TLP, a novel modulator of TGF-β signaling, has opposite effects on Smad2- and Smad3-dependent signaling

EMBO Journal

Volumn 22, Issue 17, 2003, Pages 4465-4477

  Felici, Angelina ^a   Wurthner, Jens U ^a,c   Parks, W Tony ^a,d   Giam, Louise Ruh Yu ^a   Reiss, Michael ^b   Karpova, Tatiana S ^a   McNally, James G ^a   Roberts, Anita B ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b Department of Emergency Medicine   (United States)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Smad proteins; TGF receptors; TGF signaling; TRAP 1

Indexed keywords

ACTIVIN; ACTIVIN RECEPTOR 2; BINDING PROTEIN; CELL SURFACE RECEPTOR; CHAPERONE; CYTOKINE; PROTEIN SERINE THREONINE KINASE; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRAP 1 LIKE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL SPECIFICITY; COMPLEX FORMATION; CONTROLLED STUDY; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RECEPTOR BINDING; REPORTER GENE; SIGNAL TRANSDUCTION;

ACTIVINS; AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CELL LINE; CLONING, MOLECULAR; COS CELLS; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; ENDOCYTOSIS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KINETICS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA;

EID: 0042738094     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg428     Document Type: Article

References (53)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
2. Caplan, S., Hartnell, L.M., Aguilar, R.C., Naslavsky, N. and Bonifacino, J.S. (2001) Human Vam6p promotes lysosome clustering and fusion in vivo. J. Cell Biol., 154, 109-122.
3. Charng, M.J., Zhang, D., Kinnunen, P. and Schneider, M.D. (1998) A novel protein distinguishes between quiescent and activated forms of the type I transforming growth factor beta receptor. J. Biol. Chem., 273, 9365-9368.
4. Chen, R.H., Miettinen, P.J., Maruoka, E.M., Choy, L. and Derynck, R. (1995) A WD-domain protein that is associated with and phosphorylated by the type II TGF-beta receptor. Nature, 377, 548-552.
5. Datta, P.K. and Moses, H.L. (2000) STRAP and Smad7 synergize in the inhibition of Transforming growth factor β signaling. Mol. Cell. Biol., 20, 3157-3167.
6. de Caestecker, M.P., Piek, E. and Roberts, A.B. (2000) Role of transforming growth factor-beta signaling in cancer. J. Natl Cancer Inst., 92, 1388-1402.
7. de Renzis, S., Sonnichsen, B. and Zerial, M. (2002) Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes. Nat. Cell Biol., 4, 124-133.
8. Di Guglielmo, G.M., Le Roy, C., Goodfellow, A.F. and Wrana, J.L. (2003) Distinct endocytic pathways regulate TGF-b receptor signaling and turnover. Nat. Cell Biol., 5, 410-421.
9. Doré, J.J.E., Jr, Edens, M., Garamszegi, N. and Leof, E.B. (1998) Heteromeric and homomeric transforming growth factor-β receptors show distinct signaling and endocytic responses in epithelial cells. J. Biol. Chem., 273, 31770-31777.
10. Elbashir, S.M., Harboth, J., Lendeckel, W., Yalcin, A., Weber, K. and Tuschl, T. (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature, 411, 494-498.
11. Griswold-Prenner, I., Kamibayashi, C., Maruoka, E.M., Mumby, M.C. and Derynck, R. (1998) Physical and functional interactions between type I transforming growth factor beta receptors and Balpha, a WD-40 repeat subunit of phosphatase 2A. Mol. Cell. Biol., 18, 6595-6604.
12. Hayes, S., Chawla, A. and Corvera, S. (2002) TGF beta receptor internalization into EEA1-enriched early endosomes: role in signaling to Smad2. J. Cell Biol., 158, 1239-1249.
13. Hocevar, B.A., Smine, A., Xu, X-X. and Howe, P.H. (2001) The adaptor molecule Disabled-2 links the transforming growth factor β receptors to the Smad pathway. EMBO J., 20, 2789-2801.
14. Hu, Y., Chuang, J.Z., Xu, K., McGraw, T.G. and Sung, C.H. (2002) SARA, a FYVE domain protein, affects Rab5-mediated endocytosis. J. Cell Sci., 115, 4755-4763.
15. Inman, G.J. and Hill, C. (2002) Stoichiometry of active Smad-transcription factor complexes on DNA. J. Biol. Chem., 277, 51008-51016.
16. Itoh, F., Divecha, N., Brocks, L., Oomen, L., Janssen, H., Calafat, J., Itoh, S. and Dijke, Pt.P. (2002) The FYVE domain in Smad anchor for receptor activation (SARA) is sufficient for localization of SARA in early endosomes and regulates TGF-beta/Smad signaling. Genes Cells, 7, 321-331.
17. Korchynskyi, O. and ten Dijke, P. (2002) Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Idl promoter. J. Biol. Chem., 277, 4883-4891.
18. Labbé, E., Silvestri, C., Hoodless, P.A., Wrana, J.L. and Attisano, L. (1998). Smad2 and Smad3 positively and negatively regulate TGF-dependent transcription through the forkhead DNA binding protein FAST2. Mol. Cell, 2, 109-120.
19. McPherson, PS (2002) The endocytic machinery at an interface with the actin cytoskeleton: a dynamic, hip intersection. Trends Cell Biol., 12, 312-315.
20. Macias-Silva, M., Abdollah, S., Hoodless, P.A., Pirone, R., Attisano, L. and Wrana, J.L. (1996) MADR2 is a substrate of the TGFbeta receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell, 87, 1215-1224.
21. Madaule, P., Furuyashiki, T., Reid, T., Ishizaki, T., Watanabe, G., Morii, N. and Narumiya, S. (1995) A novel partner for the GTP-bound forms of rho and rac. FEBS Lett., 377, 243-248.
22. Massague, J. and Chen, Y.G. (2000) Controlling TGF-beta signaling. Genes Dev., 14, 627-644.
23. Massague, J., Blain, S.W. and Lo, R.S. (2000) TGFbeta signaling in growth control, cancer and heritable disorders. Cell, 103, 295-309.
24. Mishra, S.K., Keyel, P.A., Hawryluk, M.J., Agostinelli, N.R., Watkins, S.C. and Traub, L.M. (2002) Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J., 21, 4915-4926.
25. Miura, S. et al. (2000) Hgs (Hrs), a FYVE domain protein, is involved in Smad signaling through cooperation with SARA. Mol. Cell. Biol., 20, 9346-9355.
26. Miyazono, K., ten Dijke, P. and Heldin, C.H. (2000) TGF-beta signaling by Smad proteins. Adv. Immunol., 75, 115-157.
27. Morris, S.M. and Cooper, J.A. (2001) Disabled-2 colocalizes with the LDLR in clathrin-coated pits and interacts with AP-2. Traffic, 2, 111-123.
28. Moustakas, A. and Heldin, C.H. (2002) From mono- to oligo-Smads: the heart of the matter in TGF-signal transduction. Genes Dev., 16, 1867-1871.
29. Moustakas, A., Souchelnytskyi, S. and Heldin, C.H. (2001) Smad regulation in TGF-beta signal transduction. J. Cell Sci., 114, 4359-4369.
30. Nagarajan, R.P., Liu, J. and Chen, Y. (1999) Smad3 inhibits transforming growth factor-beta and activin signaling by competing with Smad4 for FAST-2 binding. J. Biol. Chem., 274, 31229-31235.
31. Nagase, T., Kikuno, R., Ishikawa, K., Hirosawa, M. and Ohara, O. (2000) Prediction of the coding sequences of unidentified human genes. XVII. The complete sequences of 100 new cDNA clones from brain which code for large proteins in vitro. DNA Res., 7, 143-150.
32. Nakamura, N., Hirata, A., Ohsumi, Y. and Wada, Y. (1997) Vam2/Vps41p and Vam6/Vps39p are components of a protein complex on the vacuolar membranes and involved in the vacuolar assembly in the yeast Saccharomyces cerevisiae. J. Biol. Chem., 272, 11344-11349.
33. Panopoulou, E., Gillooly, D.J., Wrana, J.L., Zerial, M., Stenmark, H., Murphy, C. and Fotsis, T. (2002) Early endosomal regulation of Smad-dependent signaling in endothelial cells. J. Biol. Chem., 277, 18046-18052.
34. Penheiter, S.G., Mitchell, H., Garamszegi, N., Edens, M., Dore, J.J., Jr and Leof, E.B. (2002) Internalization-dependent and -independent requirements for transforming growth factor beta receptor signaling via the Smad pathway. Mol. Cell. Biol., 22, 4750-4759.
35. Perlman, R., Schiemann, W.P., Brooks, M.W., Lodish, H.F. and Weinberg, R.A. (2001) TGF-beta-induced apoptosis is mediated by the adaptor protein Daxx that facilitates JNK activation. Nat. Cell Biol., 8, 708-714.
36. Piek, E. et al. (2001) Functional characterization of transforming growth factor beta signaling in Smad2- and Smad3-deficient fibroblasts. J. Biol. Chem., 276, 19945-19953.
37. Raiborg, C., Bache, K.G., Mehlum, A., Stang, E. and Stenmark, H. (2001) Hrs recruits clathrin to early endosomes. EMBO J., 20, 5008-5021.
38. Raiborg, C., Bache, K.G., Gillooly, D.J., Madshus, I.H., Stang, E. and Stenmark, H. (2002) Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat. Cell Biol., 4, 394-398.
39. Razani, B., Zhang, X.L., Bitzer, M., von Gersdorff, G., Bottinger, E.P. and Lisanti, M.P. (2001) Caveolin-1 regulates transforming growth factor (TGF)-b/SMAD signaling through an interaction with the TGF-β type I receptor. J. Biol. Chem., 276, 6727-6738.
40. Roberts, A.B. and Sporn, M.B. (1990) The transforming growth factors-b. In Sporn, M.B. and Roberts, A.B. (eds), Handbook of Experimental Pharmacology. Peptide Growth Factors and Their Receptors. Springer-Verlag, Berlin, pp. 419-472.
41. Schultz, J., Copley, R.R., Doerks, T., Ponting, C.P. and Bork, P. (2000) SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res., 28, 231-234.
42. Seet, L.F. and Hong, W. (2001) Endofin, an endosomal FYVE domain protein. J. Biol. Chem., 276, 42445-42454.
43. Tsukazaki, T., Chiang, T.A., Davison, A.F., Attisano, L. and Wrana, J.L. (1998) SARA, a FYVE domain protein that recruits Smad2 to the TGFbeta receptor. Cell, 95, 779-791.
44. von Gersdorff, G., Susztak, K., Rezvani, F., Bitzer, M., Liang, D. And Bottinger, E.P. (2000) Smad3 and Smad4 mediate transcriptional activation of the human Smad7 promoter by transforming growth factor B. J. Biol. Chem., 275, 11320-11326.
45. Wang, T., Li, B.Y., Danielson, P.D., Shah, P.C., Rockwell, S., Lechleider, R.J., Martin, J., Manganaro, T. and Donahoe, P.K. (1996) The immunophilin FKBP12 functions as a common inhibitor of the TGF beta family type I receptors. Cell, 86, 435-444.
46. Weinstein, M., Yang, X. and Deng, C (2000) Functions of mammalian Smad genes as revealed by targeted gene disruption in mice. Cytokine Growth Factor Rev., 11, 49-58.
47. Weis-Garcia, F. and Massague, J. (1996) Complementation between kinase-defective and activation-defective TGF-beta receptors reveals a novel form of receptor cooperativity essential for signaling. EMBO J., 15, 276-289.
48. Wieser, R., Wrana, J.L. and Massague, J. (1995) GS domain mutations that constitutively activate T beta R-I, the downstream signaling component in the TGF-beta receptor complex. EMBO J., 14, 2199-2208.
49. Wurthner, J.U., Frank, D.B., Felici, A., Green, H.M., Cao, Z., Schneider, M.D., McNally, J.G., Lechleider, R.J. and Roberts, A.B. (2001) Transforming growth factor-beta receptor-associated protein 1 is a Smad4 chaperone. J. Biol. Chem., 276, 19495-19502.
50. Yagi, K., Goto, D., Hamamoto, T., Takenoshita, S., Kato, M. and Miyazono, K. (1999) Alternatively spliced variant of Smad2 lacking exon 3. Comparison with wild-type Smad2 and Smad3. J. Biol. Chem., 274, 703-709.
51. 2 subunit. Mol. Biol. Cell, 13, 4001-4012.
52. Ybe, J.A., Brodsky, F.M., Hofmann, K., Lin, K., Liu, S.H., Chen, L., Earnest, T.N., Fletterick, R.J. and Hwang, P.K. (1999) Clathrin self-assembly is mediated by a tandemly repeated superhelix. Nature, 399, 371-375.
53. Zawel, L., Dai, J.L., Buckhaults, P., Zhou, S., Kinzler, K.W., Vogelstein, B and Kern, S.E. (1998) Human Smad3 and Smad4 are sequence-specific transcription activators. Mol. Cell, 1, 611-617.