Retinoic acid triggers c-kit gene expression in spermatogonial stem cells through an enhanceosome constituted between transcription factor binding sites for retinoic acid response element (RARE), spleen focus forming virus proviral integration oncogene (SPFI1) (PU.1) and E26 transformation-specific (ETS)
Swanand Koli A , Ayan Mukherjee B and Kudumula Venkata Rami Reddy A C
+ Author Affiliations
- Author Affiliations
A Division of Molecular Immunology and Microbiology, National Institute for Research in Reproductive Health, Indian Council of Medical Research, J.M Street, Parel, Mumbai-400 012, India.
B Department of Biological Science, Kent State University, Kent, OH 44240, USA.
C Corresponding author. Email: reddyk@nirrh.res.in
Reproduction, Fertility and Development 29(3) 521-543 https://doi.org/10.1071/RD15145
Submitted: 13 April 2015 Accepted: 14 August 2015 Published: 14 October 2015
Abstract
Restricted availability of retinoic acid (RA) in the testicular milieu regulates transcriptional activity of c-kit (KIT, CD117), which aids in the determination of spermatogonial stem-cell differentiation. The effect of RA on c-kit has been reported previously, but its mode of genomic action remains unresolved. We studied the molecular machinery guiding RA responsiveness to the c-kit gene using spermatogonial stem-cell line C18–4 and primary spermatogonial cells. A novel retinoic acid response element (RARE) positioned at –989 nucleotides upstream of the transcription start site (TSS) was identified, providing a binding site for a dimeric RA receptor (i.e. retinoic acid receptor gamma (RARγ) and retinoic X receptor). RA treatment influenced c-kit promoter activity, along with endogenous c-kit expression in C18–4 cells. A comprehensive promoter deletion assay using the pGL3B reporter system characterised the region spanning –271 bp and –1011 bp upstream of the TSS, which function as minimal promoter and maximal promoter, respectively. In silico analysis predicted that the region –1011 to +58 bp comprised the distal enhancer RARE and activators such as spleen focus forming virus proviral integration oncogene (SPFI1) (PU.1), specificity protein 1 (SP1) and four E26 transformation-specific (ETS) tandem binding sites at the proximal region. Gel retardation and chromatin immunoprecipitation (ChIP) assays showed binding for RARγ, PU.1 and SP1 to the predicted consensus binding sequences, whereas GABPα occupied only two out of four ETS binding sites within the c-kit promoter region. We propose that for RA response, an enhanceosome is orchestrated through scaffolding of a CREB-binding protein (CBP)/p300 molecule between RARE and elements in the proximal promoter region, controlling germ-line expression of the c-kit gene. This study outlines the fundamental role played by RARγ, along with other non-RAR transcription factors (PU.1, SP1 and GABPα), in the regulation of c-kit expression in spermatogonial stem cells in response to RA.
Additional keywords: CBP/p300, differentiation, spermatogenesis.
References
Bastos, H., Lassale, B., Chicheportiche, A., Riou, L., Testart, J., Allemand, I., and Fouchet, P. (2005). Flow cytometric characterisation of viable meiotic and postmeiotic cells by Hoechst 33342 in mouse spermatogenesis. Cytometry A 65A, 40–49.| Flow cytometric characterisation of viable meiotic and postmeiotic cells by Hoechst 33342 in mouse spermatogenesis.Crossref | GoogleScholarGoogle Scholar |
Black, A. R., Black, J. D., and Azizkhan-Clifford, J. (2001). Sp1 and kruppel-like factor family of transcription factors in cell growth regulation and cancer. J. Cell. Physiol. 188, 143–160.
| Sp1 and kruppel-like factor family of transcription factors in cell growth regulation and cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltVKmsbc%3D&md5=ea9dd198bc08f186e8367f9465f97565CAS | 11424081PubMed |
Bokemeyer, C., Kuczyk, M. A., Dunn, T., Serth, J., Hartmann, K., Jonasson, J., Pietsch, T., Jonas, U., and Schmoll, H. J. (1996). Expression of stem-cell factor and its receptor c-kit protein in normal testicular tissue and malignant germ-cell tumours. J. Cancer Res. Clin. Oncol. 122, 301–306.
| Expression of stem-cell factor and its receptor c-kit protein in normal testicular tissue and malignant germ-cell tumours.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtlCisbo%3D&md5=b4561a14534b1cc0f3006641ac393fc5CAS | 8609154PubMed |
Brown, T. A., and McKnight, S. L. (1992). Specificities of protein–protein and protein–DNA interaction of GABP-alpha and two newly defined ETS-related proteins. Genes Dev. 6, 2502–2512.
| Specificities of protein–protein and protein–DNA interaction of GABP-alpha and two newly defined ETS-related proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXkvVOrsbc%3D&md5=00736c30a9e49a27592214da7770d5d3CAS | 1340465PubMed |
Busada, J. T., Chappell, V. A., Niedenberger, B. A., Kaye, E. P., Keiper, B. D., Hogarth, C. A., and Geyer, C. B. (2015). Retinoic acid regulates Kit translation during spermatogonial differentiation in the mouse. Dev. Biol. 397, 140–149.
| Retinoic acid regulates Kit translation during spermatogonial differentiation in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvV2gsLbI&md5=2f032c47fccf73b098fb6d1b4b286ed4CAS | 25446031PubMed |
Carter, R. S., and Avadhani, N. G. (1994). Cooperative binding of GA-binding protein transcription factors to duplicated transcription initiation region repeats of the cytochrome c oxidase subunit IV gene. J. Biol. Chem. 269, 4381–4387.
| 1:CAS:528:DyaK2cXhvVCmtbs%3D&md5=329fa743ad6aaded88ca7b096c0418dbCAS | 8308008PubMed |
Chabot, B., Stephenson, D. A., Chapman, V. M., Besmer, P., and Bernstein, A. (1988). The proto-oncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature 335, 88–89.
| The proto-oncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXlvVCks7o%3D&md5=08471301b2b6c3b6e248e27c72091dc9CAS | 2457811PubMed |
Chan, H. M., and La Thangue, N. B. (2001). p300/CBP proteins: HATs for transcriptional bridges and scaffolds. J. Cell Sci. 114, 2363–2373.
| 1:CAS:528:DC%2BD3MXlsFamt7c%3D&md5=7d9e7e9d2232586e757ce10796d3cc4cCAS | 11559745PubMed |
Chen, W., Jia, W., Wang, K., Si, X., Zhu, S., Duan, T., and Kang, J. (2013). Distinct roles for CBP and p300 on the RA-mediated expression of the meiosis commitment gene Stra8 in mouse embryonic stem cells. PLoS One 8, e66076.
| Distinct roles for CBP and p300 on the RA-mediated expression of the meiosis commitment gene Stra8 in mouse embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVems7%2FN&md5=b3739b5df441d041ee3e467720bd3fe3CAS | 23785470PubMed |
Clermont, Y., and Perey, B. (1957). Quantitative study of the cell population of the seminiferous tubules in immature rats. Am. J. Anat. 100, 241–267.
| Quantitative study of the cell population of the seminiferous tubules in immature rats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG2s%2FotF2htg%3D%3D&md5=8c00808028c641444cff88cffa56f4b9CAS | 13435229PubMed |
Coffey, J., Linger, R., Pugh, J., Dudakia, D., Sokal, M., Easton, D. F., Timothy Bishop, D., Stratton, M., Huddart, R., and Rapley, E. A. (2008). Somatic KIT mutations occur predominantly in seminoma germ-cell tumours and are not predictive of bilateral disease: report of 220 tumours and review of literature. Genes Chromosomes Cancer 47, 34–42.
| Somatic KIT mutations occur predominantly in seminoma germ-cell tumours and are not predictive of bilateral disease: report of 220 tumours and review of literature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVWrtrnO&md5=aa2cdb23a9c34ff04a76072b142b7ed2CAS | 17943970PubMed |
Cooke, P. S., Hess, R. A., Simon, L., Schlesser, H. N., Carnes, K., Tyagi, G., Hofmann, M. C., and Murphy, K. M. (2006). The transcription factor ETS-related molecule (ERM) is essential for spermatogonial stem-cell maintenance and self renewal. Anim. Reprod. 3, 98–107.
Dekker, J., Rippe, K., Dekker, M., and Kleckner, N. (2002). Capturing chromosome conformation. Science 295, 1306–1311.
| Capturing chromosome conformation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsVGhsbk%3D&md5=f7dd0489d0b85ef4ffc8240ecb5e1947CAS | 11847345PubMed |
Emami, K. H., Burke, T. W., and Smale, S. T. (1998). Sp1 activation of a TATA-less promoter requires a species-specific interaction involving transcription factor IID. Nucleic Acids Res. 26, 839–846.
| Sp1 activation of a TATA-less promoter requires a species-specific interaction involving transcription factor IID.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtV2ksbY%3D&md5=30aec381badc37853d5c29fc348b9486CAS | 9443978PubMed |
Emili, A., Greenblatt, J., and Ingles, C. (1994). Species-specific interaction of the glutamine-rich activation domains of Sp1 with the TATA box-binding protein. Mol. Cell. Biol. 14, 1582–1593.
| 1:CAS:528:DyaK2cXitlymu7k%3D&md5=cb06438eacf509c3b218d52f8d397608CAS | 8114696PubMed |
Freiman, R. N. (2009). Specific variants of general transcription factors regulate germ-cell development in diverse organisms. Biochim. Biophys. Acta 1789, 161–166.
| Specific variants of general transcription factors regulate germ-cell development in diverse organisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVeguro%3D&md5=83eb12a2dee4f1f36d15bb9bd19c18b5CAS | 19437618PubMed |
Galvagni, F., Capo, S., and Oliviero, S. (2001). Sp1 and Sp3 physically interact and co-operate with GABP for the activation of the utrophin promoter. J. Mol. Biol. 306, 985–996.
| Sp1 and Sp3 physically interact and co-operate with GABP for the activation of the utrophin promoter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFOhu7w%3D&md5=46d1ce03a18904bb75c3254ff9f5667eCAS | 11237613PubMed |
Gely-Pernot, A., Raverdeau, M., Célébi, C., Dennefeld, C., Feret, B., Klopfenstein, M., Yoshida, S., Ghyselinck, N. B., and Mark, M. (2012). Spermatogonia differentiation requires retinoic acid receptor γ. Endocrinology 153, 438–449.
| Spermatogonia differentiation requires retinoic acid receptor γ.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XovFWkuw%3D%3D&md5=b54faf7979a72403c4fd261442036045CAS | 22045663PubMed |
Goodman, R. H., and Smolik, S. (2000). CBP/p300 in cell growth, transformation and development. Genes Dev. 14, 1553–1577.
| 1:CAS:528:DC%2BD3cXkvFCkurc%3D&md5=58cf9b0b4ed0febc6fd3b09e201c89bcCAS | 10887150PubMed |
Graves, B. J., and Petersen, J. M. (1998). Specificity within the ETS family of transcription factors. Adv. Cancer Res. 75, 1–55.
| Specificity within the ETS family of transcription factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXpsFyr&md5=39a936cdd28fb8fbd74f2bca7cdffc44CAS | 9709806PubMed |
Hao, H., Qi, H., and Ratnam, M. (2003). Modulation of the folate receptor type beta gene by co-ordinate actions of retinoic acid receptors at activator Sp1/ETS and repressor AP-1 sites. Blood 101, 4551–4560.
| Modulation of the folate receptor type beta gene by co-ordinate actions of retinoic acid receptors at activator Sp1/ETS and repressor AP-1 sites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktFKhu7g%3D&md5=c5e6247b6bea46087a8cffa2e8eb6d10CAS | 12543860PubMed |
Hofmann, M.-C., Braydich-Stolle, L., Dettin, L., Johnson, E., and Dym, M. (2005). Immortalisation of mouse germ-line stem cells. Stem Cells 23, 200–210.
| Immortalisation of mouse germ-line stem cells.Crossref | GoogleScholarGoogle Scholar | 15671143PubMed |
Huckins, C., and Oakberg, E. F. (1978). Morphological and quantitative analysis of spermatogonia in mouse testes using whole mounted seminiferous tubules in the normal testes. Anat. Rec. 192, 519–528.
| Morphological and quantitative analysis of spermatogonia in mouse testes using whole mounted seminiferous tubules in the normal testes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1M7gtFOhtw%3D%3D&md5=ae0df4e5dd925757f1fd65617d83b8d9CAS | 736272PubMed |
Jayaraman, G., Srinivas, R., Duggan, C., Ferreira, E., Swaminathan, S., Somasundaram, K., Williams, J., Hauser, C., Kurkinen, M., Dhar, R., Weitzman, S., Buttice, G., and Thimmapaya, B. (1999). p300/cAMP-responsive element-binding protein interactions with ETS-1 and ETS-2 in the transcriptional activation of the human stromelysin promoter. J. Biol. Chem. 274, 17 342–17 352.
| p300/cAMP-responsive element-binding protein interactions with ETS-1 and ETS-2 in the transcriptional activation of the human stromelysin promoter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvVGrs70%3D&md5=e2b053b11c9790ee6d33a40b712141b7CAS |
Kimmins, S., Kotaja, N., Davidson, I., and Sassone-Corsi, P. (2004). Testis-specific transcription mechanisms promoting male germ-cell differentiation. Reproduction 128, 5–12.
| Testis-specific transcription mechanisms promoting male germ-cell differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXms1elsbo%3D&md5=658b210b353fa023805c6881734507dbCAS | 15232059PubMed |
LaMarco, K., Thompson, C., Byers, B., Walton, E., and McKnight, S. L. (1991). Identification of ETS- and notch-related subunits in GA-binding protein. Science 253, 789–792.
| Identification of ETS- and notch-related subunits in GA-binding protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XksVaqsrw%3D&md5=fca9ea46e7d72a76f8ed5fc2f21f619bCAS | 1876836PubMed |
Lin, S. Y., Black, A. R., Kostic, D., Pajovic, S., Hoover, C. N., and Azizkhan, J. C. (1996). Cell cycle-regulated association of E2F1 and Sp1 is related to their functional interaction. Mol. Cell. Biol. 16, 1668–1675.
| 1:CAS:528:DyaK28XhvVagsrc%3D&md5=31e293d06d8e07f425a832eaf6f3ed7eCAS | 8657142PubMed |
Manova, K., Nocka, K., Besmer, P., and Bachvarova, R. F. (1990). Gonadal expression of c-kit encoded at the W locus of the mouse. Development 110, 1057–1069.
| 1:CAS:528:DyaK3MXhs1Wntb4%3D&md5=813aee63e7f728e622b8453a66557183CAS | 1712701PubMed |
McIntyre, A., Summersgill, B., Grygalewicz, B., Gillis, A. J., Stoop, J., van Gurp, R. J., Dennis, N., Fisher, C., Huddart, R., Cooper, C., Clark, J., Oosterhuis, J. W., Looijenga, L. H., and Shipley, J. (2005). Amplification and overexpression of the KIT gene is associated with progression in the seminoma subtype of testicular germ-cell tumours of adolescents and adults. Cancer Res. 65, 8085–8089.
| Amplification and overexpression of the KIT gene is associated with progression in the seminoma subtype of testicular germ-cell tumours of adolescents and adults.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVShsbrO&md5=94fc72a9fa709156fd1c0d1b1ebd9653CAS | 16166280PubMed |
Merchiers, P., Bulens, F., De Vriese, A., Collen, D., and Belayew, A. (1999). Involvement of Sp1 in basal and retinoic acid-induced transcription of the human tissue-type plasminogen activator gene. FEBS Lett. 456, 149–154.
| Involvement of Sp1 in basal and retinoic acid-induced transcription of the human tissue-type plasminogen activator gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsFWgsr8%3D&md5=0f3e24b48933220a0c04b7b14ea8367cCAS | 10452548PubMed |
Muciaccia, B., Sette, C., Paronetto, M. P., Barchi, M., Pensini, S., D’Agostino, A., Gandini, L., Geremia, R., Stefanini, M., and Rossi, P. (2010). Expression of a truncated form of KIT tyrosine kinase in human spermatozoa correlates with sperm DNA integrity. Hum. Reprod. 25, 2188–2202.
| Expression of a truncated form of KIT tyrosine kinase in human spermatozoa correlates with sperm DNA integrity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGru77K&md5=2ef754e4a07fcb2818f9bfff000af674CAS | 20601678PubMed |
Nakamura, B. N., Lawson, G., Chan, J. Y., Banuelos, J., Cortés, M. M., Hoang, Y. D., Ortiz, L., Rau, B. A., and Luderer, U. (2010). Knockout of the transcription factor NRF2 disrupts spermatogenesis in an age-dependent manner. Free Radic. Biol. Med. 49, 1368–1379.
| Knockout of the transcription factor NRF2 disrupts spermatogenesis in an age-dependent manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1WlsbfI&md5=ae4ea1a813e6b561a8113e01980b3bc1CAS | 20692336PubMed |
Oakberg, E. F. (1971). Spermatogonial stem-cell renewal in the mouse. Anat. Rec. 169, 515–531.
| Spermatogonial stem-cell renewal in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE3M7lsVWmsw%3D%3D&md5=72734c98a68707a2a2b4e43a3d57a849CAS | 5550531PubMed |
Ohta, H., Yomogida, K., Dohmae, K., and Nishimune, Y. (2000). Regulation of proliferation and differentiation in spermatogonial stem cells: the role of c-kit and its ligand SCF. Development 127, 2125–2131.
| 1:CAS:528:DC%2BD3cXktl2jtL0%3D&md5=72a2beb07dbd1a5a6ab0f11103af198eCAS | 10769236PubMed |
Olive, V., Wagner, N., Chan, S., Kastner, P., Vannetti, C., Cuzin, F., and Rassoulzadegan, M. (2007). PU.1 (Sfpi1), a pleiotropic regulator expressed from the first embryonic stages with a crucial function in germinal progenitors. Development 134, 3815–3825.
| PU.1 (Sfpi1), a pleiotropic regulator expressed from the first embryonic stages with a crucial function in germinal progenitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVeku7rK&md5=d91a9a721420ef73fa9aff0e6e63c857CAS | 17913791PubMed |
Pellegrini, M., Filipponi, D., Gori, M., Barrios, F., Lolicato, F., Grimaldi, P., Rossi, P., Jannini, E. A., Geremia, R., and Dolci, S. (2008). ATRA and KL promote differentiation toward the meiotic program of male germ cells. Cell Cycle 7, 3878–3888.
| ATRA and KL promote differentiation toward the meiotic program of male germ cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvVSit7o%3D&md5=0f1bfe69e5e8e2d10efdbd1c831106deCAS | 19098446PubMed |
Prabhu, S. M., Meistrich, M. L., McLaughlin, E. A., Roman, S. D., Warne, S., Mendis, S., Itman, C., and Loveland, K. L. (2006). Expression of c-Kit receptor mRNA and protein in the developing, adult and irradiated rodent testis. Reproduction 131, 489–499.
| Expression of c-Kit receptor mRNA and protein in the developing, adult and irradiated rodent testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs12jsL8%3D&md5=21d3d27d71be9dceb83876e0ab2849cdCAS | 16514192PubMed |
Raverdeau, M., Gely-Pernot, A., Feret, B., Dennefeld, C., Benoit, G., Davidson, I., Chambon, P., Mark, M., and Ghyselinck, N. B. (2012). Retinoic acid induces Sertoli cell paracrine signals for spermatogonia differentiation but cell autonomously drives spermatocyte meiosis. Proc. Natl. Acad. Sci. USA 109, 16 582–16 587.
| Retinoic acid induces Sertoli cell paracrine signals for spermatogonia differentiation but cell autonomously drives spermatocyte meiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFKltrjN&md5=073b725bceebe5a329bfc5f5600e123dCAS |
Resendes, K. K., and Rosmarin, A. G. (2006). GA-binding protein and p300 are essential components of a retinoic acid-induced enhanceosome in myeloid cells. Mol. Cell. Biol. 26, 3060–3070.
| GA-binding protein and p300 are essential components of a retinoic acid-induced enhanceosome in myeloid cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs1SltrY%3D&md5=7724504d7efd2666cb35795e23620524CAS | 16581781PubMed |
Richardson, R. T., Alekseev, O., Alekseev, O. M., and O’Rand, M. G. (2006). Characterisation of the NASP promoter in 3T3 fibroblasts and mouse spermatogenic cells. Gene 371, 52–58.
| Characterisation of the NASP promoter in 3T3 fibroblasts and mouse spermatogenic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xisl2rtrY%3D&md5=958bc75f51db9a6ae69d9097ab618ed3CAS | 16423470PubMed |
Ristevski, S., O’Leary, D., Thornell, A., Owen, M., Kola, I., and Hertzog, P. J. (2004). The ETS transcription factor GABPα is essential for early embryogenesis. Mol. Cell. Biol. 24, 5844–5849.
| The ETS transcription factor GABPα is essential for early embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXls1aqt74%3D&md5=0c20568b57f8280b0532152901c14780CAS | 15199140PubMed |
Rosmarin, A. G., Luo, M., Caprio, D. G., Shang, J., and Simkevich, C. P. (1998). Sp1 cooperates with the ETS transcription factor, GABP, to activate the CD18 (2 leukocyte integrin) promoter. J. Biol. Chem. 273, 13 097–13 103.
| Sp1 cooperates with the ETS transcription factor, GABP, to activate the CD18 (2 leukocyte integrin) promoter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjsVGit7c%3D&md5=53c84344ac3ec9928e9cb753a9718739CAS |
Schrans-Stassen, B. H., van de Kant, H. J., and de Rooij, D. G. (1999). Differential expression of c-kit in mouse undifferentiated and differentiating Type A spermatogonia. Endocrinology 140, 5894–5900.
| Differential expression of c-kit in mouse undifferentiated and differentiating Type A spermatogonia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns12htbc%3D&md5=93c9da786a1b566ce42a324275488910CAS | 10579355PubMed |
Sharrocks, A. D., Brown, A. L., Ling, Y., and Yates, P. R. (1997). The ETS-domain transcription factor family. Int. J. Biochem. Cell Biol. 29, 1371–1387.
| The ETS-domain transcription factor family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitlOhu70%3D&md5=fe06fc7c82fe38afbdae3e479643089dCAS | 9570133PubMed |
Shirasaki, F., Makhluf, H., LeRoy, C., Watson, D., and Trojanowska, M. (1999). ETS transcription factors cooperate with Sp1 to activate the human tenascin-C promoter. Oncogene 18, 7755–7764.
| ETS transcription factors cooperate with Sp1 to activate the human tenascin-C promoter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1WgtA%3D%3D&md5=d0d96487471569424fba5ce4fd208045CAS | 10618716PubMed |
Sleigh, M. J., and Lockett, T. J. (1985). SV40 enhancer activation during retinoic acid-induced differentiation of F9 embryonal carcinoma cells. EMBO J. 4, 3831–3837.
| 1:CAS:528:DyaL28XhvVSrsrs%3D&md5=a4d872dc9fba23d3f5c662d15df4fe50CAS | 3004973PubMed |
Sorrentino, V., Giorgi, M., Geremia, R., Besmer, P., and Rossi, P. (1991). Expression of the c-kit proto-oncogene in murine male germ cells. Oncogene 6, 149–151.
| 1:CAS:528:DyaK3MXhtF2hsLo%3D&md5=971a79b848183890a84c132b6ac93c5eCAS | 1704118PubMed |
Strohmeyer, T., Reese, D., Press, M., Ackermann, R., Hartmann, M., and Slamon, D. (1995). Expression of the c-kit proto-oncogene and its ligand stem-cell factor (SCF) in normal and malignant human testicular tissue. J. Urol. 153, 511–515.
| Expression of the c-kit proto-oncogene and its ligand stem-cell factor (SCF) in normal and malignant human testicular tissue.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M7hsFahtg%3D%3D&md5=263422ee69343b2a815545f61a327306CAS | 7529338PubMed |
van Pelt, A. M., and de Rooij, D. G. (1990). Synchronisation of the seminiferous epithelium after vitamin A replacement in vitamin A-deficient mice. Biol. Reprod. 43, 363–367.
| Synchronisation of the seminiferous epithelium after vitamin A replacement in vitamin A-deficient mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXltlWjsLY%3D&md5=f0e3978c9ad2ff7f19882c439aef6ce6CAS | 2271719PubMed |
Wasylyk, B., Hagman, J., and Gutierrez-Hartmann, A. (1998). ETS transcription factors: nuclear effectors of the Ras-MAP kinase signalling pathway. Trends Biochem. Sci. 23, 213–216.
| ETS transcription factors: nuclear effectors of the Ras-MAP kinase signalling pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktVSlsLc%3D&md5=a7321985450f1cf3aed15f2ee6de7885CAS | 9644975PubMed |
Yamamoto, H., Kihara-Negishi, F., Yamada, T., Hashimoto, Y., and Oikawa, T. (1999). Physical and functional interactions between the transcription factor PU.1 and the co-activator CBP. Oncogene 18, 1495–1501.
| Physical and functional interactions between the transcription factor PU.1 and the co-activator CBP.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhs1ygurw%3D&md5=66ab2785f665783e48cb4919d1e1406dCAS | 10050886PubMed |
Yang, Q. E., Racicot, K. E., Kaucher, A. V., Oatley, M. J., and Oatley, J. M. (2013). MicroRNAs 221 and 222 regulate the undifferentiated state in mammalian male germ cells. Development 140, 280–290.
| MicroRNAs 221 and 222 regulate the undifferentiated state in mammalian male germ cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjt1Cgu70%3D&md5=3ff172d85c2a753f9f4546b6ffbf1441CAS | 23221369PubMed |
Yao, T.-P., Oh, S. P., Fuchs, M., Zhou, N.-D., Ch’ng, L.-E., Newsome, D., Bronson, R. T., Li, E., Livingston, D. M., and Eckner, R. (1998). Gene dosage-dependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell 93, 361–372.
| Gene dosage-dependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtFCjtLo%3D&md5=86d37268d4e8625fbfd2d7a40237c563CAS | 9590171PubMed |
Yoshinaga, K., Nishikawa, S., Ogawa, M., Hayashi, S., Kunisada, T., Fujimoto, T., and 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.
| 1:STN:280:DyaK387ks1akuw%3D%3D&md5=485d6a4b2f415fe2fa6b277b7b036d65CAS | 1723681PubMed |
Zhang, L., Tang, J., Haines, C., Feng, H., Lai, L., Teng, X., and Han, Y. (2011). c-kit and its related genes in spermatogonial differentiation. Spermatogenesis 1, 186–194.
| c-kit and its related genes in spermatogonial differentiation.Crossref | GoogleScholarGoogle Scholar | 22319667PubMed |
Zhang, L., Jiangjing, T., Christopher, J., Huai, F., Liangxue, L., Teng, X., and Han, Y. (2013). c-kit expression profile and regulatory factors during spermatogonial stem cell differentiation. BMC Dev. Biol. 13, 38–51.
| c-kit expression profile and regulatory factors during spermatogonial stem cell differentiation.Crossref | GoogleScholarGoogle Scholar | 24161026PubMed |
Zhou, Q., and Griswold, M. D. (2008) ‘Regulation of Spermatogonia’. (Harvard Stem Cell Institute: Cambridge, MA, USA.)
