Home LiteratureArticle Details
PMID: 8601609 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

UV activates growth factor receptors via reactive oxygen intermediates.

The Journal of cell biology ·Vol. 133 ·No. 1 ·1996-04-00 ·Pages 211-20

Huang RP, Wu JX, Fan Y, Adamson ED

Abstract

Exposure of mammalian cells to UV irradiation induces rapid and transient expression of early growth response-1 gene (Egr-1) encoding a transcription factor that plays a role in cell survival. These signals from the irradiated cell surface are likely to involve more than one pathway, and we show here that an essential pathway involves activation of several growth factor receptors by reactive oxygen intermediates (ROI). UVC irradiation causes the tyrosine phosphorylation of EGF receptor (EGFR) in mouse NIH 3T3 fibroblasts and HC11 mouse mammary cells. EGFR activation by irradiation of cells is abrogated by suramin, by antioxidants, and by the presence of a dominant negative EGFR. UV induces the formation of complexes between activated EGFR and SOS, Grb2, PLC gamma, and SHC that can be precipitated with antibodies to EGFR. The activation of EGFR by UV is mimicked by H2O2, suggesting that ROI may function upstream of EGFR activation. Our observations support the hypothesis that ROI and growth factor receptors operate in the early steps of the UV signal that lead to the enhanced expression and activity of Egr-1.

MeSH Terms
3T3 Cells Animals Antioxidants/pharmacology Base Sequence Cells, Cultured Culture Media, Conditioned/pharmacology DNA-Binding Proteins/biosynthesis,genetics Down-Regulation Early Growth Response Protein 1 Epithelium ErbB Receptors/analysis,physiology Gene Expression Regulation/radiation effects Growth Substances/pharmacology Immediate-Early Proteins Mice Molecular Sequence Data Phosphorylation Proline/analogs & derivatives,pharmacology Proteins/analysis Reactive Oxygen Species Receptors, Growth Factor/physiology Signal Transduction/radiation effects Suramin/pharmacology Thiocarbamates/pharmacology Transcription Factors/biosynthesis,genetics Tyrosine/metabolism Ultraviolet Rays
Chemicals
Antioxidants Culture Media, Conditioned DNA-Binding Proteins Early Growth Response Protein 1 Egr1 protein, mouse Growth Substances Immediate-Early Proteins Proteins Reactive Oxygen Species Receptors, Growth Factor Thiocarbamates Transcription Factors prolinedithiocarbamate Tyrosine Suramin Proline ErbB Receptors
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Huang R P
La Jolla Cancer Research Foundation, California 92037, USA.
Wu J X
Fan Y
Adamson E D
References (62)
62 references, click to expand
  1. Distinct effects of thioredoxin and antioxidants on the activation of transcription factors NF-kappa B and AP-1.
    Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1672-6 PMID: 8127864
  2. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain.
    Cell. 1994 Mar 25;76(6):1025-37 PMID: 8137421
  3. Suppression of v-sis-dependent transformation by the transcription factor, Egr-1.
    Oncogene. 1994 May;9(5):1367-77 PMID: 8152797
  4. The UV response involving the Ras signaling pathway and AP-1 transcription factors is conserved between yeast and mammals.
    Cell. 1994 May 6;77(3):381-90 PMID: 8181058
  5. The phosphorylated forms of the transcription factor, Egr-1, bind to DNA more efficiently than non-phosphorylated.
    Biochem Biophys Res Commun. 1994 May 16;200(3):1271-6 PMID: 8185575
  6. Heterogeneity in the HeLa cell cycle response to UVC analyzed by the BrdUrd two-parameter method.
    Exp Cell Res. 1994 Jun;212(2):176-89 PMID: 8187814
  7. Enucleation of mammalian cells by cytochalasin B. I. Characterization of anucleate cells.
    Exp Cell Res. 1972 Aug;73(2):273-86 PMID: 4626574
  8. The insulin-like effect of hydrogen peroxide on pathways of lipid synthesis in rat adipocytes.
    J Biol Chem. 1979 Sep 25;254(18):9017-21 PMID: 479177
  9. Activation of pyruvate dehydrogenase in rat adipocytes by concanavalin A: evidence for insulin-like effect mediated by hydrogen peroxide.
    Biochem Biophys Res Commun. 1980 Mar 13;93(1):36-41 PMID: 6990929
  10. Stimulation of glucose transport and oxidation in adipocytes by fatty acids: evidence for a regulatory role in the cellular response to insulin.
    Biochem Biophys Res Commun. 1980 May 30;94(2):682-9 PMID: 6994726
  11. Dimethyl sulfoxide prevents DNA nicking mediated by ionizing radiation or iron/hydrogen peroxide-generated hydroxyl radical.
    Proc Natl Acad Sci U S A. 1981 Feb;78(2):1001-3 PMID: 6940118
  12. Epithelial mouse mammary cell line exhibiting normal morphogenesis in vivo and functional differentiation in vitro.
    Proc Natl Acad Sci U S A. 1984 Jun;81(12):3756-60 PMID: 6587390
  13. The mammalian UV response: mechanism of DNA damage induced gene expression.
    Adv Enzyme Regul. 1994;34:381-95 PMID: 7942283
  14. Ultraviolet radiation and immunology: something new under the sun--presidential address.
    Cancer Res. 1994 Dec 1;54(23):6102-5 PMID: 7954455
  15. The binding of immobilized IgG2a to Fc gamma 2a receptor activates NF-kappa B via reactive oxygen intermediates and tumor necrosis factor-alpha 1.
    J Biol Chem. 1994 Dec 2;269(48):30561-8 PMID: 7982975
  16. Activation of the mitogen-activated protein kinase signaling pathway in neutrophils. Role of oxidants.
    J Biol Chem. 1994 Dec 9;269(49):31234-42 PMID: 7983067
  17. Identification of amino acids in the N-terminal SH2 domain of phospholipase C gamma 1 important in the interaction with epidermal growth factor receptor.
    Biochemistry. 1994 Dec 13;33(49):14671-8 PMID: 7993895
  18. A biological role for Egr-1 in cell survival following ultra-violet irradiation.
    Oncogene. 1995 Feb 2;10(3):467-75 PMID: 7845671
  19. V-sis induces Egr-1 expression by a pathway mediated by c-Ha-Ras.
    J Cell Biochem. 1994 Dec;56(4):469-79 PMID: 7890805
  20. Involvement of reactive oxygen species in cytokine and growth factor induction of c-fos expression in chondrocytes.
    J Biol Chem. 1995 May 19;270(20):11727-30 PMID: 7744816
  21. Neu differentiation factor/heregulin modulates growth and differentiation of HC11 mammary epithelial cells.
    Mol Endocrinol. 1995 Jan;9(1):14-23 PMID: 7760847
  22. A UV-responsive G2 checkpoint in rodent cells.
    Mol Cell Biol. 1995 Jul;15(7):3722-30 PMID: 7791779
  23. Gene-specific and strand-specific DNA repair in the G1 and G2 phases of the cell cycle.
    Mol Cell Biol. 1995 Jul;15(7):3731-7 PMID: 7791780
  24. Rapid responses to oxidative stress mediated by iron regulatory protein.
    EMBO J. 1995 Jun 15;14(12):2917-24 PMID: 7796817
  25. UV activation of receptor tyrosine kinase activity.
    Oncogene. 1995 Aug 3;11(3):561-9 PMID: 7543196
  26. Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity.
    Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8115-9 PMID: 7667254
  27. Egr-1 negatively regulates human tumor cell growth via the DNA-binding domain.
    Cancer Res. 1995 Nov 1;55(21):5054-62 PMID: 7585551
  28. Efficient reversion of simian sarcoma virus-transformation and inhibition of growth factor-induced mitogenesis by suramin.
    Proc Natl Acad Sci U S A. 1986 Sep;83(17):6440-4 PMID: 3018732
  29. Preparation and properties of monoclonal and polyclonal antibodies to mouse epidermal growth factor (EGF) receptors: evidence for cryptic EGF receptors in embryonal carcinoma cells.
    Development. 1987 Jun;100(2):351-63 PMID: 3308402
  30. A zinc finger-encoding gene coregulated with c-fos during growth and differentiation, and after cellular depolarization.
    Cell. 1988 Apr 8;53(1):37-43 PMID: 3127059
  31. Two mouse genes encoding potential transcription factors with identical DNA-binding domains are activated by growth factors in cultured cells.
    Proc Natl Acad Sci U S A. 1988 Jul;85(13):4691-5 PMID: 3133658
  32. Prolactin regulation of beta-casein gene expression and of a cytosolic 120-kd protein in a cloned mouse mammary epithelial cell line.
    EMBO J. 1988 Jul;7(7):2089-95 PMID: 3416834
  33. UV-induced DNA damage is an intermediate step in UV-induced expression of human immunodeficiency virus type 1, collagenase, c-fos, and metallothionein.
    Mol Cell Biol. 1989 Nov;9(11):5169-81 PMID: 2557547
  34. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1.
    EMBO J. 1991 Aug;10(8):2247-58 PMID: 2065663
  35. In-vivo studies of the action spectrum and time course for release of transforming growth factor-alpha by ultraviolet irradiation in man.
    Br J Dermatol. 1991 Dec;125(6):566-8 PMID: 1760361
  36. UVC modulation of epidermal growth factor receptor number in HeLa S3 cells.
    Carcinogenesis. 1992 Feb;13(2):183-7 PMID: 1740007
  37. DNA damage-induced gene expression: signal transduction and relation to growth factor signaling.
    Rev Physiol Biochem Pharmacol. 1992;119:187-223 PMID: 1604153
  38. UV induction of transforming growth factor alpha in melanoma cell lines is a posttranslational event.
    J Cell Physiol. 1992 Aug;152(2):328-36 PMID: 1639867
  39. Nature of the interaction of growth factors with suramin.
    Biochemistry. 1992 Sep 22;31(37):9016-24 PMID: 1390688
  40. Ionizing radiation activates transcription of the EGR1 gene via CArG elements.
    Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10149-53 PMID: 1332031
  41. The mammalian ultraviolet response is triggered by activation of Src tyrosine kinases.
    Cell. 1992 Dec 24;71(7):1081-91 PMID: 1473146
  42. Nuclear factor kappa B: an oxidative stress-responsive transcription factor of eukaryotic cells (a review).
    Free Radic Res Commun. 1992;17(4):221-37 PMID: 1473734
  43. Genotoxic-stress-response genes and growth-arrest genes. gadd, MyD, and other genes induced by treatments eliciting growth arrest.
    Ann N Y Acad Sci. 1992 Nov 21;663:139-53 PMID: 1482047
  44. Low fluences of ultraviolet irradiation stimulate HeLa cell surface aminopeptidase and candidate "TGF alpha ase" activity.
    J Cell Biochem. 1993 Jan;51(1):102-15 PMID: 8432738
  45. UV irradiation-induced interleukin-1 and basic fibroblast growth factor synthesis and release mediate part of the UV response.
    J Biol Chem. 1993 Mar 25;268(9):6734-41 PMID: 8454646
  46. UV-induced activation of AP-1 involves obligatory extranuclear steps including Raf-1 kinase.
    EMBO J. 1993 Mar;12(3):1005-12 PMID: 8384549
  47. Induction of cellular p53 activity by DNA-damaging agents and growth arrest.
    Mol Cell Biol. 1993 Jul;13(7):4242-50 PMID: 8321226
  48. Inhibition of differentiation in P19 embryonal carcinoma cells by the expression of vectors encoding truncated or antisense EGF receptor.
    Dev Biol. 1993 Sep;159(1):208-22 PMID: 8365561
  49. Long-wavelength UVA radiation induces oxidative stress, cytoskeletal damage and hemolysis.
    Photochem Photobiol. 1993 Jun;57(6):1018-26 PMID: 8367531
  50. NF-kappa B activation by ultraviolet light not dependent on a nuclear signal.
    Science. 1993 Sep 10;261(5127):1442-5 PMID: 8367725
  51. Hydrogen peroxide stimulates transcription of c-jun in vascular smooth muscle cells: role of arachidonic acid.
    Oncogene. 1993 Oct;8(10):2759-64 PMID: 8378085
  52. Bcl-2 functions in an antioxidant pathway to prevent apoptosis.
    Cell. 1993 Oct 22;75(2):241-51 PMID: 7503812
  53. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain.
    Genes Dev. 1993 Nov;7(11):2135-48 PMID: 8224842
  54. X-irradiation, phorbol esters, and H2O2 stimulate mitogen-activated protein kinase activity in NIH-3T3 cells through the formation of reactive oxygen intermediates.
    Cancer Res. 1994 Jan 1;54(1):12-5 PMID: 8261431
  55. Damage to DNA by UV light and activation of transcription factors.
    Biochem Pharmacol. 1994 Jan 13;47(1):129-36 PMID: 8311837
  56. Photodynamic therapy mediated induction of early response genes.
    Cancer Res. 1994 Mar 1;54(5):1374-80 PMID: 8118827
  57. Hierarchy of binding sites for Grb2 and Shc on the epidermal growth factor receptor.
    Mol Cell Biol. 1994 Aug;14(8):5192-201 PMID: 7518560
  58. ZAP-70 tyrosine kinase, CD45, and T cell receptor involvement in UV- and H2O2-induced T cell signal transduction.
    J Biol Chem. 1994 Aug 12;269(32):20718-26 PMID: 8051172
  59. Production of hydrogen peroxide by transforming growth factor-beta 1 and its involvement in induction of egr-1 in mouse osteoblastic cells.
    J Cell Biol. 1994 Aug;126(4):1079-88 PMID: 8051207
  60. Involvement of growth factor receptors in the mammalian UVC response.
    Cell. 1994 Sep 23;78(6):963-72 PMID: 7923365
  61. Nitric oxide reduces early growth response-1 gene expression in rat lung macrophages treated with interferon-gamma and lipopolysaccharide.
    J Biol Chem. 1994 Oct 14;269(41):25239-42 PMID: 7523382
  62. Induction of nuclear factor kappa B after low-dose ionizing radiation involves a reactive oxygen intermediate signaling pathway.
    Radiat Res. 1994 Oct;140(1):97-104 PMID: 7938461
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.133.1.211
Published
1996-04-00
Pages
211-20
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2120786
Subset
IM
Grants
NCI NIH HHS · CA 28427 · United States
NCI NIH HHS · CA 67888 · United States
External Links
PubMed source DOI: 10.1083/jcb.133.1.211 PMC Full Text View journal details
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