Activation of Rac1 and the p38 Mitogen-activated Protein Kinase Pathway in Response to All-trans-retinoic Acid

Alsayed, Yazan; Uddin, Shahab; Mahmud, Nadim; Lekmine, Fatima; Kalvakolanu, Dhananjaya V.; Minucci, Saverio; Bokoch, Gary; Platanias, Leonidas C.

doi:10.1074/jbc.m007431200

Cited by 161Retinoids in leukemia and cellular processesProtein Kinase Regulation and GTPase SignalingProtein Tyrosine Phosphatases

Activation of Rac1 and the p38 Mitogen-activated Protein Kinase Pathway in Response to All-trans-retinoic Acid

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Alsayed, Yazan, Uddin, Shahab, Mahmud, Nadim, Lekmine, Fatima, Kalvakolanu, Dhananjaya V., Minucci, Saverio, Bokoch, Gary, Platanias, Leonidas C.·2001·Journal of Biological Chemistry

DOI 10.1074/jbc.m007431200

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Abstract

Several signaling pathways are activated by all-trans-retinoic acid (RA) to mediate induction of differentiation and apoptosis of malignant cells. In the present study we provide evidence that the p38 MAP kinase pathway is activated in a RA-dependent manner in the NB-4, acute pro-myelocytic leukemia, and the MCF-7, breast carcinoma, cell lines. RA treatment of cells induces a time- and dose-dependent phosphorylation of p38, and such phosphorylation results in activation of its catalytic domain. p38 activation is not inducible by RA in a variant NB-4 cell line, NB-4.007/6, which is resistant to the effects of RA, suggesting a role for this pathway in the induction of RA responses. Our data also demonstrate that the small G-protein Rac1 is activated by RA and functions as an upstream regulator of p38 activation, whereas the MAPKAPK-2 serine kinase is a downstream effector for the RA-activated p38. To obtain information on the functional role of the Rac1/p38/MAPKAPK-2 pathway in RA signaling, the effects of pharmacological inhibition of p38 on RA-induced gene transcription and cell differentiation were determined. Our results indicate that treatment of cells with the SB203580 inhibitor does not inhibit RA-dependent gene transcription via retinoic acid response elements or induction of Stat1 protein expression. However, treatment with SB203580 or SB202190 strongly enhances RA-dependent induction of cell differentiation and RA-regulated growth inhibitory responses. Altogether, our findings demonstrate that the Rac1/p38 MAP kinase pathway is activated in a RA-dependent manner and exhibits negative regulatory effects on the induction of differentiation.

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RA activates p38MAPK in fibroblasts, mouse embryo carcinoma cells, mammary breast tumor cells, and leukemia cells.
“RA activates the p38 mitogen-activated protein kinase (p38MAPK) in fi broblasts, mouse embryo carcinoma cells, mammary breast tumor cells, and leukemia cells ( 96,111,114,115 ).”
From Vitamin A and retinoid signaling: genomic and nongenomic effects (2013) · cites this paper as [114]
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 [114]

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Retinoic Acid Receptor α Mediates Growth Inhibition by Retinoids in Human Colon Carcinoma HT29 Cells
Nicke, B., Kaiser, A., Wiedenmann, B. J., Riecken, E., & Rosewicz, S. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.1086 · Cited by 29 · see citing works

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Map kinase signaling pathways and hematologic malignancies
Platanias, L. C. (2003) · Blood · doi:10.1182/blood-2002-12-3647 · Cited by 432 · see citing works
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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
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
Macrophage MerTK Promotes Liver Fibrosis in Nonalcoholic Steatohepatitis
Cai, B., Dongiovanni, P., Corey, K. E., Wang, X., Shmarakov, I. O., Zheng, Z., Kasikara, C., Davra, V., Meroni, M., Chung, R. T., et al. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2019.11.013 · Cited by 266 · see citing works
Remodeling of White Adipose Tissue after Retinoic Acid Administration in Mice
Mercader, J., Ribot, J., Murano, I., Felipe, F., Cinti, S., Bonet, M. L., & Palou, A. (2006) · Endocrinology · doi:10.1210/en.2006-0760 · Cited by 244 · 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
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
General Molecular Biology and Architecture of Nuclear Receptors
Pawlak, M., Lefèbvre, P., & Staels, B. (2012) · Current Topics in Medicinal Chemistry · doi:10.2174/156802612799436641 · Cited by 168 · see citing works
The p38 mitogen-activated protein kinase pathway and its role in interferon signaling
Platanias, L. C. (2003) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(03)00016-0 · Cited by 161 · see citing works
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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
Phosphorylation by p38MAPK and recruitment of SUG‐1 are required for RA‐induced RARγ degradation and transactivation
Giannì, M., Bauer, A., Garattini, E., Chambon, P., & Rochette‐Egly, C. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf374 · Cited by 151 · 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
Altered SMRT levels disrupt vitamin D3 receptor signalling in prostate cancer cells
Khanim, F. L., Gommersall, L. M., Wood, V. H. J., Smith, K. L., Montalvo, L., O’Neill, L. P., Xu, Y., Peehl, D. M., Stewart, P. M., Turner, B. M., et al. (2004) · Oncogene · doi:10.1038/sj.onc.1207772 · Cited by 141 · 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
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
Nonclassical Action of Retinoic Acid on the Activation of the cAMP Response Element-binding Protein in Normal Human Bronchial Epithelial Cells
Aggarwal, S., Kim, S. W., Cheon, K., Tabassam, F. H., Yoon, J., & Koo, J. S. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-06-0519 · Cited by 125 · see citing works
Activation of Protein Kinase Cδ by IFN-γ
Deb, D. K., Sassano, A., Lekmine, F., Majchrzak, B., Verma, A., Kambhampati, S., Shahab Uddin, M. S., Rahman, A., Fish, E. N., & Platanias, L. C. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.1.267 · Cited by 124 · see citing works
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Activation of Rac1 and the p38 Mitogen-activated Protein Kinase Pathway in Response to Arsenic Trioxide
Verma, A., Mohindru, M., Deb, D. K., Sassano, A., Kambhampati, S., Ravandi, F., Minucci, S., Kalvakolanu, D. V., & Platanias, L. C. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m207176200 · Cited by 122 · see citing works
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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
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
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
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Retinoic acid receptors are required for skeletal growth, matrix homeostasis and growth plate function in postnatal mouse
Williams, J. A., Kondo, N., Okabe, T., Takeshita, N., Pilchak, D. M., Koyama, E., Ochiai, T., Jensen, D. A., Chu, M., Kane, M. A., et al. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.01.031 · Cited by 101 · see citing works
Retinoic acid signaling and mouse embryonic stem cell differentiation: Cross talk between genomic and non-genomic effects of RA
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
Rosiglitazone and Retinoic Acid Induce Uncoupling Protein-1 (UCP-1) in a p38 Mitogen-activated Protein Kinase-dependent Manner in Fetal Primary Brown Adipocytes
Teruel, T., Hernández, R., Benito, M., & Lorenzo, M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m207200200 · Cited by 97 · see citing works
Dual mTORC2/mTORC1 Targeting Results in Potent Suppressive Effects on Acute Myeloid Leukemia (AML) Progenitors
Altman, J. K., Sassano, A., Kaur, S., Glaser, H., Kroczyńska, B., Redig, A. J., Russo, S. M., Barr, S. M., & Platanias, L. C. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-2285 · Cited by 95 · see citing works
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A retinoic acid receptor RARα pool present in membrane lipid rafts forms complexes with G protein αQ to activate p38MAPK
Piskunov, A., & Rochette-Egly, C. (2012) · Oncogene · doi:10.1038/onc.2011.499 · Cited by 95 · see citing works
A Role for Protein Phosphatase-2A in p38 Mitogen-activated Protein Kinase-mediated Regulation of the c-Jun NH2-terminal Kinase Pathway in Human Neutrophils
Briones, N. J., Malcolm, K. C., Nick, J. A., & Worthen, G. S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204455200 · Cited by 89 · see citing works
Retinoic acid treatment of human leiomyoma cells transformed the cell phenotype to one strongly resembling myometrial cells
Malik, M., Webb, J., & Catherino, W. H. (2008) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2008.03207.x · Cited by 84 · see citing works
Disruption of Epithelial Barrier Integrity bySalmonella entericaSerovar Typhimurium Requires Geranylgeranylated Proteins
Tafazoli, F., Magnusson, K., & Zheng, L. (2003) · Infection and Immunity · doi:10.1128/iai.71.2.872-881.2003 · Cited by 83 · see citing works
Interferon-α targets JAK2V617F-positive hematopoietic progenitor cells and acts through the p38 MAPK pathway
Lü, M., Zhang, W., Li, Y., Berenzon, D. P., Wang, X., Wang, J., Mascarenhas, J. O., Xu, M., & Hoffman, R. (2010) · Experimental Hematology · doi:10.1016/j.exphem.2010.03.005 · Cited by 81 · see citing works
P38MAPK‐dependent phosphorylation and degradation of SRC‐3/AIB1 and RARα‐mediated transcription
Giannì, M., Parrella, E., Raska, I., Gaillard, E., Nigro, E. A., Gaudon, C., Garattini, E., & Rochette‐Egly, C. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7600981 · Cited by 81 · see citing works
Role of the p38 Mitogen-Activated Protein Kinase Pathway in the Generation of Arsenic Trioxide–Dependent Cellular Responses
Giafis, N., Katsoulidis, E., Sassano, A., Tallman, M. S., Higgins, L. S., Nebreda, Á. R., Davis, R. J., & Platanias, L. C. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3699 · Cited by 81 · see citing works
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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
Suppressive Effects of Statins on Acute Promyelocytic Leukemia Cells
Sassano, A., Katsoulidis, E., Antico, G., Altman, J. K., Redig, A. J., Minucci, S., Tallman, M. S., & Platanias, L. C. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-3686 · Cited by 80 · see citing works
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Anticancer effects of ginsenoside Rg1, cinnamic acid, and tanshinone IIA in osteosarcoma MG-63 cells: Nuclear matrix downregulation and cytoplasmic trafficking of nucleophosmin
Li, Q., Shi, S., Liu, Q., Tang, J., Song, J.-Y., & Liang, Y. (2008) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2008.01.031 · Cited by 79 · see citing works
Aldehyde dehydrogenase in solid tumors and other diseases: Potential biomarkers and therapeutic targets
Xia, J. L., Li, S., Liu, S., & Zhang, L. (2023) · MedComm · doi:10.1002/mco2.195 · Cited by 80 · see citing works
Ser727/Tyr701-phosphorylated Stat1 is required for the regulation of c-Myc, cyclins, and p27Kip1 associated with ATRA-induced G0/G1 arrest of U-937 cells
Dimberg, A., Karlberg, I., Nilsson, K., & Oberg, F. G. (2003) · Blood · doi:10.1182/blood-2002-10-3149 · Cited by 73 · see citing works
Magnolol and honokiol enhance HL-60 human leukemia cell differentiation induced by 1,25-dihydroxyvitamin D3 and retinoic acid
Fong, W. F., Tse, A. K., Poon, K.-H., & Wang, C. (2004) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2004.05.021 · Cited by 72 · see citing works
All-Trans Retinoic Acid Antagonizes UV-Induced VEGF Production and Angiogenesis via the Inhibition of ERK Activation in Human Skin Keratinocytes
Kim, M., Kim, Y. K., Eun, H. C., Cho, K. H., & Chung, J. H. (2006) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5700463 · Cited by 72 · see citing works
Role of the p38 Mitogen-activated Protein Kinase Pathway in the Generation of the Effects of Imatinib Mesylate (STI571) in BCR-ABL-expressing Cells
Parmar, S., Katsoulidis, E., Verma, A. K., Li, Y., Sassano, A., Lal, L., Majchrzak, B., Ravandi, F., Tallman, M. S., Fish, E. N., et al. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m400590200 · Cited by 70 · see citing works
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Retinoids in nephrology: Promises and pitfalls
Xu, Q., Lucio-Cazaña, F. J., Kitamura, M., Ruan, X. Z., Fine, L. G., & Norman, J. T. (2004) · Kidney International · doi:10.1111/j.1523-1755.2004.66002.x · Cited by 69 · see citing works
Suppression of Programmed Cell Death 4 (PDCD4) Protein Expression by BCR-ABL-regulated Engagement of the mTOR/p70 S6 Kinase Pathway
Carayol, N., Katsoulidis, E., Sassano, A., Altman, J. K., Druker, B. J., & Platanias, L. C. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m707934200 · Cited by 69 · see citing works
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DIM stimulates IFNγ gene expression in human breast cancer cells via the specific activation of JNK and p38 pathways
Xue, L., Firestone, G. L., & Bjeldanes, L. F. (2005) · Oncogene · doi:10.1038/sj.onc.1208434 · Cited by 69 · see citing works
Retinoids and myelomonocytic growth factors cooperatively activate RARΑ and induce human myeloid leukemia cell differentiation via MAP kinase pathways
Glasow, A., Prodromou, N., Xu, K., von Lindern, M., & Zelent, A. (2005) · Blood · doi:10.1182/blood-2004-03-1074 · Cited by 68 · see citing works
Retinoic acid alters the proliferation and survival of the epithelium and mesenchyme and suppresses Wnt/β-catenin signaling in developing cleft palate
Hu, X., Gao, J. H., Liao, Y., Tang, S., & Lu, F. (2013) · Cell Death and Disease · doi:10.1038/cddis.2013.424 · Cited by 63 · see citing works
CSK Controls Retinoic Acid Receptor (RAR) Signaling: a RAR–c-SRC Signaling Axis Is Required for Neuritogenic Differentiation
Dey, N., De, P. K., Wang, M., Zhang, H., Dobrota, E. A., Robertson, K. A., & Durden, D. L. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01352-06 · Cited by 62 · see citing works
p38 Mitogen-Activated Protein Kinase Stimulates Estrogen-Mediated Transcription and Proliferation through the Phosphorylation and Potentiation of the p160 Coactivator Glucocorticoid Receptor-Interacting Protein 1
Frigo, D. E., Basu, A., Nierth-Simpson, E. N., Weldon, C. B., Dugan, C. M., Elliott, S. G., Collins‐Burow, B. M., Salvo, V. A., Zhu, Y., Melnik, L. I., et al. (2006) · Molecular Endocrinology · doi:10.1210/me.2004-0075 · Cited by 62 · see citing works
BIRB 796 enhances cytotoxicity triggered by bortezomib, heat shock protein (Hsp) 90 inhibitor, and dexamethasone via inhibition of p38 mitogen‐activated protein kinase/Hsp27 pathway in multiple myeloma cell lines and inhibits paracrine tumour growth
Yasui, H., Hideshima, T., Ikeda, H., Jin, J., Ocio, E. M., Kiziltepe, T., Okawa, Y., Vallet, S., Podar, K., Ishitsuka, K., et al. (2006) · British Journal of Haematology · doi:10.1111/j.1365-2141.2006.06443.x · Cited by 60 · see citing works
Activation of the Mitogen- and Stress-activated Kinase 1 by Arsenic Trioxide
Kannan-Thulasiraman, P., Katsoulidis, E., Tallman, M. S., Arthur, J. S. C., & Platanias, L. C. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m603111200 · Cited by 59 · see citing works
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Selective Inhibition of the Myeloid Src-Family Kinase Fgr Potently Suppresses AML Cell Growth in Vitro and in Vivo
Weir, M. C., Shu, S. T., Patel, R. K., Hellwig, S., Chen, L., Tan, L., Gray, N. S., & Smithgall, T. E. (2018) · ACS Chemical Biology · doi:10.1021/acschembio.8b00154 · Cited by 53 · see citing works
Down-regulation of the Phosphatidylinositol 3-Kinase/Akt Pathway Is Involved in Retinoic Acid-induced Phosphorylation, Degradation, and Transcriptional Activity of Retinoic Acid Receptor γ2
Gianni’, M., Kopf, E., Bastien, J., Oulad‐Abdelghani, M., Garattini, E., Chambon, P., & Rochette‐Egly, C. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.c200230200 · Cited by 53 · see citing works
Progestin upregulates G‐protein‐coupled receptor 30 in breast cancer cells
Ahola, T. M., Purmonen, S., Pennanen, P. T., Zhuang, Y., Tuohimaa, P., & Ylikomi, T. J. (2002) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2002.02912.x · Cited by 51 · see citing works
CEBPD Reverses RB/E2F1-Mediated Gene Repression and Participates in HMDB-Induced Apoptosis of Cancer Cells
Pan, Y.-C., Li, C., Ko, C., Pan, M., Chen, P., Tseng, J. T.-C., Wu, W.-C., Chang, W., Huang, A., Sterneck, E., et al. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-1025 · Cited by 50 · see citing works
Downregulation of Rac1 activation by caffeic acid in aortic smooth muscle cells
Xu, J., Ikeda, K., Kobayakawa, A., Ikami, T., Kayano, Y., Mitani, T., & Yamori, Y. (2005) · Life Sciences · doi:10.1016/j.lfs.2004.11.015 · Cited by 48 · see citing works
Regulatory Effects of Mammalian Target of Rapamycin-mediated Signals in the Generation of Arsenic Trioxide Responses
Altman, J. K., Yoon, P., Katsoulidis, E., Kroczyńska, B., Sassano, A., Redig, A. J., Glaser, H., Jordan, A., Tallman, M. S., Hay, N., et al. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m705227200 · Cited by 46 · see citing works
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A novel role for Gab2 in bFGF-mediated cell survival during retinoic acid–induced neuronal differentiation
Mao, Y., & Lee, A. W. ‐. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200505061 · Cited by 46 · see citing works
Differential effects of invasion by and phagocytosis of Salmonella typhimurium on apoptosis in human macrophages: potential role of Rho–GTPases and Akt
Forsberg, M., Blomgran, R., Lerm, M., Särndahl, E., Sebti, S. M., Hamilton, A. D., Stendahl, O. I., & Zheng, L. (2003) · Journal of Leukocyte Biology · doi:10.1189/jlb.1202586 · Cited by 45 · see citing works
Phytochemical Regulation of UDP-Glucuronosyltransferases: Implications for Cancer Prevention
Saracino, M. R., & Lampe, J. W. (2007) · Nutrition and Cancer · doi:10.1080/01635580701458178 · Cited by 44 · 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
Activation of the p70 S6 kinase by all-trans-retinoic acid in acute promyelocytic leukemia cells
Lal, L., Li, Y., Smith, J., Sassano, A., Shahab Uddin, M. S., Parmar, S., Tallman, M. S., Minucci, S., Hay, N., & Platanias, L. C. (2004) · Blood · doi:10.1182/blood-2004-06-2078 · Cited by 43 · see citing works
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Retinoids interfere with the AP1 signalling pathway in human breast cancer cells
Dedieu, S., & Lefèbvre, P. (2005) · Cellular Signalling · doi:10.1016/j.cellsig.2005.08.001 · Cited by 42 · see citing works
microRNA-339-5p modulates Na+/I− symporter-mediated radioiodide uptake
Lakshmanan, A., Wójcicka, A., Kotlarek, M., Zhang, X., Jażdżewski, K., & Jhiang, S. M. (2014) · Endocrine Related Cancer · doi:10.1530/erc-14-0439 · Cited by 42 · see citing works
Opposing Roles of c-Jun NH2-Terminal Kinase and p38 Mitogen-Activated Protein Kinase in the Cellular Response to Ionizing Radiation in Human Cervical Cancer Cells
Kim, M., Choi, S.-Y., Park, I., Hwang, S., Kim, C., Choi, Y.-H., Kim, H., Lee, K.-H., & Lee, S. (2008) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-08-0032 · Cited by 40 · see citing works
Gene Expression Profiling during All-trans Retinoic Acid-Induced Cell Differentiation of Acute Promyelocytic Leukemia Cells
Yang, L., Zhao, H., Li, S.-W., Ahrens, K. P., Collins, C., Eckenrode, S., Ruan, Q., McIndoe, R., & She, J. (2003) · Journal of Molecular Diagnostics · doi:10.1016/s1525-1578(10)60476-x · Cited by 39 · see citing works
Alltrans-retinoic acid induces apoptosis via p38 and caspase pathways in metaplastic Barrett's cells
Hormi-Carver, K. K., Feagins, L. A., Spechler, S. J., & Souza, R. F. (2006) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00237.2006 · Cited by 39 · see citing works
p38 Mitogen-Activated Protein Kinase and Hematologic Malignancies
Feng, Y., Wen, J., & Chang, C.-C. (2009) · Archives of Pathology & Laboratory Medicine · doi:10.5858/133.11.1850 · 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
Fibroblast nemosis arrests growth and induces differentiation of human leukemia cells
Kankuri, E. M., Babušíková, O., Hlubinova, K., Salmenperä, P., Boccaccio, C., Lubitz, W., Harjula, A. L. J., & Bízik, J. (2007) · International Journal of Cancer · doi:10.1002/ijc.23179 · Cited by 34 · see citing works
BIRB796, the Inhibitor of p38 Mitogen-Activated Protein Kinase, Enhances the Efficacy of Chemotherapeutic Agents in ABCB1 Overexpression Cells
He, D., Zhao, X.-Q., Chen, X.-G., Fang, Y., Singh, S., Talele, T. T., Qiu, H., Liang, Y.-J., Wang, X.-K., Zhang, G.-Q., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054181 · Cited by 33 · see citing works
Retinoic Acid Stimulation of the Sodium/Iodide Symporter in MCF-7 Breast Cancer Cells Is Meditated by the Insulin Growth Factor-I/Phosphatidylinositol 3-Kinase and p38 Mitogen-Activated Protein Kinase Signaling Pathways
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
Signaling Via the Interferon-α Receptor in Chronic Myelogenous Leukemia Cells
Verma, A., & Platanias, L. C. (2002) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.1080/10428190290016782 · Cited by 33 · see citing works
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Effects of all-trans retinoic acid nanoparticles on corneal epithelial wound healing
Hattori, M., Shimizu, K., Katsumura, K., Oku, H., Sano, Y., Matsumoto, K., Yamaguchi, Y., & Ikeda, T. (2011) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-011-1849-8 · Cited by 32 · see citing works
Bis-indols: a novel class of molecules enhancing the cytodifferentiating properties of retinoids in myeloid leukemia cells
Pisano, C., Kollár, P., Gianni’, M., Kalaç, Y., Giordano, V., Ferrara, F. F., Tancredi, R. J., Devoto, A., Rinaldi, A., Rambaldi, A., et al. (2002) · Blood · doi:10.1182/blood-2002-03-0720 · Cited by 32 · see citing works
Signalling Pathways Activated by All- <i>trans</i> -Retinoic Acid in Acute Promyelocytic Leukemia Cells
Kambhampati, S., Verma, A., Li, Y., Parmar, S., Sassano, A., & Platanias, L. (2004) · Leukemia & Lymphoma · doi:10.1080/10428190410001722053 · Cited by 29 · see citing works
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Retinoid Signaling Regulates CTGF Expression in Hypertrophic Chondrocytes With Differential Involvement of MAP Kinases
Shimo, T., Koyama, E., Sugito, H., Wu, C., Shimo, S., & Pacifici, M. (2005) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.041235 · Cited by 31 · see citing works
Interferon regulatory factor-1 binds c-Cbl, enhances mitogen activated protein kinase signaling and promotes retinoic acid-induced differentiation of HL-60 human myelo-monoblastic leukemia cells
Shen, M., Bunaciu, R. P., Congleton, J., Jensen, H. A., Sayam, L. G., Varner, J. D., & Yen, A. (2011) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428194.2011.603449 · Cited by 31 · see citing works
All-Trans Retinoic Acid-Induced Deficiency of the Wnt/β-Catenin Pathway Enhances Hepatic Carcinoma Stem Cell Differentiation
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Authors: Alsayed, Y., Uddin, S., Mahmud, N., Lekmine, F., Kalvakolanu, D. V., Minucci, S., Bokoch, G., & Platanias, L. C.
Affiliations: Jesse Brown VA Medical Center (US)
University of Maryland, Baltimore (US)
European Institute of Oncology (IT)
Scripps Research Institute (US)
Corresponding author: Platanias, Leonidas C.
ORCID: Mahmud, Nadim
Minucci, Saverio
Platanias, Leonidas C.
Venue: Journal of Biological Chemistry
Publisher: Elsevier BV
Published: 2001-02
Volume: 276
Issue: 6
Pages: 4012-4019
ISSN: 0021-9258 (ISSN-L)
DOI: 10.1074/jbc.m007431200
OpenAlex: W2047204411
Cited by: 161
References: 73
Citations by year: 2026: 1 · 2025: 4 · 2024: 3 · 2023: 6 · 2022: 1 · 2020: 3 · 2019: 6 · 2018: 5 · 2017: 3 · 2016: 4 · 2015: 7 · 2014: 6 · 2013: 12 · 2012: 4
FWCI: 3.62
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 7193 d)
Locations: Journal of Biological Chemistry (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
INFM-OAR (INFN Catania) (submittedVersion, cc-by)
Funders: U.S. Department of Veterans Affairs
National Institutes of Health (5r29ca073381-03, 5r01ca071401-06, CA77816)
National Cancer Institute (CA-77816, CA78282, R01CA078282, CA73381, CA-71401, R01CA077816)
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 › Protein Tyrosine Phosphatases
Keywords: all-trans retinoic acid, Rac1, p38 MAPK, MAPKAPK2, retinoic acid signaling, leukemia cell differentiation, retinoic acid response element, STAT1, SB203580, SB202190, MCF-7 cells, cell differentiation, gene transcription, growth inhibition
MeSH terms: MAP-Kinase-Activated Kinase 2, Cell Differentiation, Enzyme Activation, Enzyme Inhibitors, Humans, Imidazoles, Pyridines, Tretinoin, Tumor Cells, Cultured, Protein Serine-Threonine Kinases, rac1 GTP-Binding Protein, Mitogen-Activated Protein Kinases, MAP Kinase Signaling System, Intracellular Signaling Peptides and Proteins, p38 Mitogen-Activated Protein Kinases

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Activation of Rac1 and the p38 Mitogen-activated Protein Kinase Pathway in Response to All-trans-retinoic Acid

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