Receptor internalization-independent activation of Smad2 in activin signaling

Molecular Endocrinology

Volumn 18, Issue 7, 2004, Pages 1818-1826

  Zhou, Yunli ^a   Scolavino, Staci ^a   Funderburk, Sarah F ^a   Ficociello, Laura F ^a   Zhang, Xun ^a   Klibanski, Anne ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; ACTIVIN RECEPTOR 1; ALANINE; MUTANT PROTEIN; PHOSPHOTRANSFERASE; SMAD2 PROTEIN; TRYPTOPHAN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; INTERNALIZATION; NONHUMAN; POTASSIUM CELL LEVEL; POTASSIUM DEPLETION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ACTIVINS; ALANINE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; DNA-BINDING PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; POINT MUTATION; POTASSIUM; PROMOTER REGIONS (GENETICS); PROTEINS; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; TRANS-ACTIVATORS; TRYPTOPHAN;

ANIMALIA;

EID: 3042707155     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2004-0079     Document Type: Article

References (49)

1. Woodruff TK 1998 Regulation of cellular and system function by activin. Biochem Pharmacol 55:953-963
2. Shav-Tal Y, Zipori D 2002 The role of activin a in regulation of hemopoiesis. Stem Cells 20:493-500
3. Sakai R, Eto Y 2001 Involvement of activin in the regulation of bone metabolism. Mol Cell Endocrinol 180:183-188
4. Wankell M, Werner S, Alzheimer C 2003 The roles of activin in cytoprotection and tissue repair. Ann NY Acad Sci 995:48-58
5. Phillips DJ, Jones KL, Scheerlinck JY, Hedger MP, de Kretser DM 2001 Evidence for activin A and follistatin involvement in the systemic inflammatory response. Mol Cell Endocrinol 180:155-162
6. Zhou Y, Sun H, Danila DC, Johnson SR, Sigai DP, Zhang X, Klibanski A 2000 Truncated activin type I receptor Alk4 isoforms are dominant negative receptors inhibiting activin signaling. Mol Endocrinol 14:2066-2075
7. Alexander JM, Bikkal HA, Zervas NT, Laws Jr ER, Klibanski A 1996 Tumor-specific expression and alternate splicing of messenger ribonucleic acid encoding activin/transforming growth factor-β receptors in human pituitary adenomas. J Clin Endocrinol Metab 81:783-790
8. Hempen PM, Zhang L, Bansal RK, Iacobuzio-Donahue CA, Murphy KM, Maitra A, Vogelstein B, Whitehead RH, Markowitz SD, Willson JK, Yeo CJ, Hruban RH, Kern SE 2003 Evidence of selection for clones having genetic inactivation of the activin A type II receptor (ACVR2) gene in gastrointestinal cancers. Cancer Res 63:994-999
9. Su GH, Bansal R, Murphy KM, Montgomery E, Yeo CJ, Hruban RH, Kern SE 2001 ACVR1B (ALK4, activin receptor type 1B) gene mutations in pancreatic carcinoma. Proc Natl Acad Sci USA 98:3254-3257
10. Massague J 1998 TGF-β signal transduction. Annu Rev Biochem 67:753-791
11. Shi Y, Massague J 2003 Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113:685-700
12. Tsukazaki T, Chiang TA, Davison AF, Attisano L, Wrana JL 1998 SARA, a FYVE domain protein that recruits Smad2 to the TGFβ receptor. Cell 95:779-791
13. Panopoulou E, Gillooly DJ, Wrana JL, Zerial M, Stenmark H, Murphy C, Fotsis T 2002 Early endosomal regulation of Smad-dependent signaling in endothelial cells. J Biol Chem 277:18046-18052
14. Miura S, Takeshita T, Asao H, Kimura Y, Murata K, Sasaki Y, Hanai JI, Beppu H, Tsukazaki T, Wrana JL, Miyazono K, Sugamura K 2000 Hgs (Hrs), a FYVE domain protein, is involved in Smad signaling through cooperation with SARA. Mol Cell Biol 20:9346-9355
15. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL 2003 Distinct endocytic pathways regulate TGF-β receptor signalling and turnover. Nat Cell Biol 5:410-421
16. Penheiter SG, Mitchell H, Garamszegi N, Edens M, Dore Jr JJ, Leof EB 2002 Internalization-dependent and -independent requirements for transforming growth factor β receptor signaling via the Smad pathway. Mol Cell Biol 22:4750-4759
17. Lu Z, Murray JT, Luo W, Li H, Wu X, Xu H, Backer JM, Chen YG 2002 Transforming growth factor β activates Smad2 in the absence of receptor endocytosis. J Biol Chem 277:29363-29368
18. Hayes S, Chawla A, Corvera S 2002 TGF β receptor internalization into EEA1-enriched early endosomes: role in signaling to Smad2. J Cell Biol 158:1239-1249
19. Ehrlich M, Shmuely A, Henis YI 2001 A single internalization signal from the di-leucine family is critical for constitutive endocytosis of the type II TGF-β receptor. J Cell Sci 114:1777-1786
20. Traub LM 2003 Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J Cell Biol 163:203-208
21. Yao D, Ehrlich M, Henis YI, Leof EB 2002 Transforming growth factor-β receptors interact with AP2 by direct binding to β2 subunit. Mol Biol Cell 13:4001-4012
22. Garamszegi N, Dore Jr JJ, Penheiter SG, Edens M, Yao D, Leof EB 2001 Transforming growth factor β receptor signaling and endocytosis are linked through a COOH terminal activation motif in the type I receptor. Mol Biol Cell 12:2881-2893
23. Wicks SJ, Lui S, Abdel-Wahab N, Mason RM, Chantry A 2000 Inactivation of smad-transforming growth factor β signaling by Ca(2+)-calmodulin-dependent protein kinase II. Mol Cell Biol 20:8103-8111
24. Matsuzaki T, Hanai S, Kishi H, Liu Z, Bao Y, Kikuchi A, Tsuchida K, Sugino H 2002 Regulation of endocytosis of activin type II receptors by a novel PDZ protein through Ral/Ral-binding protein 1 -dependent pathway. J Biol Chem 277:19008-19018
25. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, Oeda E, Tamaki K, Hanai J, Heldin CH, Miyazono K, ten Dijke P 1997 TGF-β receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J 16:5353-5362
26. Chen YG, Hata A, Lo RS, Wotton D, Shi Y, Pavletich N, Massague J 1998 Determinants of specificity in TGF-β signal transduction. Genes Dev 12:2144-2152
27. Lin HY, Wang XF, Ng-Eaton E, Weinberg RA, Lodish HF 1992 Expression cloning of the TGF-β type II receptor, a functional transmembrane serine/threonine kinase. Cell [Erratum (1992) 70:following 1068] 68:775-785
28. ten Dijke P, Ichijo H, Franzen P, Schulz P, Saras J, Toyoshima H, Heldin CH, Miyazono K 1993 Activin receptor-like kinases: a novel subclass of cell-surface receptors with predicted serine/threonine kinase activity. Oncogene 8:2879-2887
29. Feng XH, Derynck R 1997 A kinase subdomain of transforming growth factor-β (TGF-β) type I receptor determines the TGF-β intracellular signaling specificity. EMBO J 16:3912-3923
30. Franzen P, ten Dijke P, Ichijo H, Yamashita H, Schulz P, Heldin CH, Miyazono K 1993 Cloning of a TGF β type I receptor that forms a heteromeric complex with the TGF β type II receptor. Cell 75:681-692
31. ten Dijke P, Yamashita H, Ichijo H, Franzen P, Laiho M, Miyazono K, Heldin CH 1994 Characterization of type I receptors for transforming growth factor-β and activin. Science 264:101-104
32. Penton A, Chen Y, Staehling-Hampton K, Wrana JL, Attisano L, Szidonya J, Cassill JA, Massague J, Hoffmann FM 1994 Identification of two bone morphogenetic protein type I receptors in Drosophila and evidence that Brk25D is a decapentaplegic receptor. Cell 78:239-250
33. Nellen D, Affolter M, Basler K 1994 Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic. Cell 78:225-237
34. Wrana JL, Tran H, Attisano L, Arora K, Childs SR, Massague J, O'Connor MB 1994 Two distinct transmembrane serine/threonine kinases from Drosophila melanogaster form an activin receptor complex. Mol Cell Biol 14:944-950
35. Georgi LL, Albert PS, Riddle DL 1990 daf-1, A C. elegans gene controlling dauer larva development, encodes a novel receptor protein kinase. Cell 61:635-645
36. Donaldson CJ, Mathews LS, Vale WW 1992 Molecular cloning and binding properties of the human type II activin receptor. Biochem Biophys Res Commun 184:310-316
37. Hilden K, Tuuri T, Eramaa M, Ritvos O 1994 Expression of type II activin receptor genes during differentiation of human K562 cells and cDNA cloning of the human type IIB activin receptor. Blood 83:2163-2170
38. Rosenzweig BL, Imamura T, Okadome T, Cox GN, Yamashita H, ten Dijke P, Heldin CH, Miyazono K 1995 Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc Natl Acad Sci USA 92:7632-7636
39. Teixeira J, He WW, Shah PC, Morikawa N, Lee MM, Catlin EA, Hudson PL, Wing J, Maclaughlin DT, Donahoe PK 1996 Developmental expression of a candidate mullerian inhibiting substance type II receptor. Endocrinology 137:160-165
40. ten Dijke P, Miyazono K, Heldin CH 2000 Signaling inputs converge on nuclear effectors in TGF-β signaling. Trends Biochem Sci 25:64-70
41. Attisano L, Wrana JL, Montalvo E, Massague J 1996 Activation of signalling by the activin receptor complex. Mol Cell Biol 16:1066-1073
42. Kirchhausen T 2002 Clathrin adaptors really adapt. Cell 109:413-416
43. Kirchhausen T 1999 Adaptors for clathrin-mediated traffic. Annu Rev Cell Dev Biol 15:705-732
44. Hanks SK, Quinn AM, Hunter T 1988 The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42-52
45. Chen F, Weinberg RA 1995 Biochemical evidence for the autophosphorylation and transphosphorylation of transforming growth factor β receptor kinases. Proc Natl Acad Sci USA 92:1565-1569
46. Zhou Y, Mehta KR, Choi AP, Scolavino S, Zhang X 2003 DNA damage-induced inhibition of securin expression is mediated by p53. J Biol Chem 278:462-470
47. Wrana JL, Attisano L, Carcamo J, Zentella A, Doody J, Laiho M, Wang XF, Massague J 1992 TGFβ signals through a heteromeric protein kinase receptor complex. Cell 71:1003-1014
48. Marmorstein AD, Zurzolo C, Bivic AL, Rodriguez-Boulan E 1998 Cell surface biotinylation techniques and determination of protein polarity. In: Celis JE, ed. Cell biology: a laboratory handbook. 2nd ed. San Diego: Academic Press; 341-350
49. Larkin JM, Brown MS, Goldstein JL, Anderson RG 1983 Depletion of intracellular potassium arrests coated pit formation and receptor-mediated endocytosis in fibroblasts. Cell 33:273-285