Nonclassical action of retinoic acid on the activation of the cAMP response element-binding protein in normal human bronchial epithelial cells

Molecular Biology of the Cell

Volumn 17, Issue 2, 2006, Pages 566-575

  Aggarwal, Sita ^a   Kim, Seung Wook ^a   Cheon, Kyounga ^a   Tabassam, Fazal H ^a   Yoon, Joo Heon ^b   Koo, Ja Seok ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b Yonsei University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE C; RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOID X RECEPTOR; RETINOL; S6 KINASE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR;

ARTICLE; BRONCHUS MUCOSA; CELL DIFFERENTIATION; CELL GROWTH; CONTROLLED STUDY; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; MUCOCILIARY CLEARANCE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

BRONCHI; CELL LINE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MAP KINASE SIGNALING SYSTEM; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASES; RESPIRATORY MUCOSA; RETINOID X RECEPTORS; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TRETINOIN;

EID: 31944443124     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-06-0519     Document Type: Article

References (50)

1. Aggarwal, S., Takada, Y., Mhashilkar, A. M., Sieger, K., Chada, S., and Aggarwal, B. B. (2004). Melanoma differentiation-associated gene-7/IL-24 gene enhances NF-kappa B activation and suppresses apoptosis induced by TNF. J. Immunol. 173, 4368-4376.
2. Alsayed, Y., Uddin, S., Mahmud, N., Lekmine, F., Kalvakolanu, D. V., Minucci, S., Bokoch, G., and Platanias, L. C. (2001). Activation of Rac1 and the p38 mitogen-activated protein kinase pathway in response to all-trans-retinoic acid. J. Biol. Chem. 276, 4012-4019.
3. Canon, E., Cosgaya, J. M., Scsucova, S., and Aranda, A. (2004). Rapid effects of retinoic acid on CREB and ERK phosphorylation in neuronal cells. Mol. Biol. Cell 15, 5583-5592.
4. Chambon, P. (1996). A decade of molecular biology of retinoic acid receptors. FASEB J. 10, 940-954.
5. Deak, M., Clifton, A. D., Lucocq, L. M., and Alessi, D. R. (1998). Mitogen- and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J. 17, 4426-4441.
6. Du, K., and Montminy, M. (1998). CREB is a regulatory target for the protein kinase Akt/PKB. J. Biol. Chem. 273, 32377-32379.
7. Fix, C., Jordan, C., Cano, P., and Walker, W. H. (2004). Testosterone activates mitogen-activated protein kinase and the cAMP response element binding protein transcription factor in Sertoli cells. Proc. Natl. Acad. Sci. USA 101, 10919-10924.
8. Frodin, M., and Gammeltoft, S. (1999). Role and regulation of 90 kDa ribosomal S6 kinase (RSK) in signal transduction. Mol. Cell. Endocrinol. 151, 65-77.
9. Giguere, V. (1994). Retinoic acid receptors and cellular retinoid binding proteins: complex interplay in retinoid signaling. Endocr. Rev. 15, 61-79.
10. Ginty, D. D., Bonni, A., and Greenberg, M. E. (1994). Nerve growth factor activates a Ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB. Cell 77, 713-725.
11. Gonzalez, G. A., Yamamoto, K. K., Fischer, W. H., Karr, D., Menzel, P., Biggs, W., 3rd, Vale, W. W., and Montminy, M. R. (1989). A. cluster of phosphorylation sites on the cyclic AMP-regulated nuclear factor CREB predicted by its sequence. Nature 337, 749-752.
12. Gray, T., Nettesheim, P., Basbaum, C., and Koo, J. (2001). Regulation of mucin gene expression in human tracheobronchial epithelial cells by thyroid hormone. Biochem J 353, 727-734.
13. Gray, T. E., Guzman, K., Davis, C. W., Abdullah, L. H., and Nettesheim, P. (1996). Mucociliary differentiation of serially passaged normal human tracheobronchial epithelial cells. Am. J. Respir. Cell. Mol. Biol. 14, 104-112.
14. Gudas, L. J., Sporn, M. B., and Roberts, A. B. (1994). Cellular Biology and Biochemistry of the Retinoids. In: The Retinoids: Biology, Chemistry, and Medicine, ed. M. B. Sporn, A. B. Roberts, and D. S. Goodman, New York: Raven Press, 443-520.
15. Hagiwara, M., Brindle, P., Harootunian, A., Armstrong, R., Rivier, J., Vale, W., Tsien, R., and Montminy, M. R. (1993). Coupling of hormonal stimulation and transcription via the cyclic AMP-responsive factor CREB is rate limited by nuclear entry of protein kinase A. Mol. Cell. Biol. 13, 4852-4859.
16. Hoyos, B., Imam, A., Chua, R., Swenson, C., Tong, G. X., Levi, E., Noy, N., and Hammerling, U. (2000). The cysteine-rich regions of the regulatory domains of Raf and PKC as retinoid receptors. J Exp Med 192, 835-845.
17. Imam, A., Hoyos, B., Swenson, C., Levi, E., Chua, R., Viriya, E., and Hammerling, U. (2001). Retinoids as ligands and coactivators of PKC alpha. FASEB J. 15, 28-30.
18. Impey, S., McCorkle, S. R., Cha-Molstad, H., Dwyer, J. M., Yochum, G. S., Boss, J. M., McWeeney, S., Dunn, J. J., Mandel, G., and Goodman, R. H. (2004). Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell 119, 1041-1054.
19. Johannessen, M., Delghandi, M. P., and Moens, U. (2004). What turns CREB on? Cell Signal. 16, 1211-1227.
20. Kambhampati, S. et al. (2003). Activation of PKC delta by all-trans-retinoic acid. J. Biol. Chem. 278, 32544-32551.
21. Klemm, D. J., Watson, P. A., Frid, M. G., Dempsey, E. C., Schaack, J., Colton, L. A., Nesterova, A., Stenmark, K. R., and Reusch, J. E. (2001). cAMP response element-binding protein content is a molecular determinant of smooth muscle cell proliferation and migration. J. Biol. Chem. 276, 46132-46141.
22. Kolodziejski, P. J., Musial, A., Koo, J. S., and Eissa, N. T. (2002). Ubiquitination of inducible nitric oxide synthase is required for its degradation. Proc. Natl. Acad. Sci. USA 99, 12315-12320.
23. Koo, J. S., Yoon, J. H., Gray, T., Norford, D., Jetten, A. M., and Nettesheim, P. (1999). Restoration of the mucous phenotype by retinoic acid in retinoid-deficient human bronchial cell cultures: changes in mucin gene expression. Am. J. Respir. Cell. Mol. Biol. 20, 43-52.
24. Kruyt, F. A., Folkers, G., van den Brink, C. E., and van der Saag, P. T. (1992). A cyclic AMP response element is involved in retinoic acid-dependent RAR beta 2 promoter activation. Nucleic Acids Res. 20, 6393-6399.
25. Lopez-Andreo, M. J., Torrecillas, A., Conesa-Zamora, P., Corbalan-Garcia, S., and Gomez-Fernandez, J. C. (2005). Retinoic acid as a modulator of the activity of protein kinase calpha. Biochemistry 44, 11353-11360.
26. Mangelsdorf, D. J., and Evans, R. M. (1995). The RXR heterodimers and orphan receptors 83, 841-850.
27. Matthews, R. P., Guthrie, C. R., Wailes, L. M., Zhao, X., Means, A. R., and McKnight, G. S. (1994). Calcium/calmodulin-dependent protein kinase types II and IV differentially regulate CREB-dependent gene expression. Mol. Cell. Biol. 14, 6107-6116.
28. Mayr, B., and Montminy, M. (2001). Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell. Biol. 2, 599-609.
29. McDowell, E. M., Keenan, K. P., and Huang, M. (1984a). Effects of vitamin A-deprivation on hamster tracheal epithelium. A quantitative morphologic study. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 45, 197-219.
30. McDowell, E. M., Keenan, K. P., and Huang, M. (1984b). Restoration of mucociliary tracheal epithelium following deprivation of vitamin A. A quantitative morphologic study. Virchows Arch. B Cell Pathol. Incl. Mol. Pat. 45, 221-240.
31. Montminy, M. R., Gonzalez, G. A., and Yamamoto, K. K. (1990). Characteristics of the cAMP response unit. Metabolism 39, 6-12.
32. Nguyen, L. Q., Kopp, P., Martinson, F., Stanfield, K., Roth, S. I., and Jameson, J. L. (2000). A dominant negative CREB (cAMP response element-binding protein) isoform inhibits thyrocyte growth, thyroid-specific gene expression, differentiation, and function. Mol. Endocrinol. 14, 1448-1461.
33. Ochoa, W. F., Corbalan-Garcia, S., Eritja, R., Rodriguez-Alfaro, J. A., Gomez-Fernandez, J. C., Fita, I., and Verdaguer, N. (2002). Additional binding sites for anionic phospholipids and calcium ions in the crystal structures of complexes of the C2 domain of protein kinase calpha. J. Mol. Biol. 320, 277-291.
34. Ochoa, W. F., Torrecillas, A., Fita, I., Verdaguer, N., Corbalan-Garcia, S., and Gomez-Fernandez, J. C. (2003). Retinoic acid binds to the C2-domain of PKC(alpha). Biochemistry 42, 8774-8779.
35. Radominska-Pandya, A., Chen, G., Czernik, P. J., Little, J. M., Samokyszyn, V. M., Carter, C. A., and Nowak, G. (2000). Direct interaction of all-transretinoic acid with PKC. Implications for PKC signaling and cancer therapy. J. Biol. Chem. 275, 22324-22330.
36. Reusch, J. E., Colton, L. A., and Klemm, D. J. (2000). CREB activation induces adipogenesis in 3T3-L1 cells. Mol. Cell. Biol. 20, 1008-1020.
37. Scobey, M., Bertera, S., Somers, J., Watkins, S., Zeleznik, A., and Walker, W. (2001). Delivery of a cyclic adenosine 3′,5′- monophosphate response element-binding protein (creb) mutant to seminiferous tubules results in impaired spermatogenesis. Endocrinology 142, 948-954.
38. Shankar, D. B., Cheng, J. C., Kinjo, K., Federman, N., Moore, T. B., Gill, A., Rao, N. P., Landaw, E. M., and Sakamoto, K. M. (2005). The role of CREB as a proto-oncogene in hematopoiesis and in acute myeloid leukemia. Cancer Cell 7, 351-362.
39. Song, K. S., Seong, J. K., Chung, K. C., Lee, W. J., Kim, C. H., Cho, K. N., Kang, C. D., Koo, J. S., and Yoon, J. H. (2003). Induction of MUC8 gene expression by interleukin-1 beta is mediated by a sequential ERK MAPK/RSK1/CREB cascade pathway in human airway epithelial cells. J. Biol. Chem. 278, 34890-34896.
40. Stevenson, A. S., Cartin, L., Wellman, T. L., Dick, M. H., Nelson, M. T., and Lounsbury, K. M. (2001). Membrane depolarization mediates phosphorylation and nuclear translocation of CREB in vascular smooth muscle cells. Exp. Cell Res. 263, 118-130.
41. Sturgill, T. W., Ray, L. B., Erikson, E., and Maller, J. L. (1988). Insulin-stimulated MAP-2 kinase phosphorylates and activates ribosomal protein S6 kinase II. Nature 334, 715-718.
42. Sun, P., Enslen, H., Myung, P. S., and Maurer, R. A. (1994). Differential activation of CREB by Ca2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes Dev. 8, 2527-2539.
43. Sung, J. Y., Shin, S. W., Ahn, Y. S., and Chung, K. C. (2001). Basic fibroblast growth factor-induced activation of novel CREB kinase during the differentiation of immortalized hippocampal cells. J. Biol. Chem. 276, 13858-13866.
44. Tan, Y., Rouse, J., Zhang, A., Cariati, S., Cohen, P., and Comb, M. J. (1996). FGF and stress regulate CREB and ATF-1 via a pathway involving p38 MAP kinase and MAPKAP kinase-2. EMBO J. 15, 4629-4642.
45. Wang, J., and Yen, A. (2004). A novel retinoic acid-responsive element regulates retinoic acid-induced BLR1 expression. Mol. Cell. Biol. 24, 2423-2443.
46. Xing, J., Ginty, D. D., and Greenberg, M. E. (1996). Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273, 959-963.
47. Yamamoto, K. K., Gonzalez, G. A., Biggs, W. H., 3rd, and Montminy, M. R. (1988). Phosphorylarion-induced binding and transcriptional efficacy of nuclear factor CREB. Nature 334, 494-498.
48. Yen, A., Roberson, M. S., and Varvayanis, S. (1999). Retinoic acid selectively activates the ERK2 but not JNK/SAPK or p38 MAP kinases when inducing myeloid differentiation. In Vitro Cell Dev. Biol. Anim. 35, 527-532.
49. Yen, A., Roberson, M. S., Varvayanis, S., and Lee, A. T. (1998). Retinoic acid induced mitogen-activated protein (MAP)/extracellular signal-regulated kinase (ERK) kinase-dependent MAP kinase activation needed to elicit HL-60 cell differentiation and growth arrest. Cancer Res. 58, 3163-3172.
50. Zhang, B., Liu, S., Perpetua, M. D., Walker, W. H., and Harbrecht, B. G. (2004). Cytokines increase CRE binding but decrease CRE-mediated reporter activity in rat hepatocytes by increasing c-Jun. Hepatology 39, 1343-1352.