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The FASEB Journal, Vol 5, 2924-2933, Copyright © 1991 by The Federation of American Societies for Experimental Biology

REVIEWS

Retinoids and their receptors in differentiation, embryogenesis, and neoplasia

LM De Luca
Laboratory of Cellular Carcinogenesis and Tumor Promotion, National Cancer Institute, Bethesda, Maryland 20892.

The crucial role of retinoids in controlling differentiation processes has become evident from studies conducted in a variety of in vivo and in vitro systems. Most striking is the role of retinoic acid as a morphogenic substance in vertebrate limb development, but equally important is its role in the maintenance of epithelial integrity in most superficial linings of the body. The similarity of the mode of action of retinoids to that of the steroid and thyroid hormones has recently been demonstrated with the discovery of the nuclear receptors for retinoic acid, which belong to the steroid/thyroid hormone receptor superfamily. These receptors act as transcriptional activators by binding as heterodimers to specific nucleotide sequences in the response elements of target genes. Response elements for retinoic acid have so far been identified for the rat growth hormone and phosphoenolpyruvate carboxykinase, the mouse complement H and laminin B1, the human and mouse retinoic acid receptor beta, the human osteocalcin, and the human alcohol dehydrogenase genes. The retinoic acid response element (RARE) for the rat growth hormone gene is also a thyroid hormone response element (TRE), and the AP-1 binding site of the human osteocalcin promoter is also a vitamin D response element (VDRE) and a RARE. Both these elements are palindromic. Other RAREs have a direct repeat configuration of the half-site motif AGGTCA separated by five nucleotides (AGGTCA xxxxx AGGTCA). The direct repeat arrangement of the same core motif AGGTCA separated by three or four nucleotides becomes a VDRE or TRE, respectively. A point mutation has been identified in the RAR alpha gene of embryonal carcinoma cells resistant to retinoic acid. In addition to the three retinoic acid receptors (alpha, beta, gamma) belonging to the steroid/thyroid hormone receptor superfamily, a second class of retinoid receptors (RXR) alpha, beta, gamma has also been characterized and its relatedness to a gene, XR2C, of the locus ultraspiracle required for pattern formation in Drosophila has been established. That would suggest that both vertebrates and invertebrates may require similar transcriptional activators during morphogenesis. An RXRE has been identified in the CRBPII gene promoter and it contains five repeats of the canonical sequence AGGTCA separated by one nucleotide. The importance of retinoids, both as chemopreventive agents of tumorigenesis and potent differentiation inducers of neoplastic cells, can only be emphasized by the recent finding that the t(15;17) (q21- q11-22) translocation, specifically associated with acute promyelocytic leukemia, also causes translocation of the retinoic acid receptor alpha gene and its fusion with with a new locus, myl, of unknown function.(ABSTRACT TRUNCATED AT 250 WORDS)


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G. M. Ledda-Columbano, A. Perra, R. Loi, H. Shinozuka, and A. Columbano
Cell Proliferation Induced by Triiodothyronine in Rat Liver Is Associated with Nodule Regression and Reduction of Hepatocellular Carcinomas
Cancer Res., February 1, 2000; 60(3): 603 - 609.
[Abstract] [Full Text]

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 JCOHome page
Y. Lotan, X. C. Xu, M. Shalev, R. Lotan, R. Williams, T. M. Wheeler, T. C. Thompson, and D. Kadmon
Differential Expression of Nuclear Retinoid Receptors in Normal and Malignant Prostates
J. Clin. Oncol., January 1, 2000; 18(1): 116 - 116.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Y. Iitsuka, H. Shimizu, M. M. Kang, K. Sasagawa, S. Sekiya, T. Tokuhisa, and M. Hatano
An Enhancer Element for Expression of the Ncx (Enx, Hox11L1) Gene in Neural Crest-derived Cells
J. Biol. Chem., August 20, 1999; 274(34): 24401 - 24407.
[Abstract] [Full Text] [PDF]

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 Cell Growth Differ.Home page
J. X. Kang, J. Bell, R. L. Beard, and R. A. S. Chandraratna
Mannose 6-Phosphate/Insulin-like Growth Factor II Receptor Mediates the Growth-Inhibitory Effects of Retinoids
Cell Growth Differ., August 1, 1999; 10(8): 591 - 600.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
V. Moreno-Manzano, Y. Ishikawa, J. Lucio-Cazana, and M. Kitamura
Suppression of Apoptosis by All-trans-Retinoic Acid. DUAL INTERVENTION IN THE c-JUN N-TERMINAL KINASE-AP-1 PATHWAY
J. Biol. Chem., July 16, 1999; 274(29): 20251 - 20258.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. Kaiser, F. H. Brembeck, B. Nicke, B. Wiedenmann, E.-O. Riecken, and S. Rosewicz
All-trans-Retinoic Acid-mediated Growth Inhibition Involves Inhibition of Human Kinesin-related Protein HsEg5
J. Biol. Chem., July 2, 1999; 274(27): 18925 - 18931.
[Abstract] [Full Text] [PDF]

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 GutHome page
K Hellemans, I Grinko, K Rombouts, D Schuppan, and A Geerts
All-trans and 9-cis retinoic acid alter rat hepatic stellate cell phenotype differentially
Gut, July 1, 1999; 45(1): 134 - 142.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
H. Wan, N. Oridate, D. Lotan, W. K. Hong, and R. Lotan
Overexpression of Retinoic Acid Receptor {beta} in Head and Neck Squamous Cell Carcinoma Cells Increases Their Sensitivity to Retinoid-induced Suppression of Squamous Differentiation by Retinoids
Cancer Res., July 1, 1999; 59(14): 3518 - 3526.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S.-Y. Sun, P. Yue, G. S. Wu, W. S. El-Deiry, B. Shroot, W. K. Hong, and R. Lotan
Implication of p53 in Growth Arrest and Apoptosis Induced by the Synthetic Retinoid CD437 in Human Lung Cancer Cells
Cancer Res., June 1, 1999; 59(12): 2829 - 2833.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
X.-C. Xu, X. Liu, E. Tahara, S. M. Lippman, and R. Lotan
Expression and Up-Regulation of Retinoic Acid Receptor-{beta} Is Associated with Retinoid Sensitivity and Colony Formation in Esophageal Cancer Cell Lines
Cancer Res., May 1, 1999; 59(10): 2477 - 2483.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
S.-Y. Sun, P. Yue, and R. Lotan
Induction of Apoptosis by N-(4-Hydroxyphenyl)retinamide and Its Association with Reactive Oxygen Species, Nuclear Retinoic Acid Receptors, and Apoptosis-Related Genes in Human Prostate Carcinoma Cells
Mol. Pharmacol., March 1, 1999; 55(3): 403 - 410.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
J. Tremblay, D.B. Hardy, L.E. Pereira, and K. Yang
Retinoic Acid Stimulates the Expression of 11ß-Hydroxysteroid Dehydrogenase Type 2 in Human Choriocarcinoma JEG-3 Cells
Biol Reprod, March 1, 1999; 60(3): 541 - 545.
[Abstract] [Full Text]

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 BloodHome page
J. Dimitroulakos, D. Nohynek, K. L. Backway, D. W. Hedley, H. Yeger, M. H. Freedman, M. D. Minden, and L. Z. Penn
Increased Sensitivity of Acute Myeloid Leukemias to Lovastatin-Induced Apoptosis: A Potential Therapeutic Approach
Blood, February 15, 1999; 93(4): 1308 - 1318.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
W.-Y. Zhu, C. S. Jones, S. Amin, K. Matsukuma, M. Haque, V. Vuligonda, R. A. S. Chandraratna, and L. M. De Luca
Retinoic Acid Increases Tyrosine Phosphorylation of Focal Adhesion Kinase and Paxillin in MCF-7 Human Breast Cancer Cells
Cancer Res., January 1, 1999; 59(1): 85 - 90.
[Abstract] [Full Text] [PDF]

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 BloodHome page
C. Rius, J. D. Smith, N. Almendro, C. Langa, L. M. Botella, D. A. Marchuk, C. P.H. Vary, and C. Bernabeu
Cloning of the Promoter Region of Human Endoglin, the Target Gene for Hereditary Hemorrhagic Telangiectasia Type 1
Blood, December 15, 1998; 92(12): 4677 - 4690.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Renal Physiol.Home page
E. Moreau, J. Vilar, M. Lelievre-Pegorier, C. Merlet-Benichou, and T. Gilbert
Regulation of c-ret expression by retinoic acid in rat metanephros: implication in nephron mass control
Am J Physiol Renal Physiol, December 1, 1998; 275(6): F938 - F945.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
E. Papadimou, S. Georgiou, D. Tsambaos, and D. Drainas
Inhibition of Ribonuclease P Activity by Retinoids
J. Biol. Chem., September 18, 1998; 273(38): 24375 - 24378.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
C. D. Katsetos, I. Stadnicka, J. C. Boyd, H. Ehya, S. Zheng, C. M. Soprano, H. S. Cooper, A. S. Patchefsky, D. R. Soprano, and K. J. Soprano
Cellular Distribution of Retinoic Acid Receptor-{alpha} Protein in Serous Adenocarcinomas of Ovarian, Tubal, and Peritoneal Origin : Comparison with Estrogen Receptor Status
Am. J. Pathol., August 1, 1998; 153(2): 469 - 480.
[Abstract] [Full Text] [PDF]

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 J. Nutr.Home page
J. Sarkar, N. N. Gangopadhyay, Z. Moldoveanu, J. Mestecky, and C. B. Stephensen
Vitamin A Is Required for Regulation of Polymeric Immunoglobulin Receptor (pIgR) Expression by Interleukin-4 and Interferon-gamma in a Human Intestinal Epithelial Cell Line
J. Nutr., July 1, 1998; 128(7): 1063 - 1069.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Z. H. Yan, W. G. Karam, J. L. Staudinger, A. Medvedev, B. I. Ghanayem, and A. M. Jetten
Regulation of Peroxisome Proliferator-activated Receptor alpha -Induced Transactivation by the Nuclear Orphan Receptor TAK1/TR4
J. Biol. Chem., May 1, 1998; 273(18): 10948 - 10957.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Cell Mol. Bio.Home page
H. Adachi, G. Preston, B. Harvat, M. I. Dawson, and A. M. Jetten
Inhibition of Cell Proliferation and Induction of Apoptosis by the Retinoid AHPN in Human Lung Carcinoma Cells
Am. J. Respir. Cell Mol. Biol., March 1, 1998; 18(3): 323 - 333.
[Abstract] [Full Text]

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 J. Cell Sci.Home page
B Risek, A Pozzi, and N. Gilula
Modulation of gap junction expression during transient hyperplasia of rat epidermis
J. Cell Sci., January 5, 1998; 111(10): 1395 - 1404.
[Abstract] [PDF]

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 Mol. Endocrinol.Home page
R. K. Gill, L. M. Atkins, B. W. Hollis, and N. H. Bell
Mapping the Domains of the Interaction of the Vitamin D Receptor and Steroid Receptor Coactivator-1
Mol. Endocrinol., January 1, 1998; 12(1): 57 - 65.
[Abstract] [Full Text]

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 Proc. Natl. Acad. Sci. USAHome page
J. X. Kang, Y. Li, and A. Leaf
Mannose-6-phosphate/insulin-like growth factor-II receptor is a receptor for retinoic acid
PNAS, December 9, 1997; 94(25): 13671 - 13676.
[Abstract] [Full Text] [PDF]

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 JCBHome page
H. Chiba, J. Clifford, D. Metzger, and P. Chambon
Specific and Redundant Functions of Retinoid X Receptor/Retinoic Acid Receptor Heterodimers in Differentiation, Proliferation, and Apoptosis of F9 Embryonal Carcinoma Cells
J. Cell Biol., November 3, 1997; 139(3): 735 - 747.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
R. A. Spanjaard, M. Ikeda, P. J. Lee, B. Charpentier, W. W. Chin, and T. J. Eberlein
Specific Activation of Retinoic Acid Receptors (RARs) and Retinoid X Receptors Reveals a Unique Role for RARgamma in Induction of Differentiation and Apoptosis of S91 Melanoma Cells
J. Biol. Chem., July 25, 1997; 272(30): 18990 - 18999.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
B.-j. M. van der Leede, C. E. van den Brink, W. W. M. Pijnappel, E. Sonneveld, P. T. van der Saag, and B. van der Burg
Autoinduction of Retinoic Acid Metabolism to Polar Derivatives with Decreased Biological Activity in Retinoic Acid-sensitive, but Not in Retinoic Acid-resistant Human Breast Cancer Cells
J. Biol. Chem., July 18, 1997; 272(29): 17921 - 17928.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. Botling, D. S. Castro, F. Oberg, K. Nilsson, and T. Perlmann
Retinoic Acid Receptor/Retinoid X Receptor Heterodimers Can Be Activated through Both Subunits Providing a Basis for Synergistic Transactivation and Cellular Differentiation
J. Biol. Chem., April 4, 1997; 272(14): 9443 - 9449.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
H. F. S. Huang, M.-t. Li, S. Von Hagen, Y. F. Zhang, and R. J. Irwin
Androgen Modulation of the Messenger Ribonucleic Acid of Retinoic Acid Receptors in the Prostate, Seminal Vesicles, and Kidney in the Rat
Endocrinology, February 1, 1997; 138(2): 553 - 559.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
M Plateroti, J. Freund, C Leberquier, and M Kedinger
Mesenchyme-mediated effects of retinoic acid during rat intestinal development
J. Cell Sci., January 5, 1997; 110(10): 1227 - 1238.
[Abstract] [PDF]

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 J. Biol. Chem.Home page
M. Cippitelli, J. Ye, V. Viggiano, A. Sica, P. Ghosh, A. Gulino, A. Santoni, and H. A. Young
Retinoic Acid-induced Transcriptional Modulation of the Human Interferon-gamma Promoter
J. Biol. Chem., October 25, 1996; 271(43): 26783 - 26793.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. E. Driscoll, C. L. Seachord, J. A. Lupisella, R. P. Darveau, and P. R. Reczek
Ligand-induced Conformational Changes in the Human Retinoic Acid Receptor gamma Detected Using Monoclonal Antibodies
J. Biol. Chem., September 20, 1996; 271(38): 22969 - 22975.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. Desai, M. Michalak, N. K. Singh, and R. M. Niles
Inhibition of Retinoic Acid Receptor Function and Retinoic Acid-regulated Gene Expression in Mouse Melanoma Cells by Calreticulin. A POTENTIAL PATHWAY FOR CYCLIC AMP REGULATION OF RETINOID ACTION
J. Biol. Chem., June 21, 1996; 271(25): 15153 - 15159.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
G. Scita, N. Darwiche, E. Greenwald, M. Rosenberg, K. Politi, and L. M. De Luca
Retinoic Acid Down-regulation of Fibronectin and Retinoic Acid Receptor alpha Proteins in NIH-3T3 Cells
J. Biol. Chem., March 15, 1996; 271(11): 6502 - 6508.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. K. Cho, J.-c. Yeh, M. Cho, and R. D. Cummings
Transcriptional Regulation of alpha1,3-Galactosyltransferase in Embryonal Carcinoma Cells by Retinoic Acid
J. Biol. Chem., February 9, 1996; 271(6): 3238 - 3246.
[Abstract] [Full Text] [PDF]

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 CROBMHome page
D.T.W. Wong, R. Todd, T. Tsuji, and R.B. Donoff
Molecular Biology of Human Oral Cancer
Critical Reviews in Oral Biology & Medicine, January 1, 1996; 7(4): 319 - 328.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
R. A. Spanjaard, A. Sugawara, M. Ikeda, and W. W. Chin
Evidence that Retinoid X Receptors Mediate Retinoid-dependent Transcriptional Activation of the Retinoic Acid Receptor [IMAGE] Gene in S91 Melanoma Cells
J. Biol. Chem., July 21, 1995; 270(29): 17429 - 17436.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Y. Yanagawa, J. C. Chen, L. C. Hsu, and A. Yoshida
The Transcriptional Regulation of Human Aldehyde Dehydrogenase I Gene
J. Biol. Chem., July 21, 1995; 270(29): 17521 - 17527.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. gombi&;-Knight, H. L. Ang, M. H. Foglio, and G. Duester
Cloning of the Mouse Class IV Alcohol Dehydrogenase (Retinol Dehydrogenase) cDNA and Tissue-specific Expression Patterns of the Murine ADH Gene Family
J. Biol. Chem., May 5, 1995; 270(18): 10868 - 10877.
[Abstract] [Full Text] [PDF]


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