Retinoids regulate stem cell differentiation

Gudas, Lorraine J.; Wagner, John A.

doi:10.1002/jcp.22417

Cited by 398Retinoids in leukemia and cellular processesPeroxisome Proliferator-Activated ReceptorsPluripotent Stem Cells Research

Retinoids regulate stem cell differentiation

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Gudas, Lorraine J., Wagner, John A.·2011·Journal of Cellular Physiology

DOI 10.1002/jcp.22417PMC PMC3315372

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Abstract

Retinoids are ubiquitous signaling molecules that influence nearly every cell type, exert profound effects on development, and complement cancer chemotherapeutic regimens. All‐trans retinoic acid (RA) and other active retinoids are generated from vitamin A (retinol), but key aspects of the signaling pathways required to produce active retinoids remain unclear. Retinoids generated by one cell type can affect nearby cells, so retinoids also function in intercellular communication. RA induces differentiation primarily by binding to RARs, transcription factors that associate with RXRs and bind RAREs in the nucleus. Binding of RA: (1) initiates changes in interactions of RAR/RXRs with co‐repressor and co‐activator proteins, activating transcription of primary target genes; (2) alters interactions with proteins that induce epigenetic changes; (3) induces transcription of genes encoding transcription factors and signaling proteins that further modify gene expression (e.g., FOX03A, Hoxa1, Sox9, TRAIL, UBE2D3); and (4) results in alterations in estrogen receptor α signaling. Proteins that bind at or near RAREs include Sin3a, N‐CoR1, PRAME, Trim24, NRIP1, Ajuba, Zfp423, and MN1/TEL. Interactions among retinoids, RARs/RXRs, and these proteins explain in part the powerful effects of retinoids on stem cell differentiation. Studies of this retinol signaling cascade enhance our ability to understand and regulate stem cell differentiation for therapeutic and scientific purposes. In cancer chemotherapeutic regimens retinoids can promote tumor cell differentiation and/or induce proteins that sensitize tumors to drug combinations. Mechanistic studies of retinoid signaling continue to suggest novel drug targets and will improve therapeutic strategies for cancer and other diseases, such as immune‐mediated inflammatory diseases. J. Cell. Physiol. 226: 322–330, 2011. © 2010 Wiley‐Liss, Inc.

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Carotenoids also act as antioxidants.
“Carotenoids also act as antioxidants [126,127,128,129,130,131,132].”
From Vitamin A Update: Forms, Sources, Kinetics, Detection, Function, Deficiency, Therapeutic Use and Toxicity (2021) · cites this paper as [127]
The section “How is the Biologically Active Signaling Molecule, RA, Generated?” describes β-carotene as a dietary precursor that is converted to retinaldehyde. Searches for antioxidant activity and oxidative stress found no passage in our copy saying that carotenoids act as antioxidants. (LLM, conf=0.75)
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Augmentation of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis by the synthetic retinoid 6-[3-(1-adamantyl)-4-hydroxyphenyl]-2-naphthalene carboxylic acid (CD437) through up-regulation of TRAIL receptors in human lung cancer cells.
Sun, S., Yue, P., Hong, W. K., & Lotan, R. (2000) · PubMed · Cited by 90 · see citing works
RAR agonists stimulate SOX9 gene expression in breast cancer cell lines: evidence for a role in retinoid-mediated growth inhibition
Afonja, O., Raaka, B. M., Huang, A. J., Das, S., Zhao, X., Helmer, E., Juste, D., & Samuels, H. H. (2002) · Oncogene · doi:10.1038/sj.onc.1205985 · Cited by 86 · see citing works
Polycomb CBX7 Promotes Initiation of Heritable Repression of Genes Frequently Silenced with Cancer-Specific DNA Hypermethylation
Mohammad, H. P., Cai, Y., McGarvey, K. M., Easwaran, H., Neste, L. V., Ohm, J. E., O’Hagan, H. M., & Baylin, S. B. (2009) · Cancer Research · doi:10.1158/0008-5472.can-09-0065 · Cited by 86 · see citing works
Retinoic acid directs neuronal differentiation of human pluripotent stem cell lines in a non-cell-autonomous manner
Tonge, P. D., & Andrews, P. W. (2010) · Differentiation · doi:10.1016/j.diff.2010.04.001 · Cited by 85 · see citing works
Epigenetic Regulatory Mechanisms Distinguish Retinoic Acid-mediated Transcriptional Responses in Stem Cells and Fibroblasts
Kashyap, V., & Gudas, L. J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.115345 · Cited by 84 · see citing works
Self-citation
The atRA Regulated Gene Neuron Navigator 2 Functions in Neurite Outgrowth and Axonal Elongation
Muley, P. D., McNeill, E., Marzinke, M., Knobel, K. M., Barr, M., & Clagett-Dame, M. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20670 · Cited by 84 · see citing works
Retinyl Ester Formation by Lecithin:Retinol Acyltransferase Is a Key Regulator of Retinoid Homeostasis in Mouse Embryogenesis
Kim, Y.-K., Wassef, L., Hamberger, L., Piantedosi, R., Palczewski, K., Blaner, W. S., & Quadro, L. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m708885200 · Cited by 80 · see citing works
Zfp423 Is Required for Normal Cerebellar Development
Warming, S., Rachel, R. A., Jenkins, N. A., & Copeland, N. G. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.02255-05 · Cited by 80 · see citing works
High Histone Acetylation and Decreased Polycomb Repressive Complex 2 Member Levels Regulate Gene Specific Transcriptional Changes During Early Embryonic Stem Cell Differentiation Induced by Retinoic Acid
Lee, E. R., Murdoch, F. E., & Fritsch, M. K. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0203 · Cited by 79 · see citing works
Transcription Factor Smad3 Is Required for the Inhibition of Adipogenesis by Retinoic Acid
Marchildon, F., St‐Louis, C., Akter, R., Roodman, V., & Wiper‐Bergeron, N. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.054536 · Cited by 79 · see citing works
Discovery and Design of Retinoic Acid Receptor and Retinoid X Receptor Class- and Subtype-Selective Synthetic Analogs of All-trans-retinoic Acid and 9-cis-Retinoic Acid
Dawson, M. I., & Zhang, X.-K. (2002) · Current Medicinal Chemistry · doi:10.2174/0929867023370789 · Cited by 76 · see citing works
Retinoic Acid Synthesis Promotes Development of Neural Progenitors from Mouse Embryonic Stem Cells by Suppressing Endogenous, Wnt-Dependent Nodal Signaling
Engberg, N., Kahn, M., Petersen, D. R., Hansson, M. D., & Serup, P. (2010) · Stem Cells · doi:10.1002/stem.479 · Cited by 76 · see citing works
Phosphorylation by PKA potentiates retinoic acid receptor α activity by means of increasing interaction with and phosphorylation by cyclin H/cdk7
Gaillard, E., Bruck, N., Brelivet, Y., Bour, G., Lalevée, S., Bauer, A., Poch, O., Moras, D., & Rochette-Egly, C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509717103 · Cited by 76 · see citing works
ZNF536, a Novel Zinc Finger Protein Specifically Expressed in the Brain, Negatively Regulates Neuron Differentiation by Repressing Retinoic Acid-Induced Gene Transcription
Qin, Z., Ren, F., Xu, X., Ren, Y., Li, H., Wang, Y., Zhai, Y., & Chang, Z. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.00362-09 · Cited by 76 · see citing works
Granulocytic differentiation of human NB4 promyelocytic leukemia cells induced by all-trans retinoic acid metabolites.
Idres, N., Benoît, G., Flexor, M., Lanotte, M., & Chabot, G. G. (2001) · PubMed · Cited by 75 · see citing works
FOXO3A as a key molecule for all-trans retinoic acid–induced granulocytic differentiation and apoptosis in acute promyelocytic leukemia
Sakoe, Y., Sakoe, K., Kirito, K., Ozawa, K., & Komatsu, N. (2010) · Blood · doi:10.1182/blood-2009-05-222976 · Cited by 74 · see citing works
Analysis of Rex1 (zfp42) function in embryonic stem cell differentiation
Scotland, K. B., Chen, S., Sylvester, R., & Gudas, L. J. (2009) · Developmental Dynamics · doi:10.1002/dvdy.22037 · Cited by 74 · see citing works
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Corepressors of agonist-bound nuclear receptors
Gurevich, I., Flores, A. M., & Aneskievich, B. J. (2007) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2007.05.019 · Cited by 73 · see citing works
Suppression of Oct4 by Germ Cell Nuclear Factor Restricts Pluripotency and Promotes Neural Stem Cell Development in the Early Neural Lineage
Akamatsu, W., DeVeale, B., Okano, H., Cooney, A. J., & van der Kooy, D. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4527-08.2009 · Cited by 72 · see citing works
Retinoic Acid and its 4-Oxo Metabolites are Functionally Active in Human Skin Cells In Vitro
Baron, J. M., Heise, R., Blaner, W. S., Neis, M. M., Joussen, S., Dreuw, A., Marquardt, Y., Saurat, J. ‐., Merk, H. F., Bickers, D. R., et al. (2005) · Journal of Investigative Dermatology · doi:10.1111/j.0022-202x.2005.23791.x · Cited by 70 · see citing works
Retinoic Acid Receptor Isotype Specificity in F9 Teratocarcinoma Stem Cells Results from the Differential Recruitment of Coregulators to Retinoic Acid Response Elements
Gillespie, R. F., & Gudas, L. J. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m704845200 · Cited by 70 · see citing works
Self-citation
Interference with Sin3 function induces epigenetic reprogramming and differentiation in breast cancer cells
Farias, E., Petrie, K. R., Leibovitch, B. A., Murtagh, J., Boix-Chornet, M., Schenk, T., Zelent, A., & Waxman, S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1006737107 · Cited by 69 · see citing works
Expression of the murine retinol dehydrogenase 10 (Rdh10) gene correlates with many sites of retinoid signalling during embryogenesis and organ differentiation
Cammas, L., Romand, R., Fraulob, V., Mura, C., & Dollé, P. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21312 · Cited by 69 · see citing works
Kinetic Analysis of Human Enzyme RDH10 Defines the Characteristics of a Physiologically Relevant Retinol Dehydrogenase
Belyaeva, O. V., Johnson, M. P., & Kedishvili, N. Y. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800019200 · 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
An octamer motif contributes to the expression of the retinoic acid-regulated zinc finger gene Rex-1 (Zfp-42) in F9 teratocarcinoma cells.
Hosler, B. A., Rogers, M. B., Kozak, C. A., & Gudas, L. J. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.5.2919 · Cited by 65 · see citing works
Self-citation
Hepatic stellate cells are an important cellular site for β-carotene conversion to retinoid
Shmarakov, I. O., Fleshman, M. K., D’Ambrosio, D. N., Piantedosi, R., Riedl, K. M., Schwartz, S. J., Curley, R. W., Lintig, J. V., Rubin, L. P., Harrison, E. H., et al. (2010) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2010.05.010 · Cited by 64 · see citing works
Inhibition of ectopic bone formation by a selective retinoic acid receptor α‐agonist: A new therapy for heterotopic ossification?
Shimono, K., Morrison, T. N., Tung, W.-E., Chandraratna, R. A. S., Williams, J. A., Iwamoto, M., & Pacifici, M. (2009) · Journal of Orthopaedic Research® · doi:10.1002/jor.20985 · Cited by 59 · see citing works
Anti-tumor effects of retinoids combined with trastuzumab or tamoxifen in breast cancer cells: induction of apoptosis by retinoid/trastuzumab combinations
Koay, D. C., Zerillo, C. A., Narayan, M., Harris, L. N., & DiGiovanna, M. P. (2010) · Breast Cancer Research · doi:10.1186/bcr2625 · Cited by 57 · see citing works
N-CoR Pathway Targeting Induces Glioblastoma Derived Cancer Stem Cell Differentiation
Park, D. M., Li, J., Okamoto, H., Akeju, O., Kim, S. H., Lubensky, I. A., Vortmeyer, A. O., Dambrosia, J., Weil, R. J., Oldfield, E. H., et al. (2007) · Cell Cycle · doi:10.4161/cc.6.4.3856 · Cited by 57 · see citing works
Acidic retinoids synergize with vitamin A to enhance retinol uptake and STRA6, LRAT, and CYP26B1 expression in neonatal lung
Wu, L., & Ross, A. C. (2009) · Journal of Lipid Research · doi:10.1194/jlr.m001222 · Cited by 56 · see citing works
Cdc42-mTOR Signaling Pathway Controls Hes5 and Pax6 Expression in Retinoic Acid-dependent Neural Differentiation
Endo, M., Antonyak, M. A., & Cerione, R. A. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m807745200 · Cited by 55 · see citing works
Retinoic Acid Hydroxylase (CYP26) Is a Key Enzyme in Neuronal Differentiation of Embryonal Carcinoma Cells
Sonneveld, E., Brink, C. E. V. D., Tertoolen, L. G. J., van der Burg, B., & van der Saag, P. T. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9381 · Cited by 54 · see citing works
Zfp206 Is a Transcription Factor That Controls Pluripotency of Embryonic Stem Cells
Wang, Z.-X., Kueh, J. L. L., Teh, C. H.-L., Roßbach, M., Lim, L. S., Li, P., Wong, K., Lufkin, T., Robson, P., & Stanton, L. W. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0085 · Cited by 54 · see citing works
RNAi screen identifies UBE2D3 as a mediator of all-trans retinoic acid-induced cell growth arrest in human acute promyelocytic NB4 cells
Hattori, H., Zhang, X., Jia, Y., Subramanian, K. K., Jo, H., Loison, F., Newburger, P. E., & Luo, H. R. (2007) · Blood · doi:10.1182/blood-2006-11-059048 · Cited by 51 · see citing works
CYP26A1 knockout embryonic stem cells exhibit reduced differentiation and growth arrest in response to retinoic acid
Langton, S., & Gudas, L. J. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.12.021 · Cited by 48 · see citing works
Self-citation
Retinoic acid inhibits leukemia inhibitory factor signaling pathways in mouse embryonic stem cells
Tighe, A. P., & Gudas, L. J. (2003) · Journal of Cellular Physiology · doi:10.1002/jcp.10424 · Cited by 48 · see citing works
Self-citation
LIM protein Ajuba functions as a nuclear receptor corepressor and negatively regulates retinoic acid signaling
Hou, Z., Peng, H., White, D. E., Negorev, D. G., Maul, G. G., Feng, Y., Longmore, G. D., Waxman, S., Zelent, A., & Rauscher, F. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908656107 · Cited by 46 · see citing works
Activity of Retinoic Acid Receptor-alpha Is Directly Regulated at Its Protein Kinase A Sites in Response to Follicle-Stimulating Hormone Signaling
Santos, N. C., & Kim, K. H. (2010) · Endocrinology · doi:10.1210/en.2009-1338 · Cited by 41 · see citing works
SOX9 mediates the retinoic acid-induced HES-1 gene expression in human breast cancer cells
Müller, P., Crofts, J. D., Newman, B. S., Bridgewater, L. C., Lin, C., Gustafsson, J.-Α., & Ström, A. (2009) · Breast Cancer Research and Treatment · doi:10.1007/s10549-009-0381-6 · Cited by 41 · see citing works
Hoxa1 is required for the retinoic acid–induced differentiation of embryonic stem cells into neurons
Martinez‐Ceballos, E., & Gudas, L. J. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21729 · Cited by 39 · see citing works
Self-citation
Retinoic acid receptor alpha2 is a growth suppressor epigenetically silenced in MCF-7 human breast cancer cells.
Farias, E., Arapshian, A., Bleiweiss, I. J., Waxman, S., Zelent, A., & Mira-y-Lopez, R. (2002) · PubMed · Cited by 39 · see citing works
RARγ acts as a tumor suppressor in mouse keratinocytes
Chen, C. F., Goyette, P., & Lohnes, D. (2004) · Oncogene · doi:10.1038/sj.onc.1207682 · Cited by 39 · see citing works
Suppressive Effect of Receptor-interacting Protein 140 on Coregulator Binding to Retinoic Acid Receptor Complexes, Histone-modifying Enzyme Activity, and Gene Activation
Hu, X., Chen, Y., Farooqui, M., Thomas, M. C., Chiang, C., & Wei, L. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m307621200 · Cited by 33 · see citing works
Increased HEXIM1 expression during erythroleukemia and neuroblastoma cell differentiation
Turano, M., Napolitano, G., Dulac, C., Majello, B., Bensaude, O., & Lania, L. (2005) · Journal of Cellular Physiology · doi:10.1002/jcp.20502 · Cited by 33 · see citing works
Limiting Effects of RIP140 in Estrogen Signaling
White, K. A., Yore, M. M., Deng, D., & Spinella, M. J. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m412707200 · Cited by 32 · see citing works
Mechanism of inhibition of MMTV-neu and MMTV-wnt1 induced mammary oncogenesis by RARα agonist AM580
Lu, Y., Bertran, S., Samuels, T.-A., Mira-y-Lopez, R., & Farias, E. (2010) · Oncogene · doi:10.1038/onc.2010.119 · Cited by 31 · see citing works
Selective repression of retinoic acid target genes by RIP140 during induced tumor cell differentiation of pluripotent human embryonal carcinoma cells
Heim, K. C., White, K. A., Deng, D., Tomlinson, C. R., Moore, J. H., Freemantle, S. J., & Spinella, M. J. (2007) · Molecular Cancer · doi:10.1186/1476-4598-6-57 · Cited by 30 · see citing works
The MN1-TEL myeloid leukemia-associated fusion protein has a dominant-negative effect on RAR-RXR-mediated transcription
van Wely, K. H. M., Meester‐Smoor, M. A., Janssen, M. J. F. W., Aarnoudse, A.-J., Grosveld, G. C., & Zwarthoff, E. C. (2007) · Oncogene · doi:10.1038/sj.onc.1210382 · Cited by 28 · see citing works
RARγ is required for correct deposition and removal of Suz12 and H2A.Z in embryonic stem cells
Amat, R., & Gudas, L. J. (2010) · Journal of Cellular Physiology · doi:10.1002/jcp.22420 · Cited by 27 · see citing works
Self-citation
All-Trans Retinoic Acid Suppresses Stat3 Signaling during Skin Carcinogenesis
Syed, Z., Cheepala, S., Gill, J. N., Stein, J., Nathan, C. O., DiGiovanni, J., Batra, V., Adegboyega, P. A., Kleiner, H. E., & Clifford, J. L. (2009) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-09-0041 · Cited by 26 · see citing works
Transcriptional Activation of the Suppressor of Cytokine Signaling-3 (SOCS-3) Gene via STAT3 Is Increased in F9 REX1 (ZFP-42) Knockout Teratocarcinoma Stem Cells Relative to Wild-type Cells
Xu, J., Sylvester, R., Tighe, A. P., Chen, S., & Gudas, L. J. (2008) · Journal of Molecular Biology · doi:10.1016/j.jmb.2007.12.038 · Cited by 24 · see citing works
Self-citation
ERbeta sensitizes breast cancer cells to retinoic acid: evidence of transcriptional crosstalk.
Rousseau, C., Nichol, J. N., Pettersson, F., Couture, M.-C., & Miller, W. H. (2004) · PubMed · Cited by 24 · see citing works
Loss of CAK phosphorylation of RARa mediates transcriptional control of retinoid‐induced cancer cell differentiation
Wang, A., Alimova, I. N., Luo, P., Jgon, A., Triche, T. J., & Wu, L. (2009) · The FASEB Journal · doi:10.1096/fj.09-142976 · Cited by 22 · see citing works
LIF removal increases CRABPI and CRABPII transcripts in embryonic stem cells cultured in retinol or 4-oxoretinol
Lane, M. A., Xu, J., Wilen, E. W., Sylvester, R., Derguini, F., & Gudas, L. J. (2007) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2007.09.010 · Cited by 21 · see citing works
Self-citation
ERβ Sensitizes Breast Cancer Cells to Retinoic Acid: Evidence of Transcriptional Crosstalk
Rousseau, C., Nichol, J. N., Pettersson, F., Couture, M.-C., & Miller, W. H. (2004) · Molecular Cancer Research · doi:10.1158/1541-7786.523.2.9 · Cited by 21 · see citing works
Chicken Ovalbumin Upstream Promoter-Transcription Factor Members Repress Retinoic Acid-induced Cdx1 Expression
Béland, M., & Lohnes, D. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m412981200 · Cited by 19 · see citing works
Metabolism and regulation of gene expression by 4‐oxoretinol versus all‐trans retinoic acid in normal human mammary epithelial cells
Liu, L., Derguini, F., & Gudas, L. J. (2009) · Journal of Cellular Physiology · doi:10.1002/jcp.21824 · Cited by 9 · see citing works
Self-citation
Retinoic acid regulation of eye and testis-specific transcripts within a complex locus
Das, P., Doyle, T. J., Liu, D., Kochar, J., Kim, K. H., & Rogers, M. B. (2006) · Mechanisms of Development · doi:10.1016/j.mod.2006.10.004 · Cited by 7 · see citing works

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Mechanisms of retinoic acid signalling and its roles in organ and limb development
Cunningham, T. J., & Duester, G. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3932 · Cited by 602 · see citing works
Vitamin A Update: Forms, Sources, Kinetics, Detection, Function, Deficiency, Therapeutic Use and Toxicity
Carazo, A., Macáková, K., Matoušová, K., Krčmová, L. K., Protti, M., & Mladěnka, P. (2021) · Nutrients · doi:10.3390/nu13051703 · Cited by 418 · see citing works
Imidazoles as potential anticancer agents
Ali, I., Lone, M. N., & Aboul‐Enein, H. Y. (2017) · MedChemComm · doi:10.1039/c7md00067g · Cited by 413 · 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
Therapeutic regulation of myeloid-derived suppressor cells and immune response to cancer vaccine in patients with extensive stage small cell lung cancer
Iclozan, C., Antonia, S. J., Chiappori, A., Chen, D., & Gabrilovich, D. I. (2013) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-013-1396-8 · Cited by 318 · see citing works
Retinoic acid synthesis and functions in early embryonic development
Kin Ting Kam, R., Deng, Y., Chen, Y., & Zhao, H. (2012) · Cell & Bioscience · doi:10.1186/2045-3701-2-11 · Cited by 283 · see citing works
Retinoic acid signaling pathways in development and diseases
Das, B. C., Thapa, P., Karki, R., Das, S., Mahapatra, S., Liu, T.-C., Torregroza, I., Wallace, D. P., Kambhampati, S., Van Veldhuizen, P., et al. (2014) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2013.11.025 · Cited by 276 · see citing works
A nanotherapeutic strategy to overcome chemotherapeutic resistance of cancer stem-like cells
Shen, S., Xu, X., Lin, S., Zhang, Y., Liu, H., Zhang, C., & Mo, R. (2021) · Nature Nanotechnology · doi:10.1038/s41565-020-00793-0 · Cited by 266 · see citing works
Biodegradable Hollow Mesoporous Silica Nanoparticles for Regulating Tumor Microenvironment and Enhancing Antitumor Efficiency
Kong, M., Tang, J., Qiao, Q., Wu, T., Qi, Y., Tan, S., Gao, X., & Zhang, Z. (2017) · Theranostics · doi:10.7150/thno.19987 · Cited by 197 · see citing works
Enzymology of retinoic acid biosynthesis and degradation
Kedishvili, N. Y. (2013) · Journal of Lipid Research · doi:10.1194/jlr.r037028 · Cited by 196 · see citing works
Vitamin A Metabolism, Action, and Role in Skeletal Homeostasis
Conaway, H. H., Henning, P., & Lerner, U. H. (2013) · Endocrine Reviews · doi:10.1210/er.2012-1071 · Cited by 189 · see citing works
Dynamics of lineage commitment revealed by single-cell transcriptomics of differentiating embryonic stem cells
Semrau, S., Goldmann, J. E., Soumillon, M., Mikkelsen, T. S., Jaenisch, R., & van Oudenaarden, A. (2017) · Nature Communications · doi:10.1038/s41467-017-01076-4 · Cited by 182 · see citing works
Co-delivery of all-trans-retinoic acid and doxorubicin for cancer therapy with synergistic inhibition of cancer stem cells
Sun, R., Liu, Y., Li, S.-Y., Shen, S., Du, X.-J., Xu, C.-F., Cao, Z.-T., Bao, Y., Zhu, Y.-H., Li, Y.-P., et al. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2014.10.018 · Cited by 172 · see citing works
An update on the phenotypic switching of vascular smooth muscle cells in the pathogenesis of atherosclerosis
Zhang, F. S., Guo, X. Q., Xia, Y., & Mao, L. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-04079-z · Cited by 170 · see citing works
Retinoid Signaling in Progenitors Controls Specification and Regeneration of the Urothelium
Gandhi, D., Molotkov, A., Batourina, E., Schneider, K., Dan, H., Reiley, M., Laufer, E., METZGER, D., Liang, F., Liao, Y., et al. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.07.017 · Cited by 165 · see citing works
Pathophysiology of ocular surface squamous neoplasia
Gichuhi, S., Ohnuma, S., Sagoo, M. S., & Burton, M. J. (2014) · Experimental Eye Research · doi:10.1016/j.exer.2014.10.015 · Cited by 166 · see citing works
A set of genes critical to development is epigenetically poised in mouse germ cells from fetal stages through completion of meiosis
Lesch, B. J., Dokshin, G. A., Young, R. A., McCarrey, J. R., & Page, D. C. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1315204110 · Cited by 161 · see citing works
Emerging roles for retinoids in regeneration and differentiation in normal and disease states
Gudas, L. J. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2011.08.002 · Cited by 158 · see citing works
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ALDH as a Stem Cell Marker in Solid Tumors
Toledo-Guzmán, M. E., Ibáñez-Hernández, M. Á., Gallegos, A. A. G., & Ortíz-Sánchez, E. (2018) · Current Stem Cell Research & Therapy · doi:10.2174/1574888x13666180810120012 · Cited by 150 · see citing works
3D graphene oxide-encapsulated gold nanoparticles to detect neural stem cell differentiation
Kim, T. P., Lee, K., & Choi, J. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.07.101 · Cited by 142 · see citing works
Ovarian cancer stem cells and targeted therapy
Keyvani, V., Farshchian, M., Esmaeili, S., Yari, H., Moghbeli, M., Nezhad, S. R. K., & Abbaszadegan, M. R. (2019) · Journal of Ovarian Research · doi:10.1186/s13048-019-0588-z · Cited by 138 · see citing works
Proteinuria Impairs Podocyte Regeneration by Sequestering Retinoic Acid
Peired, A. J., Angelotti, M. L., Ronconi, E., la Marca, G., Mazzinghi, B., Sisti, A., Lombardi, D., Giocaliere, E., Bona, M. D., Villanelli, F., et al. (2013) · Journal of the American Society of Nephrology · doi:10.1681/asn.2012090950 · Cited by 139 · 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
Aldehyde dehydrogenase 1A3 influences breast cancer progression via differential retinoic acid signaling
Marcato, P., Dean, C. A., Liu, R., Coyle, K. M., Bydoun, M., Wallace, M., Clements, D. R., Turner, C., Mathenge, E. G., Gujar, S. A., et al. (2014) · Molecular Oncology · doi:10.1016/j.molonc.2014.07.010 · Cited by 132 · see citing works
Apoptosis May Explain the Pharmacological Mode of Action and Adverse Effects of Isotretinoin, Including Teratogenicity
Melnik, B. C. (2017) · Acta Dermato Venereologica · doi:10.2340/00015555-2535 · Cited by 131 · see citing works
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Authors: Gudas, L. J., & Wagner, J. A.
Affiliations: Cornell University (US)
Corresponding author: Gudas, Lorraine J.
ORCID: Gudas, Lorraine J.
Venue: Journal of Cellular Physiology
Publisher: Wiley
Published: 2010-11-26
Volume: 226
Issue: 2
Pages: 322-330
ISSN: 0021-9541 (ISSN-L)
1097-4652
DOI: 10.1002/jcp.22417
PMC: PMC3315372
OpenAlex: W2108254285
Cited by: 395
References: 133
Citations by year: 2026: 7 · 2025: 18 · 2024: 26 · 2023: 25 · 2022: 29 · 2021: 20 · 2020: 28 · 2019: 21 · 2018: 22 · 2017: 31 · 2016: 27 · 2015: 29 · 2014: 22 · 2013: 40 · 2012: 25
FWCI: 2.50
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Journal of Cellular Physiology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Cancer Institute (R01CA043796)
National Institute of Dental and Craniofacial Research (R01DE010389)
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 › Peroxisome Proliferator-Activated Receptors
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
Keywords: retinoids, all-trans retinoic acid, stem cell differentiation, retinoic acid receptor, retinoid X receptor, epigenetic regulation, drug sensitization, therapeutic target
MeSH terms: Animals, Cell Differentiation, Retinoids, Stem Cells, Transcription Factors, Transcription, Genetic, Tumor Cells, Cultured, Signal Transduction, beta Catenin, TNF-Related Apoptosis-Inducing Ligand

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Retinoids regulate stem cell differentiation

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