CSK Controls Retinoic Acid Receptor (RAR) Signaling: a RAR–c-SRC Signaling Axis Is Required for Neuritogenic Differentiation
Open accessAbstract
Herein, we report the first evidence that c-SRC is required for retinoic acid (RA) receptor (RAR) signaling, an observation that suggests a new paradigm for this family of nuclear hormone receptors. We observed that CSK negatively regulates RAR functions required for neuritogenic differentiation. CSK overexpression inhibited RA-mediated neurite outgrowth, a result which correlated with the inhibition of the SFK c-SRC. Consistent with an extranuclear effect of CSK on RAR signaling and neurite outgrowth, CSK overexpression blocked the downstream activation of RAC1. The conversion of GDP-RAC1 to GTP-RAC1 parallels the activation of c-SRC as early as 15 min following all-trans-retinoic acid treatment in LA-N-5 cells. The cytoplasmic colocalization of c-SRC and RARgamma was confirmed by immunofluorescence staining and confocal microscopy. A direct and ligand-dependent binding of RAR with SRC was observed by surface plasmon resonance, and coimmunoprecipitation studies confirmed the in vivo binding of RARgamma to c-SRC. Deletion of a proline-rich domain within RARgamma abrogated this interaction in vivo. CSK blocked the RAR-RA-dependent activation of SRC and neurite outgrowth in LA-N-5 cells. The results suggest that transcriptional signaling events mediated by RA-RAR are necessary but not sufficient to mediate complex differentiation in neuronal cells. We have elucidated a nongenomic extranuclear signal mediated by the RAR-SRC interaction that is negatively regulated by CSK and is required for RA-induced neuronal differentiation.
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In neuronal cells, Sertoli cells, and embryonic stem cells, RA instead activates p42/p44 Erk or classical MAPKs.
“However, in neuronal cells, Sertoli cells, and embryonic stem cells, RA instead activates the p42/p44 extracellular signal-regulated kinases (Erk) or classical MAPKs ( 116-122 ).”
From Vitamin A and retinoid signaling: genomic and nongenomic effects (2013) · cites this paper as [117]
In neuronal cells, the activation of Erks has been shown to involve either RARα localized in membranes or RARγ in association with the Src kinase.
“However, in neuronal cells, the activation of Erks has been shown to involve either RAR ␣ localized in membranes ( 121 ) or RAR ␥ in association with the sarcome (Src) kinase ( 117 ).”
From Vitamin A and retinoid signaling: genomic and nongenomic effects (2013) · cites this paper as [117]
RA-induced activation of the two MAPK pathways is subsequent to activation of upstream cascades involving Rho-GTPases, PI3K and/or PKB/Akt.
“Nevertheless, the RA-induced activation of the two MAPK pathways is subsequent to the activation of upstream cascades involving Rho-GTPases ( 114, 115, 117 ), phosphoinositide 3-kinase (PI3K) and/or protein kinase B (PKB)/Akt ( 120, 121, 123 ), suggesting an atypical, nongenomic activation event similar to that described for steroid nuclear receptors ( 124, 125 ).”
From Vitamin A and retinoid signaling: genomic and nongenomic effects (2013) · cites this paper as [117]
Cites
The nuclear receptor superfamily: the second decade
Mangelsdorf, D. J., Thummel, C., Beato, M., Herrlich, P., Schütz, G., Umesono, K., Blumberg, B., Kastner, P., Mark, M., Chambon, P., et al. (1995) · Cell · doi:10.1016/0092-8674(95)90199-x · Cited by 6,964 · see citing works
Rho GTPases and the Actin Cytoskeleton
Hall, A. (1998) · Science · doi:10.1126/science.279.5350.509 · Cited by 6,138 · see citing works
Norman, A. W. (1979) · Cited by 3,769 · see citing works
Blume-Jensen, P., & Hunter, T. (2001) · Nature · doi:10.1038/35077225 · Cited by 3,738 · see citing works
The RXR heterodimers and orphan receptors
Mangelsdorf, D. J., & Evans, R. M. (1995) · Cell · doi:10.1016/0092-8674(95)90200-7 · Cited by 3,133 · see citing works
Cellular functions regulated by Src family kinases.
Thomas, S. M., & Brugge, J. (1997) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.13.1.513 · Cited by 2,610 · see citing works
Rho GTPases and signaling networksPreprint
Aelst, L. V., & D’Souza‐Schorey, C. (1997) · Genes & Development · doi:10.1101/gad.11.18.2295 · Cited by 2,358 · see citing works
Neuroblastoma: biological insights into a clinical enigma
Brodeur, G. M. (2003) · Nature reviews. Cancer · doi:10.1038/nrc1014 · Cited by 2,161 · see citing works
Kamei, Y., Xu, L., Heinzel, T., Torchia, J., Kurokawa, R., Gloss, B., Lin, S.-C., Heyman, R. A., Rose, D. W., Glass, C. K., et al. (1996) · Cell · doi:10.1016/s0092-8674(00)81118-6 · Cited by 2,150 · see citing works
Matthay, K. K., Villablanca, J. G., Seeger, R. C., Stram, D. O., Harris, R. E., Ramsay, N. K. C., Swift, P. S., Shimada, H., Black, C. T., Brodeur, G. M., et al. (1999) · New England Journal of Medicine · doi:10.1056/nejm199910143411601 · Cited by 1,891 · see citing works
Nuclear Receptor Repression Mediated by a Complex Containing SMRT, mSin3A, and Histone Deacetylase
Nagy, L., Kao, H.-Y., Chakravarti, D., Lin, R. J., Hassig, C. A., Ayer, D. E., Schreiber, S. L., & Evans, R. M. (1997) · Cell · doi:10.1016/s0092-8674(00)80218-4 · Cited by 1,230 · see citing works
Regulation, substrates and functions of src
Brown, M. T., & Cooper, J. A. (1996) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/0304-419x(96)00003-0 · Cited by 1,177 · see citing works
Embryonic Stem Cells Express Neuronal Properties in Vitro
Bain, G., Kitchens, D. L., Yao, M., Huettner, J. E., & Gottlieb, D. I. (1995) · Developmental Biology · doi:10.1006/dbio.1995.1085 · Cited by 1,168 · see citing works
Nongenotropic, Sex-Nonspecific Signaling through the Estrogen or Androgen Receptors
Kousteni, S., Bellido, T., Plotkin, L. I., O’Brien, C. A., Bodenner, D., Li, H., Han, K., Gregorio, G. B. D., Katzenellenbogen, J. A., Katzenellenbogen, B. S., et al. (2001) · Cell · doi:10.1016/s0092-8674(01)00268-9 · Cited by 1,163 · see citing works
Yeatman, T. J. (2004) · Nature Reviews Cancer · doi:10.1038/nrc1366 · Cited by 1,113 · see citing works
Nonsteroid nuclear receptors: What Are genetic studies telling us about their role in real life?
Kastner, P., Mark, M. P., & Chambon, P. (1995) · Cell · doi:10.1016/0092-8674(95)90202-3 · Cited by 989 · see citing works
RHO GTPASES in neuronal morphogenesis
Luo, L. (2000) · Nature reviews. Neuroscience · doi:10.1038/35044547 · Cited by 985 · see citing works
Cytoskeletal dynamics and nerve growth
Mitchison, T. J., & Kirschner, M. W. (1988) · Neuron · doi:10.1016/0896-6273(88)90124-9 · Cited by 874 · see citing works
The promise of retinoids to fight against cancer
Altucci, L., & Gronemeyer, H. (2001) · Nature Reviews Cancer · doi:10.1038/35106036 · Cited by 773 · see citing works
Structure and regulation of Src family kinases
Boggon, T. J., & Eck, M. J. (2004) · Oncogene · doi:10.1038/sj.onc.1208081 · Cited by 712 · see citing works
Neuronal position in the developing brain is regulated by mouse disabled-1
Howell, B. W., Hawkes, R., Soriano, P., & Cooper, J. A. (1997) · Nature · doi:10.1038/39607 · Cited by 692 · see citing works
Migliaccio, A., Castoria, G., Domenico, M. D., de Falco, A., Bilancio, A., Lombardi, M., Barone, M. V., Ametrano, D., Zannini, M. S., Abbondanza, C., et al. (2000) · The EMBO Journal · doi:10.1093/emboj/19.20.5406 · Cited by 672 · see citing works
Andrews, P. W. (1984) · Developmental Biology · doi:10.1016/0012-1606(84)90316-6 · Cited by 670 · see citing works
Martin, G. S. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35073094 · Cited by 599 · see citing works
Src protein–tyrosine kinase structure and regulation
Roskoski, R. J. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.09.171 · Cited by 596 · see citing works
Boonyaratanakornkit, V., Scott, M. P., Ribon, V., Sherman, L., Anderson, S. M., Maller, J. L., Miller, W. T., & Edwards, D. P. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00304-5 · Cited by 590 · see citing works
Src kinase regulation by phosphorylation and dephosphorylation
Roskoski, R. J. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.03.012 · Cited by 577 · see citing works
The when and how of Src regulation
Cooper, J. A., & Howell, B. W. (1993) · Cell · doi:10.1016/0092-8674(93)90634-3 · Cited by 527 · see citing works
GROWTH CONE GUIDANCE: First Steps Towards a Deeper Understanding
Mueller, B. K. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.351 · Cited by 423 · see citing works
Sidell, N. (1982) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/68.4.589 · Cited by 378 · see citing works
Rac GTPases control axon growth, guidance and branching
Ng, J., Nardine, T. M., Harms, M. B., Tzu, J., Goldstein, A. Y. N., Sun, Y., Dietzl, G., Dickson, B. J., & Luo, L. (2002) · Nature · doi:10.1038/416442a · Cited by 340 · see citing works
Neuroblastoma: biology and molecular and chromosomal pathology
Schwab, M., Westermann, F., Hero, B., & Berthold, F. (2003) · The Lancet Oncology · doi:10.1016/s1470-2045(03)01166-5 · Cited by 329 · see citing works
Sidell, N., Altman, A., Haussler, M. R., & Seeger, R. C. (1983) · Experimental Cell Research · doi:10.1016/0014-4827(83)90184-2 · Cited by 318 · see citing works
Shupnik, M. A. (2004) · Oncogene · doi:10.1038/sj.onc.1208076 · Cited by 300 · see citing works
NCAM-dependent neurite outgrowth is inhibited in neurons from Fyn-minus mice.
Beggs, H. E., Soriano, P. M., & Maness, P. F. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.127.3.825 · Cited by 262 · see citing works
Chen, J. Y., Penco, S., Ostrowski, J., Balaguer, P., Pons, M., Starrett, J. E. J., Reczek, P. R., Chambon, P., & Gronemeyer, H. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb07102.x · Cited by 256 · see citing works
The biologic basis for neuroblastoma heterogeneity and risk stratification
Maris, J. M. (2005) · Current Opinion in Pediatrics · doi:10.1097/01.mop.0000150631.60571.89 · Cited by 199 · see citing works
Dynamic Shuttling and Intranuclear Mobility of Nuclear Hormone Receptors
Maruvada, P., Baumann, C. T., Hager, G. L., & Yen, P. M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m202752200 · Cited by 185 · see citing works
Govind, S., Kozma, R., Monfries, C. A. L., Lim, L., & Ahmed, S. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.152.3.579 · Cited by 162 · see citing works
Martin, G. S. (2004) · Oncogene · doi:10.1038/sj.onc.1208077 · Cited by 161 · see citing works
Alsayed, Y., Uddin, S., Mahmud, N., Lekmine, F., Kalvakolanu, D. V., Minucci, S., Bokoch, G., & Platanias, L. C. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m007431200 · Cited by 161 · see citing works
Aoki, K., Nakamura, T., & Matsuda, M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306382200 · Cited by 152 · see citing works
Aoki, K., Nakamura, T., Fujikawa, K., & Matsuda, M. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-10-0904 · Cited by 144 · see citing works
Signaling pathways in retinoid chemoprevention and treatment of cancer
Niles, R. M. (2004) · Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis · doi:10.1016/j.mrfmmm.2004.05.020 · Cited by 141 · see citing works
Pediatric neuroblastomas: genetic and epigenetic ‘Danse Macabre’
van Noesel, M. M., & Versteeg, R. (2003) · Gene · doi:10.1016/j.gene.2003.09.042 · Cited by 140 · see citing works
Rhythmic coupling among cells in the suprachiasmatic nucleus
Colwell, C. S. (2000) · Journal of Neurobiology · doi:10.1002/1097-4695(20000615)43:4 · Cited by 139 · see citing works
The role of Rho GTPases and associated kinases in regulating neurite outgrowth
Nikolić, M. (2002) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(01)00167-4 · Cited by 136 · see citing works
Neuroblastoma tumour genetics: clinical and biological aspects
Bown, N. P. (2001) · Journal of Clinical Pathology · doi:10.1136/jcp.54.12.897 · Cited by 129 · see citing works
Csk suppression of Src involves movement of Csk to sites of Src activity.
Howell, B. W., & Cooper, J. A. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.8.5402 · Cited by 127 · see citing works
Sarner, S., Kozma, R., Ahmed, S., & Lim, L. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.1.158-172.2000 · Cited by 125 · see citing works
Haussler, M. R., Sidell, N., Kelly, M. A., Donaldson, C. J., Altman, A., & Mangelsdorf, D. J. (1983) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.80.18.5525 · Cited by 109 · see citing works
Pan, J., Kao, Y., Joshi, S., Jeetendran, S., DiPette, D., & Singh, U. S. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03106.x · Cited by 94 · see citing works
Leng, X., Tsai, S. Y., O’Malley, B. W., & Tsai, M. (1993) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/0960-0760(93)90306-h · Cited by 92 · see citing works
Han, G.-R., Dohi, D. F., Lee, H., Rajah, R., Walsh, G. L., Hong, W. K., Cohen, P., & Kurie, J. M. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.21.13711 · Cited by 91 · see citing works
Protein tyrosine kinases Src and Csk: a tail’s tale
Cole, P. A., Shen, K., Qiao, Y., & Wang, D. (2003) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2003.08.009 · Cited by 89 · see citing works
Pallen, C. J. (2003) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026033452320 · Cited by 82 · see citing works
Hall, C., Michael, G. J., Cann, N., Ferrari, G., Teo, M., Jacobs, T., Monfries, C. A. L., & Lim, L. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-14-05191.2001 · Cited by 70 · see citing works
Association of Csk-homologous Kinase (CHK) (formerly MATK) with HER-2/ErbB-2 in Breast Cancer Cells
Zrihan‐Licht, S., Lim, J., Keydar, I., Sliwkowski, M. X., Groopman, J. E., & Avraham, H. K. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.3.1856 · Cited by 68 · see citing works
Zhoul, J., Hernández, G. M., Tu, S.-W., Huang, C., Tseng, C., & Hsieh, J. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-1481 · Cited by 59 · see citing works
All-trans-Retinoic Acid Inhibits Jun N-terminal Kinase-dependent Signaling Pathways
Lee, H., Walsh, G. L., Dawson, M. I., Hong, W. K., & Kurie, J. M. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.12.7066 · Cited by 54 · see citing works
RPA Stabilizes the XPA-Damaged DNA Complex through Protein−Protein Interaction
Wang, M., Mahrenholz, A. M., & Lee, S. (2000) · Biochemistry · doi:10.1021/bi000472q · Cited by 53 · see citing works
Self-citationDynamic Coupling Between the SH2 Domain and Active Site of the COOH Terminal Src Kinase, Csk
Wong, L. M., Lieser, S. A., Chie-Leon, B., Miyashita, O., Aubol, B. E., Shaffer, J., Onuchic, J. N., Jennings, P. A., Woods, V. L., & Adams, J. A. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.05.060 · Cited by 48 · see citing works
Braun, S., Lösel, R., Wehling, M., & Boldyreff, B. (2004) · FEBS Letters · doi:10.1016/j.febslet.2004.06.031 · Cited by 42 · see citing works
Hill, D. P., & Robertson, K. A. (1997) · Developmental Brain Research · doi:10.1016/s0165-3806(97)00076-x · Cited by 41 · see citing works
Self-citationAnalysis of CSK Homologous Kinase (CHK/HYL) in Hematopoiesis by Utilizing Gene Knockout Mice
Hamaguchi, I., Yamaguchi, N., Suda, J., Iwama, A., Hirao, A., Hashiyama, M., Aizawa, S.-I., & Suda, T. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.1003 · Cited by 41 · see citing works
Ultrastructural features of a human neuroblastoma cell line treated with retinoic acid
Robson, J. A., & Sidell, N. (1985) · Neuroscience · doi:10.1016/0306-4522(85)90284-2 · Cited by 39 · see citing works
Dey, N., Howell, B. W., De, P. K. R., & Durden, D. L. (2005) · Experimental Cell Research · doi:10.1016/j.yexcr.2005.02.029 · Cited by 37 · see citing works
Self-citationSubcellular Steroid/Nuclear Receptor Dynamics.
Kawata, M. (2001) · Archivum histologicum japonicum · doi:10.1679/aohc.64.353 · Cited by 32 · see citing works
Lee, M. Y., Jung, C., Lee, K., Choi, Y. H., Hong, S., & Cheong, J. (2002) · Diabetes · doi:10.2337/diabetes.51.12.3400 · Cited by 25 · see citing works
Phosphoryl Transfer Step in the C-terminal Src Kinase Controls Src Recognition
Lieser, S. A., Shindler, C., Aubol, B. E., Lee, S., Sun, G., & Adams, J. A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m411736200 · Cited by 24 · see citing works
Hill, D. P., & Robertson, K. A. (1998) · Brain Research Protocols · doi:10.1016/s1385-299x(97)00041-x · Cited by 24 · see citing works
Self-citationRegulation of collagenase-3 gene expression in osteoblastic and non-osteoblastic cell lines
Selvamurugan, N., Brown, R. J., & Partridge, N. C. (2000) · Journal of Cellular Biochemistry · doi:10.1002/1097-4644(20001101)79:2 · Cited by 24 · see citing works
Borghi, R., Venè, R., Arena, G., Schubert, D. A., Albini, A., & Tosetti, F. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01501.x · Cited by 13 · see citing works
The receptor tyrosine phosphatase CRYP? affects growth cone morphology
Mueller, B. K., Ledig, M. M., & Wahl, S. (2000) · Journal of Neurobiology · doi:10.1002/1097-4695(200008)44:2 · Cited by 12 · see citing works
Inhibition and activation of c-Src: the head and tail of a coin
Fukami, Y., Nagao, T., Iwasaki, T., & Sato, K.-I. (2002) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(02)00195-x · Cited by 12 · see citing works
Sidell, N., Pasquali, M., Malkapuram, S., Barua, A. B., Wanichkul, T., & Wada, R. K. (2003) · British Journal of Cancer · doi:10.1038/sj.bjc.6601108 · Cited by 10 · see citing works
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Dey, N., Barwick, B. G., Moreno, C. S., Ordanic-Kodani, M., Chen, Z., Oprea-Ilies, G. M., Tang, W., Catzavelos, C., Kerstann, K. F., Sledge, G. W., et al. (2013) · BMC Cancer · doi:10.1186/1471-2407-13-537 · Cited by 256 · see citing works
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Huang, G., Luo, Q., Rui, G., Zhang, W., Zhang, Q., Chen, Q., & Shen, D. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.00384-13 · Cited by 61 · see citing works
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Fishel, M. L., Colvin, E. S., Luo, M., Kelley, M. R., & Robertson, K. A. (2010) · Experimental Hematology · doi:10.1016/j.exphem.2010.08.011 · Cited by 43 · see citing works
Self-citationZeng, W., Zhang, C., Cheng, H., Wu, Y., Liu, J., Chen, Z., Huang, J., Ericksen, R. E., Chen, L., Zhang, H., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-00233-5 · Cited by 42 · see citing works
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Brown, G. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032373 · Cited by 38 · see citing works
Integrating retinoic acid signaling with brain function.
Luo, T., Wagner, E., & Dräger, U. C. (2009) · Developmental Psychology · doi:10.1037/0012-1649.45.1.139 · Cited by 37 · see citing works
Nuclear and Extra-Nuclear Effects of Retinoid Acid Receptors: How They Are Interconnected
Piskunov, A., Tanoury, Z. A., & Rochette‐Egly, C. (2014) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-94-017-9050-5_6 · Cited by 34 · see citing works
A Unique Cytoplasmic Localization of Retinoic Acid Receptor-γ and Its Regulations
Han, Y.-H., Zhou, H., Kim, J. H., Yan, T., Lee, K.-H., Wu, H., Lin, F., Lu, N., Liu, J., Zeng, J.-Z., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.007708 · Cited by 33 · see citing works
Deregulation of All-Trans Retinoic Acid Signaling and Development in Cancer
Brown, G. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241512089 · Cited by 34 · see citing works
Mezquita, B., Mezquita, P., Pau, M., Gasa, L., Navarro, L., Samitier, M., Pons, M., & Mezquita, C. (2018) · Scientific Reports · doi:10.1038/s41598-018-25526-1 · Cited by 32 · see citing works
Zhu, X., Wang, W., Zhang, X., Bai, J., Chen, G., Li, L., & Li, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0143255 · Cited by 31 · see citing works
Khatib, T., Marini, P., Nunna, S., Chisholm, D. R., Whiting, A., Redfern, C. P. F., Greig, I. R., & McCaffery, P. J. A. (2019) · Cell Communication and Signaling · doi:10.1186/s12964-019-0352-4 · Cited by 31 · see citing works
Barceinas, R. S. Q., García-Regalado, A., Aréchaga-Ocampo, E., Villegas‐Sepúlveda, N., & la Rosa, C. H. G.-D. (2015) · BioMed Research International · doi:10.1155/2015/404368 · Cited by 28 · see citing works
Pan-PI-3 kinase inhibitor SF1126 shows antitumor and antiangiogenic activity in renal cell carcinoma
Joshi, S., Singh, A. R., & Durden, D. L. (2015) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-014-2639-x · Cited by 25 · see citing works
Self-citationNon-canonical retinoid signaling in neural development, regeneration and synaptic function
Piazza, A., Carlone, R. L., & Spencer, G. E. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2024.1371135 · Cited by 24 · see citing works
Weng, X., Sheng, Y., Ge, D.-Z., Wu, J., Shi, L., & Cai, X. (2016) · Leukemia Research · doi:10.1016/j.leukres.2016.03.008 · Cited by 21 · see citing works
Girardi, C. S., Rostirolla, D. C., Lini, F. J. M., Brum, P. O., Delgado, J., Ribeiro, C. T., Teixeira, A. A., Peixoto, D. O., Heimfarth, L., Kunzler, A., et al. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2018.11.014 · Cited by 21 · see citing works
Addae, C., Cheng, H., & Martinez‐Ceballos, E. (2013) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph10105244 · Cited by 20 · see citing works
Apoptosis regulation by the tyrosine-protein kinase CSK
Fortner, A., Chera, A., Tanca, A., & Bucur, O. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1078180 · Cited by 19 · see citing works
Retinoids and glucocorticoids target common genes in hippocampal HT 22 cells
Brossaud, J., Roumes, H., Moisan, M., Pallet, V., Redonnet, A., & Corcuff, J. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12192 · Cited by 19 · see citing works
Uchibe, K., Son, J., Larmour, C., Pacifici, M., Enomoto‐Iwamoto, M., & Iwamoto, M. (2016) · Journal of Orthopaedic Research® · doi:10.1002/jor.23347 · Cited by 19 · see citing works
Ashton, A., Stoney, P. N., Ransom, J., & McCaffery, P. J. A. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-0964-5 · Cited by 20 · see citing works
Fetal Exposure to Alcohol, Developmental Brain Anomaly, and Vitamin A Deficiency: A Case Report
Goez, H., Scott, O., & Hasal, S. (2011) · Journal of Child Neurology · doi:10.1177/0883073810380458 · Cited by 13 · see citing works
Sakai, Y., & Dräger, U. C. (2010) · Methods in molecular biology · doi:10.1007/978-1-60327-325-1_16 · Cited by 10 · see citing works
Immunolocalization of retinoic acid receptor-alpha, -beta, and -gamma, in bovine and canine sperm
Kasimanickam, V. R., Kasimanickam, R. K., & Rogers, H. A. (2013) · Theriogenology · doi:10.1016/j.theriogenology.2013.01.011 · Cited by 10 · see citing works
MSK1 and Nuclear Receptors Signaling
Piskunov, A., & Rochette‐Egly, C. (2013) · Cited by 9 · see citing works
Zhang, X., Yuan, X., Chen, L., Wei, H., Chen, J., & Li, T. (2017) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2017.05.007 · Cited by 9 · see citing works
Carter, C. J. (2011) · ISRN Neurology · doi:10.5402/2011/394678 · Cited by 9 · see citing works
Ligands and DNA in the allosteric control of retinoid receptors function
Germain, P., Rochel, N., & Bourguet, W. (2021) · Essays in Biochemistry · doi:10.1042/ebc20200168 · Cited by 8 · see citing works
Bexarotene – a novel modulator of AURKA and the primary cilium in VHL -deficient cells
Chowdhury, P., Powell, R. T., STEPHAN, C. C., Uray, I. P., Talley, T., Karki, M., Tripathi, D. N., Park, Y. S., Mancini, M. A., Davies, P. J., et al. (2018) · Journal of Cell Science · doi:10.1242/jcs.219923 · Cited by 8 · see citing works
Czimmerer, Z., Halász, L., & Nagy, L. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.609099 · Cited by 7 · see citing works
Buchanan, F. Q., Rochette‐Egly, C., & Asson–Batres, M. A. (2011) · Cell and Tissue Research · doi:10.1007/s00441-011-1247-x · Cited by 7 · see citing works
Wnt-β-Catenin Pathway Regulates Vascular Mimicry in Triple Negative Breast Cancer
Aske, J. C. (2013) · Journal of Cytology & Histology · doi:10.4172/2157-7099.1000198 · Cited by 7 · see citing works
Dynamics of vitamin A uptake, storage, and utilization in vocal fold mucosa
Nishimoto, K., Toya, Y., Davis, C. R., Tanumihardjo, S. A., & Welham, N. V. (2020) · Molecular Metabolism · doi:10.1016/j.molmet.2020.101025 · Cited by 6 · see citing works
The role of RARG in solid tumor progression and therapeutic potential
Guo, S., Han, H., Ding, B., Zhang, W., & Qin, L. (2026) · Discover Oncology · doi:10.1007/s12672-026-04706-w · Cited by 4 · see citing works
Ogasawara, S., Chuman, Y., Michiba, T., Kamada, R., Imagawa, T., & Sakaguchi, K. (2019) · Journal of Biochemistry (Tokyo) · doi:10.1093/jb/mvy119 · Cited by 4 · see citing works
Targeting Non-Genomic Activity of Retinoic Acid Receptor-Gamma by Acacetin
Liu, J., Huang, J., & Zeng, J.-Z. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9585-1_2 · Cited by 2 · see citing works
Butler, A. M., Chisholm, D. R., Tomlinson, C. W. E., Khatib, T., Clark, J., Wan, S., Coveney, P. V., Greig, I. R., McCaffery, P. J. A., Pohl, E., et al. (2025) · ACS Omega · doi:10.1021/acsomega.5c00934 · Cited by 1 · see citing works
Proteolytic processing of the Alzheimer APP protein family during neuronal differentiation
Holback, S. (2009) · KTH Publication Database DiVA (KTH Royal Institute of Technology) · Cited by 1 · see citing works
Control of Gene Expression by Nuclear Retinoic Acid Receptors
Carrier, M., & Rochette‐Egly, C. (2015) · doi:10.1002/9781118628003.ch5 · Cited by 1 · see citing works
Retinoid Signaling in the Central Nervous System
McCaffery, P. J. A., & Krężel, W. (2015) · Wiley eBooks · doi:10.1002/9781118628003.ch19 · Cited by 1 · see citing works
Sinalização não-genômica do retinol mediada por espécies reativas
Gelain, D. P. (2008) · Americanae (AECID Library)
ATRA AS A POTENTIAL ANTIMETASTATIC AGENT IN COLORECTAL ADENOCARCINOMA
Edwards (2014) · OnLine Journal of Biological Sciences · doi:10.3844/ojbsci.2014.102.107
- Authors
- Dey, N., De, P. K., Wang, M., Zhang, H., Dobrota, E. A., Robertson, K. A., & Durden, D. L.
- Affiliations
- Emory University (US)
- Indiana University Indianapolis (US)
- Riley Hospital for Children (US)
- Corresponding author
- Robertson, Kent A.
- Durden, Donald L.
- Venue
- Molecular and Cellular Biology
- Publisher
- Informa UK Limited
- Published
- 2007-06
- Volume
- 27
- Issue
- 11
- Pages
- 4179-4197
- ISSN
- 0270-7306 (ISSN-L)
- 1098-5549
- PMC
- PMC1900023
- OpenAlex
- W2136392162
- Cited by
- 62
- References
- 76
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 1 · 2023: 2 · 2022: 1 · 2021: 1 · 2020: 2 · 2019: 3 · 2018: 5 · 2017: 2 · 2016: 4 · 2015: 6 · 2014: 5 · 2013: 11
- FWCI
- 1.72
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular and Cellular Biology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Aflac
- Georgia Cancer Coalition
- Emory University
- National Institutes of Health (CA94233)
- Winship Cancer Institute
- National Cancer Institute (CA 94233, R56CA094233, R01CA094233)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinoids in leukemia and cellular processes
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nuclear Receptors and Signaling
- Keywords
- Src kinase, Csk, retinoic acid receptor gamma, retinoic acid signaling, neurite outgrowth, neuronal differentiation, Rac1 activation, non-genomic signaling, nuclear receptors, proline-rich region, all-trans retinoic acid
- MeSH terms
- Retinoic Acid Receptor alpha, Animals, Antineoplastic Agents, Cell Differentiation, Cell Line, Enzyme Inhibitors, Humans, Protein-Tyrosine Kinases, Pyrazoles, Pyrimidines, Recombinant Fusion Proteins, Tretinoin, Signal Transduction, Genes, src, Proto-Oncogene Proteins pp60(c-src), Neurites, Receptors, Retinoic Acid, rac1 GTP-Binding Protein
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