Caveolin-1 is required for TGF-ß-induced transactivation of the EGF receptor pathway in hepatocytes through the activation of the metalloprotease TACE/ADAM17

Cell Death and Disease

Volumn 5, Issue 7, 2014, Pages

  Moreno Caceres J ^a   Caja, L ^a   Mainez, J ^b   Mayoral, R ^c,d   Martin Sanz P ^d,e   Moreno Vicente, R ^f   Del Pozo, M A ^f   Dooley, S ^g   Egea, G ^b   Fabregat, I ^a,h  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b Department of Cell Biology Immunology and Neuroscience School of Medicine IDIBAPSUniversity of Barcelona   (Spain)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

^e INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^f CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^g UNIVERSITY OF HEIDELBERG   (Germany)

^h UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM PROTEIN; ADAM17 PROTEIN; CASPASE 3; CAVEOLIN 1; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; UNCLASSIFIED DRUG; TUMOR NECROSIS FACTOR-ALPHA CONVERTASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; LIVER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSACTIVATION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; ENZYMOLOGY; FEMALE; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ADAM PROTEINS; ANIMALS; APOPTOSIS; CAVEOLIN 1; CELLS, CULTURED; ENZYME ACTIVATION; FEMALE; HEPATOCYTES; MALE; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84905452869     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.294     Document Type: Article

References (48)

1. Massague J. TGFbeta in cancer. Cell 2008; 134: 215-230
2. Valdes F, Murillo MM, Valverde AM, Herrera B, Sanchez A, Benito M et al. Transforming growth factor-beta activates both pro-apoptotic and survival signals in fetal rat hepatocytes. Exp Cell Res 2004; 292: 209-218
3. Valdes F, Alvarez AM, Locascio A, Vega S, Herrera B, Fernandez M et al. The epithelial mesenchymal transition confers resistance to the apoptotic effects of transforming growth factor Beta in fetal rat hepatocytes. Mol Cancer Res 2002; 1: 68-78
4. Murillo MM, del Castillo G, Sanchez A, Fernandez M, Fabregat I. Involvement of EGF receptor and c-Src in the survival signals induced by TGF-beta1 in hepatocytes. Oncogene 2005; 24: 4580-4587
5. Murillo MM, Carmona-Cuenca I, Del Castillo G, Ortiz C, Roncero C, Sanchez A et al. Activation of NADPH oxidase by transforming growth factor-beta in hepatocytes mediates up-regulation of epidermal growth factor receptor ligands through a nuclear factor-kappaBdependent mechanism. Biochem J 2007; 405: 251-259
6. Le Roy C, Wrana JL. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 2005; 6: 112-126
7. Chen YG. Endocytic regulation of TGF-beta signaling. Cell Res 2009; 19: 58-70
8. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL. Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 2003; 5: 410-421
9. Meyer C, Liu Y, Dooley S. Caveolin and TGF-beta entanglements. J Cell Physiol 2013; 228: 2097-2102
10. Meyer C, Godoy P, Bachmann A, Liu Y, Barzan D, Ilkavets I et al. Distinct role of endocytosis for Smad and non-Smad TGF-beta signaling regulation in hepatocytes. J Hepatol 2011; 55: 369-378
11. Meyer C, Liu Y, Kaul A, Peipe I, Dooley S. Caveolin-1 abrogates TGF-beta mediated hepatocyte apoptosis. Cell Death Dis 2013; 4: e466
12. Fernandez-Rojo MA, Restall C, Ferguson C, Martel N, Martin S, Bosch M et al. Caveolin-1 orchestrates the balance between glucose and lipid-dependent energy metabolism: Implications for liver regeneration. Hepatology 2012; 55: 1574-1584
13. Wang Y, Posner BI, Balbis A. Compartmentalization of epidermal growth factor receptor in liver plasma membrane. J Cell Biochem 2009; 107: 96-103
14. Pol A, Lu A, Pons M, Peiro S, Enrich C. Epidermal growth factor-mediated caveolin recruitment to early endosomes and MAPK activation. Role of cholesterol and actin cytoskeleton. J Biol Chem 2000; 275: 30566-30572
15. Park JH, Han HJ. Caveolin-1 plays important role in EGF-induced migration and proliferation of mouse embryonic stem cells: Involvement of PI3K/Akt and ERK. Am J Physiol Cell Physiol 2009; 297: C935-C944
16. Mayoral R, Valverde AM, Llorente Izquierdo C, Gonzalez-Rodriguez A, Bosca L, Martin- Sanz P. Impairment of transforming growth factor beta signaling in caveolin-1-deficient hepatocytes: role in liver regeneration. J Biol Chem 2010; 285: 3633-3642
17. Carmona-Cuenca I, Roncero C, Sancho P, Caja L, Fausto N, Fernandez M et al. Upregulation of the NADPH oxidase NOX4 by TGF-beta in hepatocytes is required for its pro-apoptotic activity. J Hepatol 2008; 49: 965-976
18. Caja L, Sancho P, Bertran E, Fabregat I. Dissecting the effect of targeting the epidermal growth factor receptor on TGF-beta-induced-apoptosis in human hepatocellular carcinoma cells. J Hepatol 2011; 55: 351-358
19. Takaguri A, Shirai H, Kimura K, Hinoki A, Eguchi K, Carlile-Klusacek M et al. Caveolin-1 negatively regulates a metalloprotease-dependent epidermal growth factor receptor transactivation by angiotensin II. J Mol Cell Cardiol 2011; 50: 545-551
20. D'Alessio A, Esposito B, Giampietri C, Ziparo E, Pober JS, Filippini A. Plasma membrane microdomains regulate TACE-dependent TNFR1 shedding in human endothelial cells. J Cell Mol Med 2012; 16: 627-636
21. Xu P, Liu J, Derynck R. Post-translational regulation of TGF-beta receptor and Smad signaling. FEBS Lett 2012; 586: 1871-1884
22. Massague J. TGFbeta signalling in context. Nat Rev Mol Cell Biol 2012; 13: 616-630
23. Vizan P, Miller DS, Gori I, Das D, Schmierer B, Hill CS. Controlling long-term signaling: receptor dynamics determine attenuation and refractory behavior of the TGF-beta pathway. Sci Signal 2013; 6: ra106
24. Sunnarborg SW, Hinkle CL, Stevenson M, Russell WE, Raska CS, Peschon JJ et al. Tumor necrosis factor-alpha converting enzyme (TACE) regulates epidermal growth factor receptor ligand availability. J Biol Chem 2002; 277: 12838-12845
25. Tellier E, Canault M, Poggi M, Bonardo B, Nicolay A, Alessi MC et al. HDLs activate ADAM17-dependent shedding. J Cell Physiol 2008; 214: 687-693
26. Parr-Sturgess CA, Rushton DJ, Parkin ET. Ectodomain shedding of the Notch ligand Jagged1 is mediated by ADAM17, but is not a lipid-raft-associated event. Biochem J 2010; 432: 283-294
27. Waugh MG, Lawson D, Hsuan JJ. Epidermal growth factor receptor activation is localized within low-buoyant density, non-caveolar membrane domains. Biochem J 1999; 337(Pt 3): 591-597
28. Mineo C, Gill GN, Anderson RG. Regulated migration of epidermal growth factor receptor from caveolae. J Biol Chem 1999; 274: 30636-30643
29. Couet J, Sargiacomo M, Lisanti MP. Interaction of a receptor tyrosine kinase, EGF-R, with caveolins. Caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J Biol Chem 1997; 272: 30429-30438
30. Kazazic M, Roepstorff K, Johannessen LE, Pedersen NM, van Deurs B, Stang E et al. EGF-induced activation of the EGF receptor does not trigger mobilization of caveolae. Traffic 2006; 7: 1518-1527
31. Henriksen L, Grandal MV, Knudsen SL, van Deurs B, Grovdal LM. Internalization mechanisms of the epidermal growth factor receptor after activation with different ligands. PLoS One 2013; 8: e58148
32. Pol A, Calvo M, Enrich C. Isolated endosomes from quiescent rat liver contain the signal transduction machinery. Differential distribution of activated Raf-1 and Mek in the endocytic compartment. FEBS Lett 1998; 441: 34-38
33. Lu Z, Ghosh S, Wang Z, Hunter T. Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion. Cancer Cell 2003; 4: 499-515
34. Ning Y, Buranda T, Hudson LG. Activated epidermal growth factor receptor induces integrin alpha2 internalization via caveolae/raft-dependent endocytic pathway. J Biol Chem 2007; 282: 6380-6387
35. Tang Y, Zeng X, He F, Liao Y, Qian N, Toi M. Caveolin-1 is related to invasion, survival, and poor prognosis in hepatocellular cancer. Med Oncol 2012; 29: 977-984
36. Tse EY, Ko FC, Tung EK, Chan LK, Lee TK, Ngan ES et al. Caveolin-1 overexpression is associated with hepatocellular carcinoma tumourigenesis and metastasis. J Pathol 2012; 226: 645-653
37. Meyer C, Dzieran J, Liu Y, Schindler F, Munker S, Muller A et al. Distinct dedifferentiation processes affect caveolin-1 expression in hepatocytes. Cell Commun Signal 2013; 11: 6
38. Bertran E, Crosas-Molist E, Sancho P, Caja L, Lopez-Luque J, Navarro E et al. Overactivation of the TGF-beta pathway confers a mesenchymal-like phenotype and CXCR4-dependent migratory properties to liver tumor cells. Hepatology 2013; 58: 2032-2044
39. Sancho P, Bertran E, Caja L, Carmona-Cuenca I, Murillo MM, Fabregat I. The inhibition of the epidermal growth factor (EGF) pathway enhances TGF-beta-induced apoptosis in rat hepatoma cells through inducing oxidative stress coincident with a change in the expression pattern of the NADPH oxidases (NOX) isoforms. Biochim Biophys Acta 2009; 1793: 253-263
40. Caja L, Ortiz C, Bertran E, Murillo MM, Miro-Obradors MJ, Palacios E et al. Differential intracellular signalling induced by TGF-beta in rat adult hepatocytes and hepatoma cells: Implications in liver carcinogenesis. Cell Signal 2007; 19: 683-694
41. Wang SE, Xiang B, Guix M, Olivares MG, Parker J, Chung CH et al. Transforming growth factor beta engages TACE and ErbB3 to activate phosphatidylinositol-3 kinase/Akt in ErbB2-overexpressing breast cancer and desensitizes cells to trastuzumab. Mol Cell Biol 2008; 28: 5605-5620
42. Wang SE, Xiang B, Zent R, Quaranta V, Pozzi A, Arteaga CL. Transforming growth factor beta induces clustering of HER2 and integrins by activating Src-focal adhesion kinase and receptor association to the cytoskeleton. Cancer Res 2009; 69: 475-482
43. Ebi M, Kataoka H, Shimura T, Kubota E, Hirata Y, Mizushima T et al. TGFbeta induces proHB-EGF shedding and EGFR transactivation through ADAM activation in gastric cancer cells. Biochem Biophys Res Commun 2010; 402: 449-454
44. Lu Y, Jiang F, Zheng X, Katakowski M, Buller B, To SS et al. TGF-beta1 promotes motility and invasiveness of glioma cells through activation of ADAM17. Oncol Rep 2011; 25: 1329-1335
45. Martin-Sanz P, Callejas NA, Casado M, Diaz-Guerra MJ, Bosca L. Expression of cyclooxygenase-2 in foetal rat hepatocytes stimulated with lipopolysaccharide and proinflammatory cytokines. Br J Pharmacol 1998; 125: 1313-1319
46. Valverde AM, Burks DJ, Fabregat I, Fisher TL, Carretero J, White MF et al. Molecular mechanisms of insulin resistance in IRS-2-deficient hepatocytes. Diabetes 2003; 52: 2239-2248
47. Grande-Garcia A, Echarri A, de Rooij J, Alderson NB, Waterman-Storer CM, Valdivielso JM et al. Caveolin-1 regulates cell polarization and directional migration through Src kinase and Rho GTPases. J Cell Biol 2007; 177: 683-694
48. Navarro-Lerida I, Alvarez-Barrientos A, Gavilanes F, Rodriguez-Crespo I. Distance-dependent cellular palmitoylation of de-novo-designed sequences and their translocation to plasma membrane subdomains. J Cell Sci 2002; 115: 3119-3130.