Reproduction 2002 124 173 180 10.1530/rep.0.1240173 12141930
34. Retinoid signaling determines germ cell fate in mice. Bowles J, Knight D, Smith C, Wilhelm D, Richman J, Mamiya S, Yashiro K, Chawengsaksophak K, Wilson MJ, Rossant J, et al. Science 2006 312 596 600 10.1126/science.1125691 16574820
35. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC, Proc Natl Acad Sci U S A 2006 103 2474 2479 10.1073/pnas.0510813103 16461896
36. Retinol-induced stage synchronization in seminiferous tubules of the rat. Morales C, Griswold MD, Endocrinology 1987 121 1 432 434 10.1210/endo-121-1-432 3595524 (Pubitemid 17089311)
37. Retinoic acid is able to reinitiate spermatogenesis in vitamin A-deficient rats and high replicate doses support the full development of spermatogenic cells. Van PAM, De Rooij DG, Endocrinology 1991 128 697 704 10.1210/endo-128-2-697 1989855
38. Immortalization of mouse germ line stem cells. Hofmann MC, Braydich-Stolle L, Dettin L, Johnson E, Dym M, Stem Cells 2005 23 200 210 10.1634/stemcells.2003-0036 15671143 (Pubitemid 40239515)
39. Immortalization of germ cells and somatic testicular cells using the SV40 large T antigen. Hofmann MC, Narisawa S, Hess RA, Millan JL, Exp Cell Res 1992 201 417 435 10.1016/0014-4827(92)90291-F 1322317
40. A haploid and a diploid cell coexist in an in vitro immortalized spermatogenic cell line. Hofmann MC, Abramian D, Millan JL, Dev Genet 1995 16 119 127 10.1002/dvg.1020160205 7736662
41. Immortalized germ cells undergo meiosis in vitro. Hofmann MC, Hess RA, Goldberg E, Millan JL, Proc Natl Acad Sci U S A 1994 91 5533 5537 10.1073/pnas.91.12.5533 8202522 (Pubitemid 24174362)
42. Expression of stimulated by retinoic acid gene 8 (Stra8) and maturation of murine gonocytes and spermatogonia induced by retinoic acid in vitro. Zhou Q, Li Y, Nie R, Friel P, Mitchell D, Evanoff RM, Pouchnik D, Banasik B, McCarrey JR, Small C, et al. Biol Reprod 2008 78 537 545 10.1095/biolreprod.107.064337 18032419 (Pubitemid 351416482)
43. beta1- and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Shinohara T, Avarbock MR, Brinster RL, Proc Natl Acad Sci U S A 1999 96 5504 5509 10.1073/pnas.96.10.5504 10318913 (Pubitemid 29234647)
44. Identification and distribution of a novel platelet-derived growth factor receptor beta variant: effect of retinoic acid and involvement in cell differentiation. Wang Y, Culty M, Endocrinology 2007 148 5 2233 2250 10.1210/en.2006-1206 17303670 (Pubitemid 46997079)
45. ATRA and KL promote differentiation toward the meiotic program of male germ cells. Pellegrini M, Filipponi D, Gori M, et al. Cell Cycle 2008 7 24 3878 3888 10.4161/cc.7.24.7262 19098446