Rapid, Nongenomic Actions of Retinoic Acid on Phosphatidylinositol-3-Kinase Signaling Pathway Mediated by the Retinoic Acid Receptor
Open accessAbstract
Retinoic acid (RA) treatment of SH-SY5Y neuroblastoma cells results in activation of phosphatidylinositol-3-kinase (PI3K) signaling pathway, and this activation is required for RA-induced differentiation. Here we show that RA activates PI3K and ERK1/2 MAPK signaling pathways through a rapid, nongenomic mechanism that does not require new gene transcription or newly synthesized proteins. Activation of PI3K by RA appears to involve the classical nuclear receptor, retinoic acid receptor (RAR), on the basis of the pharmacological profile of the activation, loss, and gain of function experiments with mouse embryo fibroblast-RAR(alpha beta gamma)(L-/L-) null cells, and the physical association between liganded RAR and PI3K activity. The association of RAR with the two subunits of PI3K was differentially regulated by the ligand. Immunoprecipitation experiments performed in SH-SY5Y cells showed stable association between RARalpha and p85, the regulatory subunit of PI3K, independently of the presence of RA. In contrast, ligand administration increased the association of p110, the catalytic subunit of PI3K, to this complex. The intracellular localization of RAR proved to be relevant for PI3K activation. A chimerical RAR fusing c-Src myristylation domain to the N terminus of RARalpha (Myr-RARalpha) was targeted to plasma membrane. Transfection of Myr-RARalpha to mouse embryo fibroblast-RAR(alpha beta gamma)(L-/L-) null cells and COS-7 cells results in strong activation of the PI3K signaling pathway, although both in the absence as well in the presence of RA. Our results support a mechanism in which ligand binding to RAR would play a major role in the assembly and intracellular location of a signaling complex involving RAR and the subunits of PI3K.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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 [121]
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 [121]
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 [121]
Cites
1 retracted
Sun, M., Yang, L., Feldman, R. I., Sun, X.-M., Bhalla, K. N., Jove, R., Nicosia, S. V., & Cheng, J. Q. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306295200 · Cited by 173 · see citing works
RetractedBrown, D. A., & Rose, J. K. (1992) · Cell · doi:10.1016/0092-8674(92)90189-j · Cited by 2,921 · see citing works
Production of high-titer helper-free retroviruses by transient transfection.
Pear, W. S., Nolan, G. P., Scott, M. L., & Baltimore, D. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.18.8392 · Cited by 2,267 · see citing works
Morgenstern, J. P., & Land, H. (1990) · Nucleic Acids Research · doi:10.1093/nar/18.12.3587 · Cited by 2,099 · 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
Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase
Simoncini, T., Hafezi‐Moghadam, A., Brazil, D. P., Ley, K. F., Chin, W. W., & Liao, J. K. (2000) · Nature · doi:10.1038/35035131 · Cited by 1,437 · see citing works
Principles for modulation of the nuclear receptor superfamily
Gronemeyer, H., Gustafsson, J.-Å., & Laudet, V. (2004) · Nature Reviews Drug Discovery · doi:10.1038/nrd1551 · Cited by 1,228 · see citing works
Katso, R., Okkenhaug, K., Ahmadi, K., White, S., Timms, J. F., & Waterfield, M. D. (2001) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.17.1.615 · Cited by 1,204 · 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
Razandi, M., Pedram, A., Greene, G. L., & Levin, E. R. (1999) · Molecular Endocrinology · doi:10.1210/mend.13.2.0239 · Cited by 1,046 · see citing works
Nongenomic actions of steroid hormones
Lösel, R., & Wehling, M. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1009 · Cited by 980 · see citing works
Tyrosine kinase/p21ras/MAP‐kinase pathway activation by estradiol‐receptor complex in MCF‐7 cells.
Migliaccio, A., Domenico, M. D., Castoria, G., de Falco, A., Bontempo, P., Nola, E., & Auricchio, F. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00471.x · Cited by 950 · see citing works
Kousteni, S. (2001) · Cell · doi:10.1016/s0092-8674(02)08100-x · Cited by 749 · see citing works
Integration of the extranuclear and nuclear actions of estrogen
Levin, E. R. (2005) · Molecular Endocrinology · doi:10.1210/me.2004-0390 · Cited by 708 · see citing works
SPECIFIC, NONGENOMIC ACTIONS OF STEROID HORMONES
Wehling, M. (1997) · Annual Review of Physiology · doi:10.1146/annurev.physiol.59.1.365 · Cited by 657 · see citing works
Thiele, C. J., Reynolds, C. P., & Israel, M. A. (1985) · Nature · doi:10.1038/313404a0 · Cited by 649 · see citing works
Hafezi‐Moghadam, A., Simoncini, T., Yang, Z., Limbourg, F. P., Plumier, J.-C., Rebsamen, M. C., Hsieh, C.-M., Chui, D.-S., Thomas, K. L., Prorock, A. J., et al. (2002) · Nature Medicine · doi:10.1038/nm0502-473 · Cited by 595 · see citing works
Påhlman, S., Ruusala, A.-I., Abrahamsson, L., Mattsson, M. E. K., & Esscher, T. (1984) · Cell Differentiation · doi:10.1016/0045-6039(84)90038-1 · Cited by 571 · see citing works
Nature of Functional Estrogen Receptors at the Plasma Membrane
Pedram, A., Razandi, M., & Levin, E. R. (2006) · Molecular Endocrinology · doi:10.1210/me.2005-0525 · Cited by 523 · see citing works
Yu, J., Zhang, Y., McIlroy, J., Rordorf-Nikolic, T., Orr, G. A., & Backer, J. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.3.1379 · Cited by 520 · see citing works
Proximal Events in Signaling by Plasma Membrane Estrogen Receptors
Razandi, M., Pedram, A., Park, S. T., & Levin, E. R. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m205692200 · Cited by 474 · see citing works
PI3‐kinase in concert with Src promotes the S‐phase entry of oestradiol‐stimulated MCF‐7 cells
Castoria, G., Migliaccio, A., Bilancio, A., Domenico, M. D., de Falco, A., Lombardi, M., Fiorentino, R., Varricchio, L., Barone, M. V., & Auricchio, F. (2001) · The EMBO Journal · doi:10.1093/emboj/20.21.6050 · Cited by 469 · see citing works
Klippel, A., Reinhard, C., Kavanaugh, W. M., Apell, G., Escobedo, M.-A., & Williams, L. T. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.8.4117 · Cited by 441 · see citing works
Palmitoylation-dependent Estrogen Receptor α Membrane Localization: Regulation by 17β-Estradiol
Acconcia, F., Ascenzi, P., Bocedi, A., Spisni, E., Tomasi, V., Trentalance, A., Visca, P., & Marino, M. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-07-0547 · Cited by 440 · see citing works
Cross, F. R., Garber, E. A., Pellman, D. S., & Hanafusa, H. (1984) · Molecular and Cellular Biology · doi:10.1128/mcb.4.9.1834 · Cited by 439 · see citing works
Retinoid signalling in the development of the central nervous system
Maden, M. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn963 · Cited by 428 · 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
Non-genomic actions of sex steroid hormones
Simoncini, T., & Genazzani, A. R. (2003) · European Journal of Endocrinology · doi:10.1530/eje.0.1480281 · Cited by 369 · see citing works
Plasma Membrane Estrogen Receptors Exist and Functions as Dimers
Razandi, M., Pedram, A., Merchenthaler, I. J., Greene, G. L., & Levin, E. R. (2004) · Molecular Endocrinology · doi:10.1210/me.2004-0115 · Cited by 330 · see citing works
Razandi, M., Alton, G., Pedram, A., Ghonshani, S., Webb, P., & Levin, E. R. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.5.1633-1646.2003 · Cited by 319 · see citing works
López‐Carballo, G., Moreno, L., Masiá, S., Pérez, P., & Barettino, D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m201869200 · Cited by 301 · see citing works
Self-citationde Thé, H., Marchio, A., Tiollais, P., & Dejean, A. (1987) · Nature · doi:10.1038/330667a0 · Cited by 284 · see citing works
Ueki, K., Fruman, D. A., Brachmann, S. M., Tseng, Y., Cantley, L. C., & Kahn, C. R. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.3.965-977.2002 · Cited by 282 · see citing works
Function of Vitamin A in Vertebrate Embryonic Development
Zile, M. H. (2001) · The Journal of Nutrition · doi:10.1093/jn/131.3.705 · Cited by 263 · see citing works
Cao, X., Kambe, F., Moeller, L. C., Refetoff, S., & Seo, H. (2004) · Molecular Endocrinology · doi:10.1210/me.2004-0093 · Cited by 241 · see citing works
Rapid effects of retinoic acid on CREB and ERK phosphorylation in neuronal cells
Cañón, E., Cosgaya, J. M., Scsucova, S., & Aranda, A. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-05-0439 · Cited by 184 · see citing works
Capiati, D. A., Benassati, S., & Boland, R. (2002) · Journal of Cellular Biochemistry · doi:10.1002/jcb.10191 · Cited by 126 · see citing works
Simoncini, T., Genazzani, A. R., & Liao, J. K. (2002) · Circulation · doi:10.1161/hc1102.105267 · Cited by 125 · see citing works
Rapid signaling at the plasma membrane by a nuclear receptor for thyroid hormone
Storey, N. M., Gentile, S., Ullah, H., Russo, A., Muessel, M. J., Erxleben, C. F. J., & Armstrong, D. L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600089103 · Cited by 123 · see citing works
Transcriptional activities of retinoic acid receptors.
Lefebvre, P., Martin, P. J., Flajollet, S., Dedieu, S., Billaut, X., & Lefebvre, B. (2005) · Vitamins and hormones · doi:10.1016/s0083-6729(05)70007-8 · Cited by 118 · see citing works
Altucci, L., Rossin, A., Hirsch, O., Nebbioso, A., Vitoux, D., Wilhelm, E., Guidez, F., Simone, M. D., Schiavone, E. M., Grimwade, D. J., et al. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-3569 · Cited by 113 · see citing works
Characterization of DNA binding and retinoic acid binding properties of retinoic acid receptor.
Yang, N., Schüle, R., Mangelsdorf, D. J., & Evans, R. M. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.9.3559 · Cited by 109 · see citing works
Activation of Protein Kinase Cδ by All-trans-retinoic Acid
Kambhampati, S., Li, Y., Verma, A. K., Sassano, A., Majchrzak, B., Deb, D. K., Parmar, S., Giafis, N., Kalvakolanu, D. V., Rahman, A., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301523200 · Cited by 107 · see citing works
Vertino, A. M., Bula, C. M., Chen, J., Almeida, M., Han, L., Bellido, T., Kousteni, S., Norman, A. W., & Manolagas, S. C. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m410720200 · Cited by 105 · see citing works
Klippel, A., Escobedo, J. A., Hu, Q., & Williams, L. T. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.9.5560 · Cited by 104 · see citing works
Chambliss, K. L., & Shaul, P. W. (2002) · Steroids · doi:10.1016/s0039-128x(01)00177-5 · Cited by 94 · 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
Uruno, A., Sugawara, A., Kanatsuka, H., Kagechika, H., Saito, A. M., Sato, K., Kudo, M., Takeuchi, K., & Ito, S. (2005) · Circulation · doi:10.1161/circulationaha.104.500959 · Cited by 85 · see citing works
Johnson, A. T., Klein, E. S., Gillett, S. J., Wang, L., Song, T. K., Pino, M. E., & Chandraratna, R. A. S. (1995) · Journal of Medicinal Chemistry · doi:10.1021/jm00024a003 · Cited by 85 · see citing works
Barettino, D., Bugge, T. H., Bartůněk, P., Vivanco, M. D., Sonntag-Buck, V., Beug, H., Zenke, M., & Stunnenberg, H. G. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb05779.x · Cited by 81 · see citing works
Self-citationZhao, Q. C., Tao, J., Zhu, Q., Jia, P.-M., Dou, A.-X., Li, X., Cheng, F., Waxman, S., Chen, G.-Q., Chen, S.-J., et al. (2003) · Leukemia · doi:10.1038/sj.leu.2403226 · Cited by 79 · see citing works
Appel, B., & Eisen, J. S. (2003) · Neuron · doi:10.1016/s0896-6273(03)00688-3 · Cited by 69 · see citing works
Cabrera-Poch, N., Sánchez‐Ruiloba, L., Rodríguez‐Martínez, M., & Iglesias, T. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m312242200 · Cited by 69 · see citing works
Kim, Y. S., MacDonald, P. N., Dedhar, S., & Hruska, K. A. (1996) · Endocrinology · doi:10.1210/en.137.9.3649 · Cited by 64 · see citing works
Farias, E., Marzan, C., & Mira-y-Lopez, R. (2004) · Oncogene · doi:10.1038/sj.onc.1208347 · Cited by 52 · see citing works
Bastien, J., Plassat, J. L., Payrastre, B., & Rochette‐Egly, C. (2005) · Oncogene · doi:10.1038/sj.onc.1209241 · Cited by 46 · see citing works
Classical and novel steroid actions: a unified but complex view
Valverde, M. A., & Parker, M. G. (2002) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(02)02075-3 · Cited by 43 · see citing works
Antonyak, M. A., Boehm, J. E., & Cerione, R. A. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m112259200 · Cited by 38 · see citing works
Liou, J., Ho, S., Shen, M., Liao, Y.-P., Chiu, W., & Kang, K. (2005) · Journal of Cell Science · doi:10.1242/jcs.02603 · Cited by 34 · see citing works
Zhang, L., Nadzan, A. M., Heyman, R. A., Love, D. L., Mais, D. E., Croston, G. E., Lamph, W. W., & Boehm, M. F. (1996) · Journal of Medicinal Chemistry · doi:10.1021/jm960285j · Cited by 31 · see citing works
Palomino, T., Sánchez‐Pacheco, A., de la Peña, P., & Aranda, A. (1998) · The FASEB Journal · doi:10.1096/fasebj.12.12.1201 · Cited by 30 · see citing works
Hughes, P., Zhao, Y., Chandraratna, R. A. S., & Brown, G. (2005) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20579 · Cited by 29 · see citing works
Is there a role for retinoids to treat minimal residual disease in neuroblastoma?
Matthay, K. K., & Reynolds, C. P. (2000) · British Journal of Cancer · doi:10.1054/bjoc.2000.1430 · Cited by 24 · see citing works
Bennani, Y. L., Marron, K. S., Mais, D. E., Flatten, K. S., Nadzan, A. M., & Boehm, M. F. (1998) · The Journal of Organic Chemistry · doi:10.1021/jo971409i · Cited by 18 · see citing works
Carter, C. A. (2003) · Experimental and Molecular Pathology · doi:10.1016/s0014-4800(03)00033-9 · Cited by 10 · see citing works
Flagged first, then by citations
2 of the 67 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Retinoic acid receptors: From molecular mechanisms to cancer therapy
di Masi, A., Leboffe, L., De Marinis, E., Pagano, F., Cicconi, L., Rochette-Egly, C., Lo-Coco, F., Ascenzi, P., & Nervi, C. (2015) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2014.12.003 · Cited by 403 · see citing works
Vitamin A and retinoid signaling: genomic and nongenomic effects
Al Tanoury, Z., Piskunov, A., & Rochette-Egly, C. (2013) · Journal of Lipid Research · doi:10.1194/jlr.r030833 · Cited by 408 · see citing works
Hall, J. A., Cannons, J. L., Grainger, J. R., dos Santos, L. M., Hand, T. W., Naik, S., Wohlfert, E. A., Chou, D. B., Oldenhove, G., Robinson, M., et al. (2011) · Immunity · doi:10.1016/j.immuni.2011.03.003 · Cited by 375 · see citing works
Retinoid pathway and cancer therapeutics
Bushue, N., & Wan, Y. Y. (2010) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2010.07.003 · Cited by 373 · see citing works
From carrot to clinic: an overview of the retinoic acid signaling pathway
Theodosiou, M., Laudet, V., & Schubert, M. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0268-z · Cited by 329 · see citing works
Aldehyde Dehydrogenases: Not Just Markers, but Functional Regulators of Stem Cells
Vassalli, G. (2019) · Stem Cells International · doi:10.1155/2019/3904645 · Cited by 300 · see citing works
Vitamin A signaling and homeostasis in obesity, diabetes, and metabolic disorders
Blaner, W. S. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.01.006 · Cited by 287 · see citing works
Dynamic and combinatorial control of gene expression by nuclear retinoic acid receptors (RARs)
Rochette‐Egly, C., & Germain, P. (2009) · Nuclear Receptor Signaling · doi:10.1621/nrs.07005 · Cited by 244 · see citing works
Retinoic Acid and Its Derivatives in Skin
Szymański, Ł., Skopek, R., Palusińska, M., Schenk, T., Stengel, S., Lewicki, S., Kraj, L., Kamiński, P., & Zelent, A. (2020) · Cells · doi:10.3390/cells9122660 · Cited by 229 · see citing works
Aldehyde dehydrogenases and cancer stem cells
Xu, X., Chai, S., Wang, P., Zhang, C., Yang, Y., Yang, Y., & Wang, K. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.08.018 · Cited by 205 · see citing works
Hepatic metabolism of retinoids and disease associations
Shirakami, Y., Lee, S.-A., Clugston, R. D., & Blaner, W. S. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2011.06.023 · Cited by 203 · see citing works
The sodium iodide symporter (NIS): Regulation and approaches to targeting for cancer therapeutics
Kogai, T., & Brent, G. A. (2012) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2012.06.007 · Cited by 196 · see citing works
Control of mammalian germ cell entry into meiosis
Feng, C.-W. A., Bowles, J., & Koopman, P. A. (2013) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2013.09.026 · Cited by 161 · see citing works
Retinoids and rexinoids in cancer prevention: from laboratory to clinic
Uray, I. P., Dmitrovsky, E., & Brown, P. H. (2015) · Seminars in Oncology · doi:10.1053/j.seminoncol.2015.09.002 · Cited by 153 · see citing works
The success and the challenge of all-trans retinoic acid in the treatment of cancer
Ni, X., Hu, G., & Cai, X. (2018) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2018.1509201 · Cited by 149 · see citing works
The molecular physiology of nuclear retinoic acid receptors. From health to disease
Duong, V., & Rochette‐Egly, C. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2010.10.007 · Cited by 137 · see citing works
Retinoic acid regulates Kit translation during spermatogonial differentiation in the mouse
Busada, J. T., Chappell, V. A., Niedenberger, B. A., Kaye, E. P., Keiper, B. D., Hogarth, C. A., & Geyer, C. B. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.10.020 · Cited by 137 · see citing works
Retinoids and breast cancer: From basic studies to the clinic and back again
Garattini, E., Bolis, M., Garattini, S. K., Fratelli, M., Centritto, F., Paroni, G., Gianni’, M., Zanetti, A., Pagani, A., Fisher, J. N., et al. (2014) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2014.01.001 · Cited by 135 · see citing works
Synaptic retinoic acid signaling and homeostatic synaptic plasticity
Chen, L., Lau, A. G., & Sarti, F. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.12.004 · Cited by 128 · see citing works
Meseguer, S., Mudduluru, G., Escamilla, J. M., Allgayer, H., & Barettino, D. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.167817 · Cited by 127 · see citing works
Self-citationDetection of Temperature Difference in Neuronal Cells
Tanimoto, R., Hiraiwa, T., Nakai, Y., Shindo, Y., Oka, K., Hiroi, N. F., & Funahashi, A. (2016) · Scientific Reports · doi:10.1038/srep22071 · Cited by 127 · see citing works
ATRA and KL promote differentiation toward the meiotic program of male germ cells.
Pellegrini, M., Filipponi, D., Gori, M., Barrios, F., Lolicato, F., Grimaldi, P., Rossi, P., Jannini, E. A., Geremia, R., & Dolci, S. (2008) · Cell Cycle · doi:10.4161/cc.7.24.7262 · Cited by 126 · see citing works
Stavridis, M. P., Collins, B. J., & Storey, K. G. (2010) · Development · doi:10.1242/dev.043117 · Cited by 124 · see citing works
Seeing through the dark: New insights into the immune regulatory functions of vitamin A
Brown, C. C., & Noelle, R. J. (2015) · European Journal of Immunology · doi:10.1002/eji.201344398 · Cited by 116 · see citing works
Nuclear retinoic acid receptors: Conductors of the retinoic acid symphony during development
Samarut, É., & Rochette‐Egly, C. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.03.025 · Cited by 113 · see citing works
Preventing adolescent stress-induced cognitive and microbiome changes by diet
Provensi, G., Schmidt, S. D., Boehme, M., Bastiaanssen, T. F. S., Rani, B., Costa, A., Busca, K., Fouhy, F., Strain, C., Stanton, C., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820832116 · Cited by 110 · see citing works
A coordinated phosphorylation cascade initiated by p38MAPK/MSK1 directs RARα to target promoters
Bruck, N., Vitoux, D., Ferry, C., Duong, V., Bauer, A., de Thé, H., & Rochette‐Egly, C. (2009) · The EMBO Journal · doi:10.1038/emboj.2008.256 · Cited by 108 · see citing works
Yasuhara, R., Yuasa, T., Williams, J. A., Byers, S. W., Shah, S., Pacifici, M., Iwamoto, M., & Enomoto‐Iwamoto, M. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.053926 · Cited by 101 · see citing works
The Role of Retinoic Acid (RA) in Spermatogonial Differentiation1
Busada, J. T., & Geyer, C. B. (2015) · Biology of Reproduction · doi:10.1095/biolreprod.115.135145 · Cited by 98 · see citing works
PI3K/AKT and ERK regulate retinoic acid-induced neuroblastoma cellular differentiation
Qiao, J., Paul, P., Lee, S., Qiao, L., Josifi, E., Tiao, J. R., & Chung, D. H. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.06.125 · Cited by 97 · see citing works
Rochette‐Egly, C. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2014.04.003 · Cited by 97 · see citing works
Leonarduzzi, G., Sottero, B., & Poli, G. (2010) · Pharmacology and Therapeutics · doi:10.1016/j.pharmthera.2010.08.003 · Cited by 89 · see citing works
Piskunov, A., & Rochette-Egly, C. (2012) · Oncogene · doi:10.1038/onc.2011.499 · Cited by 95 · see citing works
Busada, J. T., Niedenberger, B. A., Velte, E. K., Keiper, B. D., & Geyer, C. B. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.08.004 · Cited by 93 · see citing works
Katsuki, H., Kurimoto, E., Takemori, S., Kurauchi, Y., Hisatsune, A., Isohama, Y., Izumi, Y., Kume, T., Shudo, K., & Akaike, A. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06171.x · Cited by 88 · see citing works
Developmental and genetic aspects of congenital diaphragmatic hernia
Veenma, D. C. M., de Klein, A., & Tibboel, D. (2012) · Pediatric Pulmonology · doi:10.1002/ppul.22553 · Cited by 84 · see citing works
The rhythm of retinoids in the brain
Ransom, J., Morgan, P. J., McCaffery, P. J. A., & Stoney, P. N. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12620 · Cited by 79 · see citing works
The Use of Retinoids for the Prevention and Treatment of Skin Cancers: An Updated Review
Ramchatesingh, B. L., Villarreal, A. M., Arcuri, D., Lagacé, F., Setah, S. A., Touma, F., Al-Badarin, F., & Litvinov, I. V. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232012622 · Cited by 73 · see citing works
Carter, C. J., Farrar, N. R., Carlone, R. L., & Spencer, G. E. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.03.023 · Cited by 69 · see citing works
Oncogenic Potential of Retinoic Acid Receptor-γ in Hepatocellular Carcinoma
Yan, T., Wu, H., Zhang, H., Lu, N., Ye, P., Yu, F.-H., Zhou, H., Li, W., Cao, X., Lin, Y., et al. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-2968 · Cited by 69 · see citing works
Kou, Y. H., Li, L., Li, H., Tan, Y., Li, B., Wang, K., & Du, B. (2016) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2016.09.061 · Cited by 69 · see citing works
Vitamin A Deficiency and Alterations in the Extracellular Matrix
Barber, T., Esteban-Pretel, G., Marín, M., & Timoneda, J. (2014) · Nutrients · doi:10.3390/nu6114984 · Cited by 63 · see citing works
Why Differentiation Therapy Sometimes Fails: Molecular Mechanisms of Resistance to Retinoids
Chlapek, P., Sláviková, V., Mazánek, P., Štěrba, J., & Veselská, R. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19010132 · Cited by 65 · see citing works
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
Iqbal, S., & Naseem, I. (2014) · Nutrition · doi:10.1016/j.nut.2014.12.014 · Cited by 61 · see citing works
Mechanisms of Feedback Regulation of Vitamin A Metabolism
O'Connor, C., Varshosaz, P., & Moise, A. (2022) · Nutrients · doi:10.3390/nu14061312 · Cited by 53 · see citing works
Targeting Angiogenesis for Controlling Neuroblastoma
Choudhury, S. R., Karmakar, S., Banik, N. L., & Ray, S. K. (2011) · Journal of Oncology · doi:10.1155/2012/782020 · Cited by 57 · see citing works
Lin, Y., Persaud, S. D., Nhieu, J., & Wei, L. (2017) · Endocrinology · doi:10.1210/en.2017-00353 · Cited by 57 · see citing works
Todd, L. J., Suarez, L., Quinn, C. H., & Fischer, A. J. (2017) · Stem Cells · doi:10.1002/stem.2742 · Cited by 54 · see citing works
García-Regalado, A., Vargas, M. A., García-Carrancá, A. M., Aréchaga-Ocampo, E., & la Rosa, C. H. G.-D. (2013) · Molecular Cancer · doi:10.1186/1476-4598-12-44 · Cited by 51 · see citing works
Ohashi, E., Kogai, T., Kagechika, H., & Brent, G. A. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-3234 · Cited by 47 · see citing works
Retinoic acid and depressive disorders: Evidence and possible neurobiological mechanisms
Hu, P., van Dam, A., Wang, Y., Lucassen, P. J., & Zhou, J.-N. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.02.013 · Cited by 47 · see citing works
Mezquita, B., & Mezquita, C. (2019) · Biomolecules · doi:10.3390/biom9100567 · Cited by 45 · see citing works
Nuclear and extranuclear effects of vitamin A
Iskakova, M., Karbyshev, M. S., Piskunov, A., & Rochette‐Egly, C. (2015) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2014-0522 · Cited by 44 · see citing works
History of Retinoic Acid Receptors
Benbrook, D. M., Chambon, P., Rochette‐Egly, C., & Asson–Batres, M. A. (2014) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-94-017-9050-5_1 · Cited by 41 · see citing works
Retinoic acid influences neuronal migration from the ganglionic eminence to the cerebral cortex
Crandall, J. E., Goodman, T. H., McCarthy, D. M., Duester, G., Bhide, P. G., Dräger, U. C., & McCaffery, P. J. A. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07471.x · Cited by 39 · see citing works
A new regulatory mechanism for Raf kinase activation, retinoic acid-bound Crabp1
Park, S. W., Nhieu, J., Persaud, S. D., Miller, M. C., Xia, Y., Lin, Y.-W., Lin, Y., Kagechika, H., Mayo, K. H., & Wei, L. (2019) · Scientific Reports · doi:10.1038/s41598-019-47354-7 · Cited by 38 · see citing works
Nuclear receptors and the Warburg effect in cancer
Thorne, J. L., & Campbell, M. J. (2014) · International Journal of Cancer · doi:10.1002/ijc.29012 · Cited by 36 · see citing works
Retinoic acid signaling in axonal regeneration
Puttagunta, R., & Giovanni, S. D. (2012) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2011.00059 · Cited by 37 · see citing works
Kunzler, A., Zeidán‐Chuliá, F., Gasparotto, J., Girardi, C. S., Klafke, K., Petiz, L. L., Bortolin, R. C., Rostirolla, D. C., Zanotto‐Filho, A., Pasquali, M. A. D. B., et al. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0189-4 · Cited by 36 · see citing works
Kurauchi, Y., Hisatsune, A., Isohama, Y., Sawa, T., Akaike, T., Shudo, K., & Katsuki, H. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06916.x · Cited by 35 · 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
Hughes, P., Lee, J. S., Reiner, N. E., & Brown, G. (2007) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21545 · 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
Control of Innate and Adaptive Lymphocytes by the RAR-Retinoic Acid Axis
Kim, C. H. (2018) · Immune Network · doi:10.4110/in.2018.18.e1 · Cited by 33 · see citing works
Alatshan, A., Kovács, G. E., Aladdin, A., Czimmerer, Z., Tar, K., & Benkő, S. (2020) · Cells · doi:10.3390/cells9071591 · Cited by 33 · see citing works
Kogai, T., Ohashi, E., Jacobs, M. S., Sajid-Crockett, S., Fisher, M., Kanamoto, Y., & Brent, G. A. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1627 · Cited by 33 · see citing works
Retinoic acid induces apoptosis by a non-classical mechanism of ERK1/2 activation
Zanotto‐Filho, A., Cammarota, M., Gelain, D. P., de Oliveira, R. B., Cañedo, A. D., Dalmolin, R. J. S., Pasquali, M. A. D. B., & Moreira, J. C. F. (2008) · Toxicology in Vitro · doi:10.1016/j.tiv.2008.04.001 · Cited by 32 · see citing works
Phosphoinositide signaling in sperm development
Brill, J. A., Yildirim, S., & Fabian, L. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2016.06.010 · Cited by 31 · 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
Gelain, D. P., Pasquali, M. A. D. B., Caregnato, F. F., & Moreira, J. C. F. (2011) · Toxicology · doi:10.1016/j.tox.2011.07.008 · Cited by 29 · see citing works
Nagl, F., Schönhofer, K., Seidler, B., Mages, J., Allescher, H., Schmid, R. M., Schneider, G., & Saur, D. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00034.2009 · Cited by 29 · 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
Jiang, M., Meng, J., Zeng, F., Qing, H., Hook, G., HOOK, V. Y. H., Wu, Z., & Ni, J. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15032 · Cited by 28 · see citing works
da Frota, M. L. C., Pires, A. S., Zeidán‐Chuliá, F., Bristot, I. J., Lopes, F. M., Pasquali, M. A. D. B., Zanotto‐Filho, A., Behr, G. A., Klamt, F., Gelain, D. P., et al. (2011) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-011-0983-2 · Cited by 27 · see citing works
Larangé, A., Takazawa, I., Kakugawa, K., Thiault, N., Ngoi, S., Olive, M. E., Iwaya, H., Seguin, L., Vicente-Suarez, I., Bécart, S., et al. (2023) · Immunity · doi:10.1016/j.immuni.2023.07.017 · Cited by 26 · see citing works
Ruiz, A., Dror, E., Handschin, C., Furrer, R., Pérez‐Schindler, J., Bachmann, C., Treves, S., & Zorzato, F. (2018) · Scientific Reports · doi:10.1038/s41598-017-18844-3 · Cited by 26 · see citing works
Chebaro, Y., Amal, I., Rochel, N., Rochette-Egly, C., Stote, R. H., & Dejaegere, A. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003012 · Cited by 25 · see citing works
Hashimoto-Hill, S., Friesen, L., Park, S., Im, S., Kaplan, M. H., & Kim, C. H. (2018) · Nature Communications · doi:10.1038/s41467-018-06341-8 · Cited by 24 · see citing works
Non-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
Coppa, A. (2012) · International Journal of Oncology · doi:10.3892/ijo.2012.1383 · Cited by 23 · see citing works
Ramos, V. D. M., Zanotto‐Filho, A., Pasquali, M. A. D. B., Klafke, K., Gasparotto, J., Dunkley, P. R., Gelain, D. P., & Moreira, J. C. F. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9506-6 · Cited by 23 · see citing works
Létondor, A., Buaud, B., Vaysse, C., Richard, E., Layé, S., Pallet, V., & Alfos, S. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00103 · Cited by 23 · see citing works
Maugeri, G., D’Amico, A. G., Rasà, D. M., Reitano, R., Saccone, S., Federico, C., Parenti, R., Magro, G. G., & D’Agata, V. (2016) · Genes & Cancer · doi:10.18632/genesandcancer.94 · Cited by 22 · see citing works
Laserna, E. J., Valero, M. L., Sanz, L., del Pino, M. M. S., Calvete, J. J., & Barettino, D. (2009) · Molecular Endocrinology · doi:10.1210/me.2009-0165 · Cited by 21 · see citing works
Self-citationZyxin cooperates with PTOV1 to confer retinoic acid resistance by repressing RAR activity
Youn, H., Kim, E., & Um, S. (2013) · Cancer Letters · doi:10.1016/j.canlet.2012.12.019 · Cited by 21 · see citing works
Higgins, S., Wong, S. H. X., Richner, M., Rowe, C. L., Newgreen, D. F., Werther, G. A., & Russo, V. C. (2009) · Endocrinology · doi:10.1210/en.2008-1797 · Cited by 21 · see citing works
Retinoic acid–induced survival effects in SH‐SY5Y neuroblastoma cells
Waetzig, V., Haeusgen, W., Andres, C., Frehse, S., Reinecke, K., Bruckmueller, H., Böhm, R., Herdegen, T., & Cascorbi, I. (2018) · Journal of Cellular Biochemistry · doi:10.1002/jcb.27885 · 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
Vitamin A and its natural derivatives
Redfern, C. P. F. (2020) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2020.02.002 · Cited by 21 · see citing works
Evolution of non-genomic nuclear receptor function
Taylor, E., & Heyland, A. (2021) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2021.111468 · Cited by 21 · see citing works
Laursen, K. B., & Gudas, L. J. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.001951 · Cited by 20 · 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
Tian, X., An, R., Luo, Y., Li, M., Xu, L., & Dong, Z. (2019) · Journal of Stroke and Cerebrovascular Diseases · doi:10.1016/j.jstrokecerebrovasdis.2019.04.017 · Cited by 19 · see citing works
Chu, J., Gao, Z., & Qu, X. (2014) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2014.10.001 · Cited by 19 · see citing works
Trillo, M. Á., Martínez, M. A., Cid, M. A., & ÚBEDA, A. (2012) · Oncology Reports · doi:10.3892/or.2012.2212 · 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
Retinoids as a Perspective in Treatment of Alzheimer’s Disease
Fahrenholz, F., Tippmann, F., & Endres, K. (2010) · Neurodegenerative Diseases · doi:10.1159/000295662 · Cited by 18 · see citing works
Molecular Signaling in Spermatogenesis and Male Infertility
Santos, D. L., & Payan‐Carreira, R. (2019) · CRC Press eBooks · doi:10.1201/9780429244216 · Cited by 18 · see citing works
- Authors
- Masiá, S., Alvarez, S., de Lera, A. R., & Barettino, D.
- Affiliations
- Biology of Hormone Action Unit (S.M., D.B.). Department of Molecular and Cellular Pathology and Therapy, Instituto de Biomedicina de Valencia [Consejo Superior de Investigaciones Cientificas (CSIC)], E-46010 Valencia, Spain;
- Universidade de Vigo (S.A., A.R.d.L.), Departamento de Química Orgánica, Facultad de Ciencias, E-36200 Vigo, Spain
- Consejo Superior de Investigaciones Científicas (ES)
- Corresponding author
- Barettino, Domingo
- Venue
- Molecular Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2007-10-01
- Volume
- 21
- Issue
- 10
- Pages
- 2391-2402
- ISSN
- 0888-8809 (ISSN-L)
- 1944-9917
- OpenAlex
- W2015219861
- Cited by
- 184
- References
- 67
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 8 · 2023: 2 · 2022: 4 · 2021: 4 · 2020: 9 · 2019: 16 · 2018: 12 · 2017: 5 · 2016: 13 · 2015: 11 · 2014: 16 · 2013: 15 · 2012: 11
- FWCI
- 5.01
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Molecular Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, other-oa)
- Funders
- European Commission
- Generalitat Valenciana
- European Regional Development Fund
- 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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › PI3K/AKT/mTOR signaling in cancer
- Keywords
- retinoic acid, non-genomic signaling, retinoic acid receptor, phosphatidylinositol 3-kinase, PI3K signaling, ERK signaling, neuronal differentiation, SH-SY5Y cells, p85 regulatory subunit, p110 catalytic subunit, RARα, subcellular localization
- MeSH terms
- Retinoic Acid Receptor alpha, Humans, Tretinoin, Signal Transduction, Receptors, Retinoic Acid, Phosphatidylinositol 3-Kinases, Mitogen-Activated Protein Kinase 1, Cell Line, Tumor, Mitogen-Activated Protein Kinase 3
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review