A JNK-independent signaling pathway regulates TNFα-stimulated, c-jun-driven FRA-1 protooncogene transcription in pulmonary epithelial cells

Journal of Immunology

Volumn 177, Issue 10, 2006, Pages 7193-7202

  Adiseshaiah, Pavan ^a   Kalvakolanu, Dhananjaya V ^b   Reddy, Sekhar P ^a  

^a The Johns Hopkins University   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN C JUN; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ENZYME ACTIVITY; EPITHELIUM CELL; FRA 1 GENE; GENE EXPRESSION; GENE INDUCTION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; LUNG ALVEOLUS EPITHELIUM; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; PROTO ONCOGENE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

EID: 33750839530     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.10.7193     Document Type: Article

References (63)

1. Bals, R., and P. S. Hiemstra. 2004. Innate immunity in the lung: how epithelial cells fight against respiratory pathogens. Eur. Respir. J. 23: 327-333.
2. Sheppard, D. 2003. Functions of pulmonary epithelial integrins: from development to disease. Physiol. Rev. 83: 673-686.
3. Baud, V., and M. Karin. 2001. Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol. 11: 372-377.
4. Erzurum, S. C. 2006. Inhibition of tumor necrosis factor α for refractory asthma. N. Engl. J. Med. 354: 754-758.
5. Aggarwal, B. B. 2003. Signalling pathways of the TNF superfamily. a double-edged sword. Nat. Rev. Immunol. 3: 745-756.
6. Foletta, V. C., D. H. Segal, and D. R. Cohen. 1998. Transcriptional regulation in the immune system: all roads lead to AP-1. J. Leukocyte Biol. 63: 139-152.
7. Karin, M., and E. Shaulian. 2001. AP-1: linking hydrogen peroxide and oxidative stress to the control of cell proliferation and death. IUBMB Life 52: 17-24.
8. Reddy, S. P., and B. T. Mossman. 2002. Role and regulation of activator protein-1 in toxicant-induced responses of the lung. Am. J. Physiol 283: L1161-L1178.
9. Eferl, R., and E. F. Wagner. 2003. AP-1: a double-edged sword in tumorigenesis. Nat. Rev. Cancer. 3: 859-868.
10. Karin, M., Z. Liu, and E. Zandi. 1997. AP-1 function and regulation. Curr. Opin. Cell Biol. 9: 240-246.
11. Li, B., C. Tournier, R. J. Davis, and R. A. Flavell. 1999. Regulation of IL-4 expression by the transcription factor JunB during T helper cell differentiation. EMBO J. 18: 420-432.
12. Zenz, R., and E. F. Wagner. 2006. Jun signalling in the epidermis: From developmental defects to psoriasis and skin tumors. Int. J. Biochem. Cell Biol. 38: 1043-1049.
13. Meixner, A., F. Karreth, L. Kenner, and E. F. Wagner. 2004. JunD regulates lymphocyte proliferation and T helper cell cytokine expression. EMBO J. 23: 1325-1335.
14. Matsui, M., M. Tokuhara, Y. Konuma, N. Nomura, and R. Ishizaki. 1990. Isolation of human fos-related genes and their expression during monocyte-macrophage differentiation. Oncogene 5: 249-255.
15. Tsuchiya, H., M. Fujii, T. Niki, M. Tokuhara, M. Matsui, and M. Seiki. 1993. Human T cell leukemia virus type 1 Tax activates transcription of the human fra-1 gene through multiple cis elements responsive to transmembrane signals. J. Virol 67: 7001-7007.
16. Zhang, Q., P. Adiseshaiah, and S. P. Reddy. 2005. Matrix metalloproteinase/epidermal growth factor receptor/mitogen-activated protein kinase signaling regulate fra-1 induction by cigarette smoke in lung epithelial cells. Am. J. Respir. Cell Mol Biol. 32:72-81.
17. Janssen, Y. M., N. H. Heintz, J. P. Marsh, P. J. Borm, and B. T. Mossman. 1994. Induction of c-fos and c-jun proto-oncogenes in target cells of the lung and pleura by carcinogenic fibers. Am. J. Respir. Cell Mol. Biol. 11: 522-530.
18. Zhang, Q., S. R. Kleeberger, and S. P. Reddy. 2003. DEP-induced fra-1 expression correlates with a distinct activation of AP1-dependent gene transcription in alveolar epithelial cells. Am. J. Physiol. 286: L427-L436.
19. Wu, L., A. Tanimoto, Y. Murata, J. Fan, Y. Sasaguri, and T. Watanabe. 2001. Induction of human matrix metalloproteinase-12 gene transcriptional activity by GM-CSF requires the AP-1 binding site in human U937 monocytic cells. Biochem. Biophys. Res. Commun. 285: 300-307.
20. Kanai, K., K. Asano, T. Hisamitsu, and H. Suzaki. 2004. Suppression of matrix metalloproteinase-9 production from neutrophils by a macrolide antibiotic, roxithromycin, in vitro. Mediat. Inflamm. 13: 313-319.
21. Hong, S., K. K. Park, J. Magae, K. Ando, T. S. Lee, T. K. Kwon, J. Y. Kwak, C. H. Kim, and Y. C. Chang. 2005. Ascochlorin inhibits matrix metalloproteinase-9 expression by suppressing activator protein-1-mediated gene expression through the ERK1/2 signaling pathway: inhibitory effects of ascochlorin on the invasion of renal carcinoma cells. J. Biol. Chem. 280: 25202-25209.
22. Belguise, K., N. Kersual, F. Galtier, and D. Chalbos. 2005. FRA-1 expression level regulates proliferation and invasiveness of breast cancer cells. Oncogene 24: 1434-1444.
23. West, K. A., J. Brognard, A. S. Clark, I. R. Linnoila, X. Yang, S. M. Swain, C. Harris, S. Belinsky, and P. A. Dennis. 2003. Rapid Akt activation by nicotine and a tobacco carcinogen modulates the phenotype of normal human airway epithelial cells. J. Clin. Invest. 111: 81-90.
24. West, K. A., I. R. Linnoila, S. A. Belinsky, C. C. Harris, and P. A. Dennis. 2004. Tobacco carcinogen-induced cellular transformation increases activation of the phosphatidylinositol 3′-kinase/Akt pathway in vitro and in vivo. Cancer Res. 64: 446-451.
25. Fiala, E. S., O. S. Sohn, C. X. Wang, E. Seibert, J. Tsurutani, P. A. Dennis, K. El-Bayoumy, R. S. Sodum, D. Desai, J. Reinhardt, and C. Aliaga. 2005. Induction of preneoplastic lung lesions in guinea pigs by cigarette smoke inhalation and their exacerbation by high dietary levels of vitamins C and E. Carcinogenesis 26: 605-612.
26. Adiseshaiah, P., S. R. Papaiahgari, H. Vuong, D. V. Kalvakolanu, and S. P. Reddy. 2003. Multiple cis-elements mediate the transcriptional activation of human fra-1 by 12-O-tetradecanoylphorbol-13-acetate in bronchial epithelial cells. J. Biol. Chem. 278: 47423-47433.
27. Wei, W., J. Jin, S. Schlisio, J. W. Harper, and W. G. Kaelin, Jr. 2005. The v-Jun point mutation allows c-Jun to escape GSK3-dependent recognition and destruction by the Fbw7 ubiquitin Hgase. Cancer Cell 8: 25-33.
28. Reddy, S. P., P. Adiseshaiah, P. Shapiro, and H. Vuong. 2002. BMK1 (ERK5) regulates squamous differentiation marker SPRR1B transcription in Clara-like H441 cells. Am. J. Respir. Cell Mol. Biol. 27: 64-70.
29. Pages, G., S. Guerin, D. Grall, F. Bonino, A. Smith, F. Anjuere, P. Auberger, and J. Pouyssegur. 1999. Defective thymocyte maturation in p44 MAP kinase (Erk 1) knockout mice. Science 286: 1374-1377.
30. Roy, S. K., J. Hu, Q. Meng, Y. Xia, P. S. Shapiro, S. P. Reddy, L. C. Platanias, D. J. Lindner, P. F. Johnson, C. Pritchard, et al. 2002. MEKK1 plays a critical role in activating the transcription factor C/EBP-β-dependent gene expression in response to IFN-γ. Proc. Natl Acad. Sci. USA 99: 7945-7950.
31. Patterson, T., H. Vuong, Y.-S. Liaw, R. Wu, D. V. Kalvakolanu, and S. P. Reddy. 2001. Mechanism of repression of squamous differentiation marker, SPRR1B, in malignant bronchial epithelial cells: role of critical TRE-sites and its transacting factors. Oncogene 20: 634-644.
32. Adiseshaiah, P., S. Peddakama, Q. Zhang, D. V. Kalvakolanu, and S. P. Reddy. 2005. Mitogen regulated induction of FRA-1 proto-oncogene is controlled by the transcription factors binding to both serum and TPA response elements. Oncogene 24: 4193-4120.
33. Treisman, R. 1995. Journey to the surface of the cell: Fos regulation and the SRE. EMBO J. 14: 4905-4913.
34. 2-terminal kinase is essential for the regulation of AP-1 by tumor necrosis factor. Mol. Cell. Biol. 23: 2871-2882.
35. Catani, M. V., A. Rossi, A. Costanzo, S. Sabatini, M. Levrero, G. Melino, and L. Avigliano. 2001. Induction of gene expression via activator protein-1 in the ascorbate protection against UV-induced damage. Biochem. J. 356: 77-85.
36. Shaulian, E., and M. Karin. 2001. AP-1 in cell proliferation and survival. Oncogene 20: 2390-2400.
37. Mechta-Grigoriou, F., D. Gerald, and M. Yaniv. 2001. The mammalian Jun proteins: redundancy and specificity. Oncogene 20: 2378-2389.
38. Whitmarsh, A. J., and R. J. Davis. 1996. Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J. Mol. Med. 74: 589-607.
39. 1 phosphorylation by the ERK MAPK pathway is required for epidermal growth factor-induced c-jun expression. J. Biol. Chem. 277: 50550-50556.
40. Han, T. H., and R. Prywes. 1995. Regulatory role of MEF2D in serum induction of the c-jun promoter. Mol. Cell. Biol. 15: 2907-2915.
41. Kayahara, M., X. Wang, and C. Tournier. 2005. Selective regulation of c-jun gene expression by mitogen-activated protein kinases via the 12-o-tetradecanoylphorbol-13-acetate-responsive element and myocyte enhancer factor 2 binding sites. Mol. Cell. Biol 25: 3784-3792.
42. Karin, M. 1995. The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem. 270: 16483-16486.
43. Musti, A. M., M. Treier, and D. Bohmann. 1997. Reduced ubiquitin-dependent degradation of c-Jun after phosphorylation by MAP kinases. Science 275: 400-402.
44. Hilberg, F., A. Aguzzi, N. Howells, and E. F. Wagner. 1993. c-jun is essential for normal mouse development and hepatogenesis. Nature 365: 179-181.
45. Behrens, A., M. Sibilia, and E. F. Wagner. 1999. Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat. Genet. 21: 326-329.
46. Wisdom, R., R. S. Johnson, and C. Moore. 1999. c-Jun regulates cell cycle progression and apoptosis by distinct mechanisms. EMBO J. 18: 188-197.
47. Johnson, R., B. Spiegelman, D. Hanahan, and R. Wisdom. 1996. Cellular transformation and malignancy induced by ras require c-jun. Mol. Cell. Biol. 16: 4504-4511.
48. Kennedy, N. J., H. K. Sluss, S. N. Jones, D. Bar-Sagi, R. A. Flavell, and R. J. Davis. 2003. Suppression of Ras-stimulated transformation by the JNK signal transduction pathway. Genes Dev. 17: 629-637.
49. 63/73 are required for CBP induced stimulation in vivo and CBP binding in vitro. Oncogene 11: 2509-2514.
50. Westermarck, J., C. Weiss, R. Saffrich, J. Kast, A. M. Musti, M. Wessely, W. Ansorge, B. Seraphin, M. Wilm, B. C. Valdez, and D. Bohmann. 2002. The DEXD/H-box RNA helicase RHII/Gu is a cofactor for c-Jun-activated transcription. EMBO J. 21:451-460.
51. Weiss, C., S. Schneider, E. F. Wagner, X. Zhang, E. Seto, and D. Bohmann. 2003. JNK phosphorylation relieves HDAC3-dependent suppression of the transcriptional activity of c-Jun. EMBO J. 22: 3686-3695.
52. Nateri, A. S., B. Spencer-Dene, and A. Behrens. 2005. Interaction of phosphorylated c-Jun with TCF4 regulates intestinal cancer development. Nature 437: 281-285.
53. Davis, R. J. 2000. Signal transduction by the JNK group of MAP kinases. Cell 103: 239-252.
54. Zhang, Q., P. Adiseshaiah, D. V. Kalvakolanu, and S. P. Reddy. 2006. A phosphatidylinositol 3-kinase regulated Akt independent signaling promotes cigarette smoke induced FRA-1 expression. J. Biol. Chem. 281: 10174-10181.
55. Herrera, R. E., P. E. Shaw, and A. Nordheim. 1989. Occupation of the c-fos serum response element in vivo by a multi-protein complex is unaltered by growth factor induction. Nature 340: 68-70.
56. Tornaletti, S., and G. P. Pfeifer. 1995. UV light as a footprinting agent: modulation of UV-induced DNA damage by transcription factors bound at the promoters of three human genes. J. Mol. Biol. 249: 714-728.
57. Kolch, W. 2000. Meaningful relationships: the regulation of the Ras/Raf/MEK/ERK pathway by protein interactions. Biochem. J. 351: 289-305.
58. Janknecht, R., and A. Nordheim. 1996. MAP kinase-dependent transcriptional coactivation by Elk-1 and its cofactor CBP. Biochem. Blophys. Res. Commun. 228: 831-837.
59. Li, Q. J., S. H. Yang, Y. Maeda, F. M. Sladek, A. D. Sharrocks, and M. Martins-Green. 2003. MAP kinase phosphorylation-dependent activation of Elk-1 leads to activation of the coactivator p300. EMBO J. 22: 281-291.
60. Mayr, B., and M. Montminy. 2001. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2: 599-609.
61. Brusselbach, S., U. Mohle-Steinlein, Z. Q. Wang, M. Schreiber, F. C. Lucibello, R. Muller, and E. F. Wagner. 1995. Cell proliferation and cell cycle progression are not impaired in fibroblasts and ES cells lacking c-Fos. Oncogene 10: 79-86.
62. Schreiber, M., C. Poirier, A. Franchi, R. Kurzbauer, J. L. Guenet, G. F. Carie, and E. F. Wagner. 1997. Structure and chromosomal assignment of the mouse fra-1 gene, and its exclusion as a candidate gene for oc (osteosclerosis). Oncogene 15: 1171-1178.
63. Hoffmann, E., A. Thiefes, D. Buhrow, O. Dittrich-Breiholz, H. Schneider, K. Resch, and M. Kracht. 2005. MEK1-dependent delayed expression of Fos-related antigen-1 counteracts c-Fos and p65 NF-κB-mediated interleukin-8 transcription in response to cytokines or growth factors. J. Biol. Chem. 280: 9706-9718.