Resveratrol upregulates Egr-1 expression and activity involving extracellular signal-regulated protein kinase and ternary complex factors

Experimental Cell Research

Volumn 332, Issue 1, 2015, Pages 116-127

  Rössler, Oliver G ^a   Glatzel, Daniel ^a,b   Thiel, Gerald ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

Egr 1; Elk 1; ERK; Lentivirus; Resveratrol; Transcription

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; HYBRID PROTEIN; LENTIVIRUS VECTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; RAF PROTEIN; RESVERATROL; TERNARY COMPLEX FACTOR; DUSP1 PROTEIN, HUMAN; EGR1 PROTEIN, HUMAN; STILBENE DERIVATIVE; TRANSCRIPTION FACTOR ELK 1;

ARTICLE; CELL STIMULATION; DNA BINDING; ENZYME PHOSPHORYLATION; GENE TRANSFER; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REPORTER GENE; SERUM RESPONSIVE ELEMENT; TRANSCRIPTION INITIATION; TRANSIENT TRANSFECTION; UPREGULATION; WESTERN BLOTTING; DNA RESPONSIVE ELEMENT; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN PROCESSING;

LENTIVIRUS; VITACEAE;

BASE SEQUENCE; DUAL SPECIFICITY PHOSPHATASE 1; EARLY GROWTH RESPONSE PROTEIN 1; ETS-DOMAIN PROTEIN ELK-1; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENES, REPORTER; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN PROCESSING, POST-TRANSLATIONAL; RESPONSE ELEMENTS; STILBENES; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 84924594986     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2015.01.013     Document Type: Article

References (53)

1. Jang M., Cai L., Udeani G.O., Slowing K.V., Thomas C.F., Beecher C.W.W., Fong H.H.S., Farnsworth N.R., Kinghorn A.D., Mehta R.G., Moon R.C., Pezzuto J.M. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 1997, 275:218-220.
2. Bhat K.P.L., Kosmeder J.W., Pezzuto J.M. Biological effects of resveratrol. Antioxid. Redox Signal. 2001, 3:1041-1064.
3. Aggarwal B.B., Bhardwaj A., Aggarwal R.S., Seeram N.P., Shishodia S., Takada Y. Role of resveratrol in prevention and therapy of cancer: preclinical and clinical studies. Anticancer Res. 2004, 24:2783-2840.
4. Baur J.A., Sinclair D.A. Therapeutic potential of resveratrol: the in vivo evidence. Nat. Rev. Drug Discov. 2006, 5:493-506.
5. Borriello A., Cucciolla V., Della Ragione F., Galletti P. Dietary polyphenols, focus on resveratrol, a promising agent in the prevention of cardiovascular diseases and control of glucose homeostasis. Nutr. Metab. Cardiovasc. Dis. 2010, 20:618-625.
6. Vang O., Ahmad N., Baile C.A., Baur J.A., Brown K., Csiszar A., Das D.K., Delmas D., Gottfried C., Lin H-Y., Ma Q.-Y., Mukhopadhyay P., Nalini N., Pezzuto J.M., Richard T., Shukla Y., Surh Y.-J., Szekeres T., Szkudelski T., Walle T., Wu J.M. What is new for an old molecule? Systematic review and recommendations on the use of resveratrol. PLoS ONE 2011, 6:e19881.
7. Beher D., Wu J., Cumine S., Kim K.W., Lu S.C., Atangan L., Wang M. Resveratrol is not a direct activator of SIRT1 enzyme activity. Chem. Biol. Drug Des. 2009, 74:619-624.
8. Pacholec M., Bleasdale J.E., Chrunyk B., Cunningham D., Flynn D., Garofalo R.S., Griffith D., Griffor M., Loulakis P., Pabst B., Qiu X., Stockman B., Thanabal V., Verghese A., Ward J., Withka J., Ahn K. SRT1720, SRT2183, SRT1460, and resveratrol are not direct activators of SIRT1. J. Biol. Chem. 2010, 285:8340-8351.
9. She Q.B., Bode A.M., Ma W.Y., Chen N.Y., Dong Z. Resveratrol-induced activation of p53 and apoptosis is mediated by extracellular-signal-regulated protein kinases and p38 kinase. Cancer Res. 2001, 61:1604-1610.
10. Ragione F.D., Cucciolla V., Criniti V., Indaco S., Borriello A., Zappia V. p21Cip1gene expression is modulated by Egr1. J. Biol. Chem. 2003, 278:23360-23368.
11. Yeung F., Hoberg J.E., Ramsey C.S., Keller M.D., Jones D.R., Frye M.D., Mayo M.W. Modulation of NF-κB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 2004, 23:2369-2380.
12. Cheng A.-S., Cheng Y.-H., Chiou C.-H., Chang T.-L. Resveratrol upregulates Nrf2 expression to attenaute methylglyoxal-induced insulin resistance in Hep G2 cells. J. Agric. Food Chem. 2012, 60:9180-9187.
13. Thiel G., Rössler O.G. Resveratrol stimulates AP-1-regulated gene transcription. Mol. Nutr. Food Res. 2014, 58:1402-1413.
14. Thiel G., Cibelli G. Regulation of life and death by the zinc finger transcription factor Egr-1. J. Cell. Physiol. 2002, 193:287-292.
15. Rössler O.G., Stefano L., Bauer I., Thiel G. Stimulus-transcription coupling in the nervous system: the zinc finger protein Egr-1. Transcription Factors in the Nervous System: Development, Brain Function, and Disease 2006, 379-395. Wiley-VCH, Weinheim, Germany. G. Thiel (Ed.).
16. Thiel G., Müller I., Rössler O.G. Expression, signaling and function of Egr transcription factors in pancreatic β-cells and insulin-responsive tissues. Mol. Cell. Endocrinol. 2014, 388:10-19.
17. Al-Sarraj A., Day R.M., Thiel G Specificity of transcriptional regulation by the zinc finger transcription factors Sp1, Sp3 and Egr-1. J. Cell. Biochem. 2005, 94:153-167.
18. Lois C., Hong E.J., Pease S., Brown E.J., Baltimore D. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 2002, 295:868-872.
19. Stefano L., Al Sarraj J., Rössler O.G., Vinson C., Thiel G. Up-regulation of tyrosine hydroxylase gene transcription by tetradecanoylphorbol acetate is mediated by the transcription factors Ets-like protein-1 (Elk-1) and Egr-1. J. Neurochem. 2006, 97:92-104.
20. Bauer I I., Sarraj J.Al, Vinson C., Larsen R., Thiel G. Interleukin 1β and tetrade-canoylphorbol acetate-induced biosynthesis of tumor necrosis factor α in human hepatoma cells involves the transcription factors ATF2 and c-Jun and stress-activated protein kinases. J. Cell. Biochem. 2007, 100:242-255.
21. Mayer S.I., Rössler O.G., Endo T., Charnay P., Thiel G. Epidermal growth factor-induced proliferation of astrocytes requires Egr transcription factors. J. Cell. Sci. 2009, 122:3340-3350.
22. Mayer S.I., Thiel G. Calcium influx into MIN6 insulinoma cells induces expression of Egr-1 involving extracellular signal-regulated protein kinase and the transcription factors Elk-1 and CREB. Eur. J. Cell Biol. 2009, 88:19-33.
23. Thiel G., Rössler O.G. Immediate-early transcriptional response to angiotensin II in human adrenocortical cells. Endocrinology 2011, 152:4211-4223.
24. Ekici M., Keim A., Rössler O.G., Hohl M., Thiel G. Chromatin structure and expression of the AMPA receptor subunit GluR2 in human glioma cells: major role of REST and Sp1. J. Cell. Biochem. 2012, 113:528-543.
25. Keim A., Müller I., Thiel G. Efficient genetic manipulation of 1321N1 astrocytoma cells using lentiviral gene transfer. J. Neurosci. Methods 2012, 206:138-142.
26. Rössler O.G., Henß I I., Thiel G. Transcriptional response to muscarinic acetylcholine receptor stimulation, regulation of Egr-1 biosynthesis by ERK, Elk-1, MKP-1, and calcineurin in carbachol-stimulated human neuroblastoma cells. Arch. Biochem. Biophys. 2008, 470:93-102.
27. 2+ concentration, phosphorylation of ERK and activation of ternary complex factor. BMC Mol. Biol. 2009, 10:40.
28. Müller I., Endo T., Thiel G. Regulation of AP-1 activity in glucose-stimulated insulinoma cells. J. Cell. Biochem. 2010, 110:1481-1494.
29. Thiel G., Kaufmann K., Magin A., Lietz M., Bach K., Cramer M. The human transcriptional repressor protein NAB1, expression and biological activity. Biochim. Biophys. Acta 2000, 1493:289-301.
30. Kaufmann K., Thiel G. Epidermal growth factor and thrombin induced proliferation of immortalized human keratinocytes is coupled to the synthesis of Egr-1, a zinc finger transcriptional regulator. J. Cell. Biochem. 2002, 85:381-391.
31. 2+ ions and c-Jun N-terminal protein kinase. Mol. Pharmacol. 2010, 78:865-876.
32. Mayer S.I., Müller I., Mannebach S., Endo T., Thiel G. Signal transduction of pregnenolone sulfate in insulinoma cells. J. Biol. Chem. 2011, 286:10084-10096.
33. Russo M.W., Sevetson B.R., Milbrandt J. Identification of NAB1, a repressor of NGFI-A and Krox20-mediated transcripton. Proc. Natl. Acad. Sci. USA 1995, 92:6873-6877.
34. Svaren J., Sevetson B.R., Apel E.D., Zimonjic D.B., Popescu N.C., Milbrandt J. NAB2, a corepressor of NGFI-A (Egr-1) and Krox20, is induced by proliferative and differentiative stimuli. Mol. Cell. Biol. 1996, 16:3545-3553.
35. McMahon M. Steroid receptor fusion proteins for conditional activation of Raf-MEK-ERK signaling pathway. Methods Enzymol. 2001, 332:401-417.
36. Thiel G., Ekici M., Rössler O.G. Regulation of cellular proliferation, differentiation and cell death by activated Raf. Cell Commun. Signal. 2009, 7:8.
37. Yokoyama T., Takano K., Yoshida A., Katada F., Sun P., Takenawa T., Andoh T., Endo T. DA-Raf1, a competent intrinsic dominant-negative antagonist of the Ras-ERK pathway, is required for myogenic differentiation. J. Cell Biol. 2007, 177:781-793.
38. Kaufmann A., Keim A., Thiel G. Regulation of immediate-early gene transcription following activation of Gαq-coupled designer receptors. J. Cell. Biochem. 2013, 114:681-696.
39. Li Q.-J., Vaingankar S., Green H.M., Martins-Green M. Activation of the 9E3/cCAF chemokine by phorbol esters occur via multiple signal transduction pathways that converge to MEK1/ERK2 and activate Elk1 transcription factor. J. Biol. Chem. 1999, 274:15454-15465.
40. Cesari F., Brecht S., Vintersten K., Vuong L.G., Hofmann M., Klingel K., Schnorr J.-J., Arsenian S., Schild H., Herdegen T., Wiebel F.F., Nordheim A. Mice deficient for the Ets transcription factor Elk-1 show normal immune responses and mildly impaired neuronal gene activation. Mol. Cell. Biol. 2004, 24:294-305.
41. Bickenbach K.A., Veerapong J., Shao M.Y., Mauceri J.J., Posner M.C., Wechselbaum R.R. Resveratrol is an effective inducer of CArG-driven TNF-alpha gene therapy. Cancer Gene Ther. 2008, 15:133-139.
42. Whitlock N.C., Bahn J.H., Lee S.-H., Eling T.E., Baek S.J. Resveratrol-induced apoptosis is mediated by early growth response-1, Krüppel-like factor 4, and activating transcription factor 3. Cancer Prev. Res. 2011, 4:116-127.
43. Utreras E., Terse A., Keller A., Iadarola M.J., Kulkarni A.B. Resveratrol inhibits Cdk5 activity through regulation of p35 expression. Mol. Pain 2011, 7:49.
44. Maher P., Dargusch R., Bodai L., Gerard P.E., Purcell J.M., Marsh J.L. ERK activation by the polyphenols fisetin and resveratrol provides neuroprotection in multiple models of HuntingtonDs disease. Hum. Mol. Genet. 2011, 20:261-270.
45. King R.E., Kent K.D., Bomser J.A. Resveratrol reduces oxidation and proliferation of human retinal pigment epithelial cells via extracellular signal-regulated kinase inhibition. Chem. Biol. Interact. 2005, 151:143-149.
46. Rössler O.G., Thiel G. Brain-derived neurotrophic factor, epidermal growth factor, or A-Raf induced growth of HaCaT keratinocytes requires extracellular signal-regulated kinase. Am. J. Physiol. Cell Physiol. 2004, 286:C1118-C1129.
47. Treisman R. Journey to the surface of the cell: Fos regulation and the SRE. EMBO J. 1995, 14:4905-4913.
48. S.I. Mayer, V. Deixheimer, E. Nishida, S. Kitajima, G. Thiel, Expression of the transcriptional repressor ATF3 in gonadotrophs is regulated by Egr-1, CREB, and ATF2 after gonadotropin-releasing hormone receptor stimulation, Endocrinology 149 (2008) 6311-6325.
49. Thiel G., Lesch A., Keim A. Transcriptional response to calcium-sensing receptor stimulation. Endocrinology 2012, 153:4716-4728.
50. Kaufmann A., Rössler O.G., Thiel G. Expression of the transcription factor Egr-1 in pancreatic acinar cells following stimulation of cholecystokinin or Gαq-coupled designer receptors. Cell. Physiol. Biochem. 2014, 33:1411-1425.
51. Boros J., Donaldson I.J., ODDonnell A., Odrowaz Z.A., Zeef L., Lupien M., Meyer C.A., Liu X.S., Brown M., Sharrocks A.D. Elucidation of the ELK1 target gene network reveals a role in the coordinate regulation of core components of the gene regulation machinery. Genome Res. 2009, 19:1963-1973.
52. Yan S.F, Fujita T., Lu K., Okada K., Zou Y.S., Mackman N., Pinsky D.J., Stern D.M. Egr-1, a master switch coordinating upregulation of divergent gene families underlying ischemic stress. Nat. Med. 2000, 6:1355-1361.
53. Virolle T., Krones-Herzig A., Baron V., De Gregorio G., Adamson E.D., Mercola D. Egr promotes growth and survival of prostate cancer cells. J. Biol. Chem. 2003, 278:11802-11810.