A self-enabling TGFβ response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells

Molecular Cell

Volumn 11, Issue 4, 2003, Pages 915-926

  Kang, Yibin ^a   Chen, Chang Rung ^a   Massagué, Joan ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; PROTEIN; SMAD3 PROTEIN; SYNAPTOPHYSIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DNA BINDING PROTEIN; ID1 PROTEIN, HUMAN; INHIBITOR OF DIFFERENTIATION 1; REPRESSOR PROTEIN; SMAD PROTEIN; SMAD3 PROTEIN, HUMAN; SMAD4 PROTEIN; SMAD4 PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; EPITHELIUM CELL; GENE FUNCTION; HUMAN; HUMAN CELL; NONHUMAN; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STRESS; TRANSCRIPTION REGULATION; ANIMAL; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE; REGULATOR GENE;

ANIMALIA;

ACTIVATING TRANSCRIPTION FACTOR 3; ANIMALS; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DNA-BINDING PROTEINS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; GENES, REGULATOR; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 1; PROMOTER REGIONS (GENETICS); PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SMAD PROTEINS; SMAD3 PROTEIN; SMAD4 PROTEIN; STRESS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 0038369998     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(03)00109-6     Document Type: Article

References (58)

1. Ashcroft G.S., Yang X., Glick A.B., Weinstein M., Letterio J.L., Mizel D.E., Anzano M., Greenwell-Wild T., Wahl S.M., Deng C., Roberts A.B. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat. Cell Biol. 1:1999;260-266.
2. Benezra R. The Id proteins. targets for inhibiting tumor cells and their blood supply Biochim. Biophys. Acta. 1551:2001;F39-F47.
3. Benezra R., Davis R.L., Lassar A., Tapscott S., Thayer M., Lockshon D., Weintraub H. Id. a negative regulator of helix-loop-helix DNA binding proteins. Control of terminal myogenic differentiation Ann. NY Acad. Sci. 599:1990;1-11.
4. Benezra R., Rafii S., Lyden D. The Id proteins and angiogenesis. Oncogene. 20:2001;8334-8341.
5. Boukamp P., Petrussevska R.T., Breitkreutz D., Hornung J., Markham A., Fusenig N.E. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106:1988;761-771.
6. Cai Y., Zhang C., Nawa T., Aso T., Tanaka M., Oshiro S., Ichijo H., Kitajima S. Homocysteine-responsive ATF3 gene expression in human vascular endothelial cells. activation of c-Jun NH(2)-terminal kinase and promoter response element Blood. 96:2000;2140-2148.
7. Calonge M.J., Massagué J. Smad4/DPC4 silencing and hyperactive Ras jointly disrupt transforming growth factor-beta antiproliferative responses in colon cancer cells. J. Biol. Chem. 274:1999;33637-33643.
8. Chen B.P., Liang G., Whelan J., Hai T. ATF3 and ATF3 delta Zip. Transcriptional repression versus activation by alternatively spliced isoforms. J. Biol. Chem. 269:1994;15819-15826.
9. Chen X., Rubock M.J., Whitman M. A transcriptional partner of MAD proteins in TGF-β signalling. Nature. 383:1996;691-696.
10. Chen C.R., Kang Y., Massagué J. Defective repression of c-myc in breast cancer cells. a loss at the core of the transforming growth factor beta growth arrest program Proc. Natl. Acad. Sci. USA. 98:2001;992-999.
11. Chen C.R., Kang Y., Siegel P.M., Massagué J. E2F4/5 and p107 as Smad cofactors linking the TGFβ receptor to c-myc repression. Cell. 110:2002;19-32.
12. Derynck R., Zhang Y., Feng X.H. Smads. transcriptional activators of TGF-β responses Cell. 95:1998;737-740.
13. Dickson M.C., Martin J.S., Cousins F.M., Kulkarni A.B., Karlsson S., Akhurst R.J. Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development. 121:1995;1845-1854.
14. Eischen C.M., Weber J.D., Roussel M.F., Sherr C.J., Cleveland J.L. Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev. 13:1999;2658-2669.
15. Flanders K.C., Sullivan C.D., Fujii M., Sowers A., Anzano M.A., Arabshahi A., Major C., Deng C., Russo A., Mitchell J.B., Roberts A.B. Mice lacking Smad3 are protected against cutaneous injury induced by ionizing radiation. Am. J. Pathol. 160:2002;1057-1068.
16. Gold L.I. The role for transforming growth factor-B (TGF-b) in human cancer. Crit. Rev. Oncog. 10:1999;303-360.
17. Hai T., Hartman M.G. The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors. activating transcription factor proteins and homeostasis Gene. 273:2001;1-11.
18. Hai T., Wolfgang C.D., Marsee D.K., Allen A.E., Sivaprasad U. ATF3 and stress responses. Gene Expr. 7:1999;321-335.
19. Hogan B.L.M. Bone morphogenetic proteins. multifunctional regulators of vertebrate development Genes Dev. 10:1996;1580-1594.
20. Iavarone A., Massagué J. Repression of the CDK activator Cdc25A and cell-cycle arrest by cytokine TGF-β in cells lacking the CDK inhibitor p15. Nature. 387:1997;417-422.
21. Ichijo H. From receptors to stress-activated MAP kinases. Oncogene. 18:1999;6087-6093.
22. Inman G.J., Nicolas F.J., Hill C.S. Nucleocytoplasmic shuttling of Smads 2, 3, and 4 permits sensing of TGF-β receptor activity. Mol. Cell. 10:2002;283-294.
23. Jen Y., Weintraub H., Benezra R. Overexpression of Id protein inhibits the muscle differentiation program. in vivo association of Id with E2A proteins Genes Dev. 6:1992;1466-1479.
24. Jen Y., Manova K., Benezra R. Expression patterns of Id1, Id2, and Id3 are highly related but distinct from that of Id4 during mouse embryogenesis. Dev. Dyn. 207:1996;235-252.
25. Kang Y., Cullen B.R. The human Tap protein is a nuclear mRNA export factor that contains novel RNA-binding and nucleocytoplasmic transport sequences. Genes Dev. 13:1999;1126-1139.
26. Korchynskyi O., ten Dijke P. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J. Biol. Chem. 277:2002;4883-4891.
27. Kretzschmar M., Doody J., Timokhina I., Massagué J. A mechanism of repression of TGFβ/Smad signaling by ongenic ras. Genes Dev. 13:1999;804-816.
28. Labbe E., Silvestri C., Hoodless P.A., Wrana J.L., Attisano L. Smad2 and Smad3 positively and negatively regulate TGF β-dependent transcription through the forkhead DNA-binding protein FAST2. Mol. Cell. 2:1998;109-120.
29. Laiho M., DeCaprio J.A., Ludlow J.W., Livingston D.M., Massagué J. Growth inhibition by TGF-β1 linked to suppression of retinoblastoma protein phosphorylation. Cell. 62:1990;175-185.
30. Langlands K., Down G.A., Kealey T. Id proteins are dynamically expressed in normal epidermis and dysregulated in squamous cell carcinoma. Cancer Res. 60:2000;5929-5933.
31. Lasorella A., Noseda M., Beyna M., Yokota Y., Iavarone A. Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins. Nature. 407:2000;592-598.
32. Lehman T.A., Modali R., Boukamp P., Stanek J., Bennett W.P., Welsh J.A., Metcalf R.A., Stampfer M.R., Fusenig N., Rogan E.M.et al. p53 mutations in human immortalized epithelial cell lines. Carcinogenesis. 14:1993;833-839.
33. Lin C.Q., Singh J., Murata K., Itahana Y., Parrinello S., Liang S.H., Gillett C.E., Campisi J., Desprez P.Y. A role for Id-1 in the aggressive phenotype and steroid hormone response of human breast cancer cells. Cancer Res. 60:2000;1332-1340.
34. López-Rovira T., Chalaux E., Massagué J., Rosa J.L., Ventura F. Direct binding of Smad1 and Smad4 to two distinct motifs mediates bone morphogenetic protein-specific transcriptional activation of Id1 gene. J. Biol. Chem. 277:2002;3176-3185.
35. Lyden D., Young A.Z., Zagzag D., Yan W., Gerald W., O'Reilly R., Bader B.L., Hynes R.O., Zhuang Y., Manova K., Benezra R. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature. 401:1999;670-677.
36. Martin J.S., Dickson M.C., Cousins F.M., Kulkarni A.B., Karlsson S., Akhurst R.J. Analysis of homozygous TGF beta 1 null mouse embryos demonstrates defects in yolk sac vasculogenesis and hematopoiesis. Ann. NY Acad. Sci. 752:1995;300-308.
37. Massagué J. TGFβ signal transduction. Annu. Rev. Biochem. 67:1998;753-791.
38. Massagué J. How cells read TGF-beta signals. Nat. Rev. Mol. Cell Biol. 1:2000;169-178.
39. Massagué J., Wotton D. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J. 19:2000;1745-1754.
40. Massagué J., Blain S.W., Lo R.S. TGFβ signaling in growth control, cancer, and heritable disorders. Cell. 103:2000;295-309.
41. Masuda A., Kondo M., Saito T., Yatabe Y., Kobayashi T., Okamoto M., Suyama M., Takahashi T. Establishment of human peripheral lung epithelial cell lines (HPL1) retaining differentiated characteristics and responsiveness to epidermal growth factor, hepatocyte growth factor, and transforming growth factor beta1. Cancer Res. 57:1997;4898-4904.
42. Norton J.D., Deed R.W., Craggs G., Sablitzky F. Id helix-loop-helix proteins in cell growth and differentiation. Trends Cell Biol. 8:1998;58-65.
43. Pepper M.S. Transforming growth factor-beta. vasculogenesis, angiogenesis, and vessel wall integrity Cytokine Growth Factor Rev. 8:1997;21-43.
44. Pfundt R., van Vlijmen-Willems I., Bergers M., Wingens M., Cloin W., Schalkwijk J. In situ demonstration of phosphorylated c-jun and p38 MAP kinase in epidermal keratinocytes following ultraviolet B irradiation of human skin. J. Pathol. 193:2001;248-255.
45. Roberts A.B., Sporn M.B. The transforming growth factor-betas. Sporn M.B., Roberts A.B. Peptide Growth Factors and Their Receptors. 1990;Springer-Verlag, Heidelberg. 419-472.pp.
46. Schindl M., Oberhuber G., Obermair A., Schoppmann S.F., Karner B., Birner P. Overexpression of Id-1 protein is a marker for unfavorable prognosis in early-stage cervical cancer. Cancer Res. 61:2001;5703-5706.
47. Seoane J., Le H.V., Massagué J. Myc suppression of the p21(Cip1) Cdk inhibitor influences the outcome of the p53 response to DNA damage. Nature. 419:2002;729-734.
48. Shi Y., Wang Y.-F., Jayaraman L., Yang H., Massagué J., Pavletich N. Crystal structure of a Smad MH1 domain bound to DNA. insights on DNA binding in TGF-β signaling Cell. 94:1998;585-594.
49. Soule H.D., Maloney T.M., Wolman S.R., Peterson W.D. Jr., Brenz R., McGrath C.M., Russo J., Pauley R.J., Jones R.F., Brooks S.C. Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res. 50:1990;6075-6086.
50. Takahashi Y., Rayman J.B., Dynlacht B.D. Analysis of promoter binding by the E2F and pRB families in vivo. distinct E2F proteins mediate activation and repression Genes Dev. 14:2000;804-816.
51. Takai N., Miyazaki T., Fujisawa K., Nasu K., Miyakawa I. Id1 expression is associated with histological grade and invasive behavior in endometrial carcinoma. Cancer Lett. 165:2001;185-193.
52. ten Dijke P., Miyazono K., Heldin C.H. Signaling inputs converge on nuclear effectors in TGF-beta signaling. Trends Biochem. Sci. 25:2000;64-70.
53. Tournay O., Benezra R. Transcription of the dominant-negative helix-loop-helix protein Id1 is regulated by a protein complex containing the immediate-early response gene Egr-1. Mol. Cell. Biol. 16:1996;2418-2430.
54. Truant R., Kang Y., Cullen B.R. The human tap nuclear RNA export factor contains a novel transportin-dependent nuclear localization signal that lacks nuclear export signal function. J. Biol. Chem. 274:1999;32167-32171.
55. Tsukazaki T., Chiang T.A., Davison A.F., Attisano L., Wrana J.L. SARA, a FYVE domain protein that recruits Smad2 to the TGFβ receptor. Cell. 95:1998;779-791.
56. Wolfgang C.D., Chen B.P., Martindale J.L., Holbrook N.J., Hai T. gadd153/Chop10, a potential target gene of the transcriptional repressor ATF3. Mol. Biol. Cell. 17:1997;6700-6707.
57. Wolfgang C.D., Liang G., Okamoto Y., Allen A.E., Hai T. Transcriptional autorepression of the stress-inducible gene ATF3. J. Biol. Chem. 275:2000;16865-16870.
58. Xu L., Kang Y., Col S., Massagué J. Smad2 nucleocytoplasmic shuttling by nucleoporins CAN/Nup214 and Nup153 feeds TGFβ signaling complexes in the cytoplasm and nucleus. Mol. Cell. 10:2002;271-282.