Opposing Effects of Retinoic Acid on Cell Growth Result from Alternate Activation of Two Different Nuclear Receptors

Cell

Volumn 129, Issue 4, 2007, Pages 723-733

  Schug, Thaddeus T ^a   Berry, Daniel C ^a,b   Shaw, Natacha S ^a   Travis, Skylar N ^a   Noy, Noa ^a,b  

^a Department of Obstetrics Gynecology   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID BINDING PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; RETINOIC ACID; RETINOIC ACID BINDING PROTEIN; RETINOIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOSOL; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION INITIATION; TUMOR GROWTH;

EID: 34249087361     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2007.02.050     Document Type: Article

References (63)

1. Akagi K., Sandig V., Vooijs M., Van der Valk M., Giovannini M., Strauss M., and Berns A. Cre-mediated somatic site-specific recombination in mice. Nucleic Acids Res. 25 (1997) 1766-1773
2. Allen G.W., Liu J.W., and De Leon M. Depletion of a fatty acid-binding protein impairs neurite outgrowth in PC12 cells. Brain Res. Mol. Brain Res. 76 (2000) 315-324
3. Altucci L., Rossin A., Raffelsberger W., Reitmair A., Chomienne C., and Gronemeyer H. Retinoic acid-induced apoptosis in leukemia cells is mediated by paracrine action of tumor-selective death ligand TRAIL. Nat. Med. 7 (2001) 680-686
4. Brouard M.C., Saurat J.H., Ghanem G., and Siegenthaler G. Urinary excretion of epidermal-type fatty acid-binding protein and S100A7 protein in patients with cutaneous melanoma. Melanoma Res. 12 (2002) 627-631
5. Bucco R.A., Zheng W.L., Davis J.T., Sierra-Rivera E., Osteen K.G., Chaudhary A.K., and Ong D.E. Cellular retinoic acid-binding protein(II) presence in rat uterine epithelial cells correlates with their synthesis of retinoic acid. Biochemistry 36 (1997) 4009-4014
6. Budhu A.S., and Noy N. Direct channeling of retinoic acid between cellular retinoic acid-binding protein II and retinoic acid receptor sensitizes mammary carcinoma cells to retinoic acid-induced growth arrest. Mol. Cell. Biol. 22 (2002) 2632-2641
7. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J. 10 (1996) 940-954
8. Chapellier B., Mark M., Messaddeq N., Calleja C., Warot X., Brocard J., Gerard C., Li M., Metzger D., Ghyselinck N.B., and Chambon P. Physiological and retinoid-induced proliferations of epidermis basal keratinocytes are differently controlled. EMBO J. 21 (2002) 3402-3413
9. De Leon M., Welcher A.A., Nahin R.H., Liu Y., Ruda M.A., Shooter E.M., and Molina C.A. Fatty acid binding protein is induced in neurons of the dorsal root ganglia after peripheral nerve injury. J. Neurosci. Res. 44 (1996) 283-292
10. Di-Poi N., Michalik L., Tan N.S., Desvergne B., and Wahli W. The anti-apoptotic role of PPARbeta contributes to efficient skin wound healing. J. Steroid Biochem. Mol. Biol. 85 (2003) 257-265
11. Di-Poi N., Tan N.S., Michalik L., Wahli W., and Desvergne B. Antiapoptotic role of PPARbeta in keratinocytes via transcriptional control of the Akt1 signaling pathway. Mol. Cell 10 (2002) 721-733
12. Donato L.J., and Noy N. Suppression of mammary carcinoma growth by retinoic acid: proapoptotic genes are targets for retinoic acid receptor and cellular retinoic acid-binding protein II signaling. Cancer Res. 65 (2005) 8193-8199
13. Donato L.J., Suh J.H., and Noy N. Suppression of mammary carcinoma cell growth by retinoic acid: the cell cycle control gene Btg2 is a direct target for retinoic acid receptor signaling. Cancer Res. 67 (2007) 609-615
14. Dong D., Ruuska S.E., Levinthal D.J., and Noy N. Distinct roles for cellular retinoic acid-binding proteins I and II in regulating signaling by retinoic acid. J. Biol. Chem. 274 (1999) 23695-23698
15. Guardavaccaro D., Corrente G., Covone F., Micheli L., D'Agnano I., Starace G., Caruso M., and Tirone F. Arrest of G(1)-S progression by the p53-inducible gene PC3 is Rb dependent and relies on the inhibition of cyclin D1 transcription. Mol. Cell. Biol. 20 (2000) 1797-1815
16. Gutierrez-Gonzalez L.H., Ludwig C., Hohoff C., Rademacher M., Hanhoff T., Ruterjans H., Spener F., and Lucke C. Solution structure and backbone dynamics of human epidermal-type fatty acid-binding protein (E-FABP). Biochem. J. 364 (2002) 725-737
17. Guy C.T., Webster M.A., Schaller M., Parsons T.J., Cardiff R.D., and Muller W.J. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc. Natl. Acad. Sci. USA 89 (1992) 10578-10582
18. Hanhoff T., Lucke C., and Spener F. Insights into binding of fatty acids by fatty acid binding proteins. Mol. Cell. Biochem. 239 (2002) 45-54
19. Henion P.D., and Weston J.A. Retinoic acid selectively promotes the survival and proliferation of neurogenic precursors in cultured neural crest cell populations. Dev. Biol. 161 (1994) 243-250
20. Icre G., Wahli W., and Michalik L. Functions of the peroxisome proliferator-activated receptor (PPAR) alpha and beta in skin homeostasis, epithelial repair, and morphogenesis. J. Invest. Dermatol. 126 Suppl (2006) 30-35
21. Jacobs S., Lie D.C., DeCicco K.L., Shi Y., DeLuca L.M., Gage F.H., and Evans R.M. Retinoic acid is required early during adult neurogenesis in the dentate gyrus. Proc. Natl. Acad. Sci. USA 103 (2006) 3902-3907
22. Kang S., Duell E.A., Fisher G.J., Datta S.C., Wang Z.Q., Reddy A.P., Tavakkol A., Yi J.Y., Griffiths C.E., Elder J.T., et al. Application of retinol to human skin in vivo induces epidermal hyperplasia and cellular retinoid binding proteins characteristic of retinoic acid but without measurable retinoic acid levels or irritation. J. Invest. Dermatol. 105 (1995) 549-556
23. Kawakubo H., Brachtel E., Hayashida T., Yeo G., Kish J., Muzikansky A., Walden P.D., and Maheswaran S. Loss of B-cell translocation gene-2 in estrogen receptor-positive breast carcinoma is associated with tumor grade and overexpression of cyclin d1 protein. Cancer Res. 66 (2006) 7075-7082
24. Kawakubo H., Carey J.L., Brachtel E., Gupta V., Green J.E., Walden P.D., and Maheswaran S. Expression of the NF-kappaB-responsive gene BTG2 is aberrantly regulated in breast cancer. Oncogene 23 (2004) 8310-8319
25. Kersten S., Mandard S., Tan N.S., Escher P., Metzger D., Chambon P., Gonzalez F.J., Desvergne B., and Wahli W. Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene. J. Biol. Chem. 275 (2000) 28488-28493
26. King C.R., Kraus M.H., and Aaronson S.A. Amplification of a novel v-erbB-related gene in a human mammary carcinoma. Science 229 (1985) 974-976
27. Kitareewan S., Pitha-Rowe I., Sekula D., Lowrey C.H., Nemeth M.J., Golub T.R., Freemantle S.J., and Dmitrovsky E. UBE1L is a retinoid target that triggers PML/RARalpha degradation and apoptosis in acute promyelocytic leukemia. Proc. Natl. Acad. Sci. USA 99 (2002) 3806-3811
28. Kleywegt G.J., Bergfors T., Senn H., Le Motte P., Gsell B., Shudo K., and Jones T.A. Crystal structures of cellular retinoic acid binding proteins I and II in complex with all-trans-retinoic acid and a synthetic retinoid. Structure 2 (1994) 1241-1258
29. Kliewer S.A., Forman B.M., Blumberg B., Ong E.S., Borgmeyer U., Mangelsdorf D.J., Umesono K., and Evans R.M. Differential expression and activation of a family of murine peroxisome proliferator-activated receptors. Proc. Natl. Acad. Sci. USA 91 (1994) 7355-7359
30. Laudet V., and Gronemeyer H. The Nuclear Receptor FactsBook (2002), Academic Press, London
31. Levin A.A., Sturzenbecker L.J., Kazmer S., Bosakowski T., Huselton C., Allenby G., Speck J., Kratzeisen C., Rosenberger M., Lovey A., et al. 9-cis retinoic acid stereoisomer binds and activates the nuclear receptor RXR alpha. Nature 355 (1992) 359-361
32. Lim R.W., Varnum B.C., O'Brien T.G., and Herschman H.R. Induction of tumor promotor-inducible genes in murine 3T3 cell lines and tetradecanoyl phorbol acetate-nonproliferative 3T3 variants can occur through protein kinase C-dependent and -independent pathways. Mol. Cell. Biol. 9 (1989) 1790-1793
33. Liu Y., Longo L.D., and De Leon M. In situ and immunocytochemical localization of E-FABP mRNA and protein during neuronal migration and differentiation in the rat brain. Brain Res. 852 (2000) 16-27
34. Loudig O., Babichuk C., White J., Abu-Abed S., Mueller C., and Petkovich M. Cytochrome P450RAI(CYP26) promoter: a distinct composite retinoic acid response element underlies the complex regulation of retinoic acid metabolism. Mol. Endocrinol. 14 (2000) 1483-1497
35. Mangelsdorf D., Umesono K., and Evans R.M. The retinoid receptors. In: Sporn M.B., Roberts A.B., and Goodman D.S. (Eds). The Retinoids, Biology, Chemistry and Medicine (1994), Raven Press, New York 319-350
36. Mangiarotti R., Danova M., Alberici R., and Pellicciari C. All-trans retinoic acid (ATRA)-induced apoptosis is preceded by G1 arrest in human MCF-7 breast cancer cells. Br. J. Cancer 77 (1998) 186-191
37. Manor D., Shmidt E.N., Budhu A., Flesken-Nikitin A., Zgola M., Page R., Nikitin A.Y., and Noy N. Mammary carcinoma suppression by cellular retinoic acid binding protein-II. Cancer Res. 63 (2003) 4426-4433
38. Muller W.J., Sinn E., Pattengale P.K., Wallace R., and Leder P. Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell 54 (1988) 105-115
39. Norris A.W., and Spector A.A. Very long chain n-3 and n-6 polyunsaturated fatty acids bind strongly to liver fatty acid-binding protein. J. Lipid Res. 43 (2002) 646-653
40. Park D.J., Chumakov A.M., Vuong P.T., Chih D.Y., Gombart A.F., Miller Jr. W.H., and Koeffler H.P. CCAAT/enhancer binding protein epsilon is a potential retinoid target gene in acute promyelocytic leukemia treatment. J. Clin. Invest. 103 (1999) 1399-1408
41. Plum L.A., Parada L.F., Tsoulfas P., and Clagett-Dame M. Retinoic acid combined with neurotrophin-3 enhances the survival and neurite outgrowth of embryonic sympathetic neurons. Exp. Biol. Med. (Maywood) 226 (2001) 766-775
42. Rochette-Egly C., and Chambon P. F9 embryocarcinoma cells: a cell autonomous model to study the functional selectivity of RARs and RXRs in retinoid signaling. Histol. Histopathol. 16 (2001) 909-922
43. Rodriguez-Tebar A., and Rohrer H. Retinoic acid induces NGF-dependent survival response and high-affinity NGF receptors in immature chick sympathetic neurons. Development 112 (1991) 813-820
44. Schmuth M., Haqq C.M., Cairns W.J., Holder J.C., Dorsam S., Chang S., Lau P., Fowler A.J., Chuang G., Moser A.H., et al. Peroxisome proliferator-activated receptor (PPAR)-beta/delta stimulates differentiation and lipid accumulation in keratinocytes. J. Invest. Dermatol. 122 (2004) 971-983
45. Sessler R.J., and Noy N. A ligand-activated nuclear localization signal in cellular retinoic acid binding protein-II. Mol. Cell 18 (2005) 343-353
46. Shaw N., Elholm M., and Noy N. Retinoic acid is a high affinity selective ligand for the peroxisome proliferator-activated receptor beta/delta. J. Biol. Chem. 278 (2003) 41589-41592
47. Soprano D.R., Qin P., and Soprano K.J. Retinoic acid receptors and cancers. Annu. Rev. Nutr. 24 (2004) 201-221
48. Strickland S., and Mahdavi V. The induction of differentiation in teratocarcinoma stem cells by retinoic acid. Cell 15 (1978) 393-403
49. Strickland S., Smith K.K., and Marotti K.R. Hormonal induction of differentiation in teratocarcinoma stem cells: generation of parietal endoderm by retinoic acid and dibutyryl cAMP. Cell 21 (1980) 347-355
50. Sussman F., and de Lera A.R. Ligand recognition by RAR and RXR receptors: binding and selectivity. J. Med. Chem. 48 (2005) 6212-6219
51. Tan N.S., Michalik L., Desvergne B., and Wahli W. Peroxisome proliferator-activated receptor-beta as a target for wound healing drugs. Expert Opin. Ther. Targets 8 (2004) 39-48
52. Tan N.S., Michalik L., Noy N., Yasmin R., Pacot C., Heim M., Fluhmann B., Desvergne B., and Wahli W. Critical roles of PPAR beta/delta in keratinocyte response to inflammation. Genes Dev. 15 (2001) 3263-3277
53. Tan N.S., Shaw N.S., Vinckenbosch N., Liu P., Yasmin R., Desvergne B., Wahli W., and Noy N. Selective cooperation between fatty acid binding proteins and peroxisome proliferator-activated receptors in regulating transcription. Mol. Cell. Biol. 22 (2002) 5114-5127
54. Tari A.M., Lim S.J., Hung M.C., Esteva F.J., and Lopez-Berestein G. Her2/neu induces all-trans retinoic acid (ATRA) resistance in breast cancer cells. Oncogene 21 (2002) 5224-5232
55. Toma S., Isnardi L., Riccardi L., and Bollag W. Induction of apoptosis in MCF-7 breast carcinoma cell line by RAR and RXR selective retinoids. Anticancer Res. 18 (1998) 935-942
56. Veerkamp J.H., and Maatman R.G. Cytoplasmic fatty acid-binding proteins: their structure and genes. Prog. Lipid Res. 34 (1995) 17-52
57. Verma A.K., Conrad E.A., and Boutwell R.K. Differential effects of retinoic acid and 7,8-benzoflavone on the induction of mouse skin tumors by the complete carcinogenesis process and by the initiation-promotion regimen. Cancer Res. 42 (1982) 3519-3525
58. White J.A., Guo Y.D., Baetz K., Beckett-Jones B., Bonasoro J., Hsu K.E., Dilworth F.J., Jones G., and Petkovich M. Identification of the retinoic acid-inducible all-trans-retinoic acid 4- hydroxylase. J. Biol. Chem. 271 (1996) 29922-29927
59. Widstrom R.L., Norris A.W., and Spector A.A. Binding of cytochrome P450 monooxygenase and lipoxygenase pathway products by heart fatty acid-binding protein. Biochemistry 40 (2001) 1070-1076
60. Wolbach S.B., and Howe P.R. Nutrition Classics. The Journal of Experimental Medicine 42: 753-77, 1925. Tissue changes following deprivation of fat-soluble A vitamin. S. Burt Wolbach and Percy R. Howe. Nutr. Rev. 36 (1978) 16-19
61. Wuarin L., Sidell N., and de Vellis J. Retinoids increase perinatal spinal cord neuronal survival and astroglial differentiation. Int. J. Dev. Neurosci. 8 (1990) 317-326
62. Xu H.E., Lambert M.H., Montana V.G., Parks D.J., Blanchard S.G., Brown P.J., Sternbach D.D., Lehmann J.M., Wisely G.B., Willson T.M., et al. Molecular recognition of fatty acids by peroxisome proliferator- activated receptors. Mol. Cell 3 (1999) 397-403
63. Zouboulis C.C. Retinoids-which dermatological indications will benefit in the near future?. Skin Pharmacol. Appl. Skin Physiol. 14 (2001) 303-315