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Article

Integrin α1β1 Regulates Epidermal Growth Factor Receptor Activation by Controlling Peroxisome Proliferator-Activated Receptor γ-Dependent Caveolin-1 Expression

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Pages 3048-3058 | Received 08 Jul 2009, Accepted 11 Mar 2010, Published online: 20 Mar 2023

REFERENCES

  • Abulrob, A., S. Giuseppin, M. F. Andrade, A. McDermid, M. Moreno, and D. Stanimirovic. 2004. Interactions of EGFR and caveolin-1 in human glioblastoma cells: evidence that tyrosine phosphorylation regulates EGFR association with caveolae. Oncogene 23:6967–6979.
  • Adams, J. C., and F. M. Watt. 1993. Regulation of development and differentiation by the extracellular matrix. Development 117:1183–1198.
  • Alam, N., H. L. Goel, M. J. Zarif, J. E. Butterfield, H. M. Perkins, B. G. Sansoucy, T. K. Sawyer, and L. R. Languino. 2007. The integrin-growth factor receptor duet. J. Cell. Physiol. 213:649–653.
  • Askari, J. A., P. A. Buckley, A. P. Mould, and M. J. Humphries. 2009. Linking integrin conformation to function. J. Cell Sci. 122:165–170.
  • Baron, W., S. J. Shattil, and C. ffrench-Constant. 2002. The oligodendrocyte precursor mitogen PDGF stimulates proliferation by activation of alpha(v)beta3 integrins. EMBO J. 21:1957–1966.
  • Burgermeister, E., and R. Seger. 2007. MAPK kinases as nucleo-cytoplasmic shuttles for PPARgamma. Cell Cycle 6:1539–1548.
  • Burgermeister, E., L. Tencer, and M. Liscovitch. 2003. Peroxisome proliferator-activated receptor-gamma upregulates caveolin-1 and caveolin-2 expression in human carcinoma cells. Oncogene 22:3888–3900.
  • Byzova, T. V., C. K. Goldman, N. Pampori, K. A. Thomas, A. Bett, S. J. Shattil, and E. F. Plow. 2000. A mechanism for modulation of cellular responses to VEGF: activation of the integrins. Mol. Cell 6:851–860.
  • Chen, J., F. Capozza, A. Wu, T. Deangelis, H. Sun, M. Lisanti, and R. Baserga. 2008. Regulation of insulin receptor substrate-1 expression levels by caveolin-1. J. Cell. Physiol. 217:281–289.
  • Chen, X., T. D. Abair, M. R. Ibanez, Y. Su, M. R. Frey, R. S. Dise, D. B. Polk, A. B. Singh, R. C. Harris, R. Zent, and A. Pozzi. 2007. Integrin α1β1 controls reactive oxygen species synthesis by negatively regulating epidermal growth factor receptor-mediated Rac activation. Mol. Cell. Biol. 27:3313–3326.
  • Chen, X., G. Moeckel, J. D. Morrow, D. Cosgrove, R. C. Harris, A. B. Fogo, R. Zent, and A. Pozzi. 2004. Lack of integrin alpha1beta1 leads to severe glomerulosclerosis after glomerular injury. Am. J. Pathol. 165:617–630.
  • Cosgrove, D., D. T. Meehan, D. Delimont, A. Pozzi, X. Chen, K. D. Rodgers, R. M. Tempero, M. Zallocchi, and V. H. Rao. 2008. Integrin alpha1beta1 regulates matrix metalloproteinases via P38 mitogen-activated protein kinase in mesangial cells: implications for Alport syndrome. Am. J. Pathol. 172:761–773.
  • Couet, J., M. Sargiacomo, and M. P. Lisanti. 1997. Interaction of a receptor tyrosine kinase, EGF-R, with caveolins. Caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J. Biol. Chem. 272:30429–30438.
  • Dasu, M. R., S. Park, S. Devaraj, and I. Jialal. 2009. Pioglitazone inhibits Toll-like receptor expression and activity in human monocytes and db/db mice. Endocrinology 150:3457–3464.
  • de Laurentiis, A., L. Donovan, and A. Arcaro. 2007. Lipid rafts and caveolae in signaling by growth factor receptors. Open Biochem. J. 1:12–32.
  • Del Galdo, F., M. P. Lisanti, and S. A. Jimenez. 2008. Caveolin-1, transforming growth factor-beta receptor internalization, and the pathogenesis of systemic sclerosis. Curr. Opin. Rheumatol. 20:713–719.
  • Del Galdo, F., F. Sotgia, C. J. de Almeida, J. F. Jasmin, M. Musick, M. P. Lisanti, and S. A. Jimenez. 2008. Decreased expression of caveolin 1 in patients with systemic sclerosis: crucial role in the pathogenesis of tissue fibrosis. Arthritis Rheum. 58:2854–2865.
  • Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475–1489.
  • Dittmann, K., C. Mayer, R. Kehlbach, and H. P. Rodemann. 2008. Radiation-induced caveolin-1 associated EGFR internalization is linked with nuclear EGFR transport and activation of DNA-PK. Mol. Cancer 7:69.
  • Echarri, A., O. Muriel, and M. A. Del Pozo. 2007. Intracellular trafficking of raft/caveolae domains: insights from integrin signaling. Semin. Cell Dev. Biol. 18:627–637.
  • Engelman, J. A., X. L. Zhang, B. Razani, R. G. Pestell, and M. P. Lisanti. 1999. p42/44 MAP kinase-dependent and -independent signaling pathways regulate caveolin-1 gene expression. Activation of Ras-MAP kinase and protein kinase A signaling cascades transcriptionally down-regulates caveolin-1 promoter activity. J. Biol. Chem. 274:32333–32341.
  • Francois, H., S. Placier, M. Flamant, P. L. Tharaux, D. Chansel, J. C. Dussaule, and C. Chatziantoniou. 2004. Prevention of renal vascular and glomerular fibrosis by epidermal growth factor receptor inhibition. FASEB J. 18:926–928.
  • Gardner, H., A. Broberg, A. Pozzi, M. Laato, and J. Heino. 1999. Absence of integrin alpha1beta1 in the mouse causes loss of feedback regulation of collagen synthesis in normal and wounded dermis. J. Cell Sci. 112:263–272.
  • Genovese, T., S. Cuzzocrea, R. Di Paola, E. Mazzon, C. Mastruzzo, P. Catalano, M. Sortino, N. Crimi, A. P. Caputi, C. Thiemermann, and C. Vancheri. 2005. Effect of rosiglitazone and 15-deoxy-delta12,14-prostaglandin J2 on bleomycin-induced lung injury. Eur. Respir. J. 25:225–234.
  • Ghosh, A. K., J. Wei, M. Wu, and J. Varga. 2008. Constitutive Smad signaling and Smad-dependent collagen gene expression in mouse embryonic fibroblasts lacking peroxisome proliferator-activated receptor-gamma. Biochem. Biophys. Res. Commun. 374:231–236.
  • Giancotti, F. G., and E. Ruoslahti. 1999. Integrin signaling. Science 285:1028–1032.
  • Gu, D., H. Li, Z. Wang, Q. Chen, J. Jiang, and H. Zhu. 2007. Caveolin-1 inhibits the growth of human laryngeal squamous cell carcinoma and down regulates EGFR-MAPKs signaling pathway. Laryngoscope 117:1782–1789.
  • Harris, R. C., E. Chung, and R. J. Coffey. 2003. EGF receptor ligands. Exp. Cell Res. 284:2–13.
  • Hynes, R. 2002. Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687.
  • Jiang, L. Q., X. Feng, W. Zhou, P. G. Knyazev, A. Ullrich, and Z. Chen. 2006. Csk-binding protein (Cbp) negatively regulates epidermal growth factor-induced cell transformation by controlling Src activation. Oncogene 25:5495–5506.
  • Kanjanabuch, T., L. J. Ma, J. Chen, A. Pozzi, Y. Guan, P. Mundel, and A. B. Fogo. 2007. PPAR-gamma agonist protects podocytes from injury. Kidney Int. 71:1232–1239.
  • Kawabe, J., S. Okumura, M. C. Lee, J. Sadoshima, and Y. Ishikawa. 2004. Translocation of caveolin regulates stretch-induced ERK activity in vascular smooth muscle cells. Am. J. Physiol. Heart Circ. Physiol. 286:H1845–H1852.
  • Kawai, T., T. Masaki, S. Doi, T. Arakawa, Y. Yokoyama, T. Doi, N. Kohno, and N. Yorioka. 2009. PPAR-gamma agonist attenuates renal interstitial fibrosis and inflammation through reduction of TGF-beta. Lab. Invest. 89:47–58.
  • Khan, E. M., J. M. Heidinger, M. Levy, M. P. Lisanti, T. Ravid, and T. Goldkorn. 2006. Epidermal growth factor receptor exposed to oxidative stress undergoes Src- and caveolin-1-dependent perinuclear trafficking. J. Biol. Chem. 281:14486–14493.
  • Krajewska, W. M., and I. Maslowska. 2004. Caveolins: structure and function in signal transduction. Cell. Mol. Biol. Lett. 9:195–220.
  • Kwon, H., and Y. Pak. 2010. Prolonged tyrosine kinase activation of insulin receptor by pY27-calveolin-2. Biochem. Biophys. Res. Commun. 391:49–54.
  • Lajoie, P., E. A. Partridge, G. Guay, J. G. Goetz, J. Pawling, A. Lagana, B. Joshi, J. W. Dennis, and I. R. Nabi. 2007. Plasma membrane domain organization regulates EGFR signaling in tumor cells. Eur. J. Cell Biol. 179:341–356.
  • Leesnitzer, L. M., D. J. Parks, R. K. Bledsoe, J. E. Cobb, J. L. Collins, T. G. Consler, R. G. Davis, E. A. Hull-Ryde, J. M. Lenhard, L. Patel, K. D. Plunket, J. L. Shenk, J. B. Stimmel, C. Therapontos, T. M. Willson, and S. G. Blanchard. 2002. Functional consequences of cysteine modification in the ligand binding sites of peroxisome proliferator activated receptors by GW9662. Biochemistry 41:6640–6650.
  • Le Saux, C. J., K. Teeters, S. K. Miyasato, P. R. Hoffmann, O. Bollt, V. Douet, R. V. Shohet, D. H. Broide, and E. K. Tam. 2008. Down-regulation of caveolin-1, an inhibitor of transforming growth factor-beta signaling, in acute allergen-induced airway remodeling. J. Biol. Chem. 283:5760–5768.
  • Llaverias, G., M. Vazquez-Carrera, R. M. Sanchez, V. Noe, C. J. Ciudad, J. C. Laguna, and M. Alegret. 2004. Rosiglitazone upregulates caveolin-1 expression in THP-1 cells through a PPAR-dependent mechanism. J. Lipid Res. 45:2015–2024.
  • Lu, Z., S. Ghosh, Z. Wang, and T. Hunter. 2003. 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 4:499–515.
  • Luetteke, N. C., H. K. Phillips, T. H. Qiu, N. G. Copeland, H. S. Earp, N. A. Jenkins, and D. C. Lee. 1994. The mouse waved-2 phenotype results from a point mutation in the EGF receptor tyrosine kinase. Genes Dev. 8:399–413.
  • Mattila, E., T. Pellinen, J. Nevo, K. Vuoriluoto, A. Arjonen, and J. Ivaska. 2005. Negative regulation of EGFR signaling through integrin-alpha1beta1-mediated activation of protein tyrosine phosphatase TCPTP. Nat. Cell Biol. 7:78–85.
  • Moro, L., M. Venturino, C. Bozzo, L. Silengo, F. Altruda, L. Beguinot, G. Tarone, and P. Defilippi. 1998. Integrins induce activation of EGF receptor: role in MAP kinase induction and adhesion-dependent cell survival. EMBO J. 17:6622–6632.
  • Ning, Y., T. Buranda, and L. G. Hudson. 2007. Activated epidermal growth factor receptor induces integrin alpha2 internalization via caveolae/raft-dependent endocytic pathway. J. Biol. Chem. 282:6380–6387.
  • Park, D. S., A. W. Cohen, P. G. Frank, B. Razani, H. Lee, T. M. Williams, M. Chandra, J. Shirani, A. P. De Souza, B. Tang, L. A. Jelicks, S. M. Factor, L. M. Weiss, H. B. Tanowitz, and M. P. Lisanti. 2003. Caveolin-1 null (-/-) mice show dramatic reductions in life span. Biochemistry 42:15124–15131.
  • Park, S. C. 2002. Functional recovery of senescent cells through restoration of receptor-mediated endocytosis. Mech. Ageing Dev. 123:917–926.
  • Park, S. S., J. E. Kim, Y. A. Kim, Y. C. Kim, and S. W. Kim. 2005. Caveolin-1 is down-regulated and inversely correlated with HER2 and EGFR expression status in invasive ductal carcinoma of the breast. Histopathology 47:625–630.
  • Park, W. Y., J. S. Park, K. A. Cho, D. I. Kim, Y. G. Ko, J. S. Seo, and S. C. Park. 2000. Up-regulation of caveolin attenuates epidermal growth factor signaling in senescent cells. J. Biol. Chem. 275:20847–20852.
  • Pozzi, A., P. E. Moberg, L. A. Miles, S. Wagner, P. Soloway, and H. A. Gardner. 2000. Elevated matrix metalloprotease and angiostatin levels in integrin alpha 1 knockout mice cause reduced tumor vascularization. Proc. Natl. Acad. Sci. U. S. A. 97:2202–2207.
  • Qiao, L., Y. Dai, Q. Gu, K. W. Chan, J. Ma, H. Y. Lan, B. Zou, C. Rocken, M. P. Ebert, and B. C. Wong. 2008. Loss of XIAP sensitizes colon cancer cells to PPARgamma independent antitumor effects of troglitazone and 15-PGJ2. Cancer Lett. 268:260–271.
  • Richards, W. G., W. E. Sweeney, B. K. Yoder, J. E. Wilkinson, R. P. Woychik, and E. D. Avner. 1998. Epidermal growth factor receptor activity mediates renal cyst formation in polycystic kidney disease. J. Clin. Invest. 101:935–939.
  • Salanueva, I. J., A. Cerezo, M. C. Guadamillas, and M. A. del Pozo. 2007. Integrin regulation of caveolin function. J. Cell. Mol. Med. 11:969–980.
  • Sasai, K., K. Kakumoto, H. Hanafusa, and T. Akagi. 2007. The Ras-MAPK pathway downregulates Caveolin-1 in rodent fibroblast but not in human fibroblasts: implications in the resistance to oncogene-mediated transformation. Oncogene 26:449–455.
  • Schneller, E. S., K. Vuori, and E. Ruoslahti. 1997. Alphavbeta3 integrin associates with activated insulin and PDGFbeta receptors and potentiates the biological activity of PDGF. EMBO J. 16:5600–5607.
  • Sedding, D. G., J. Hermsen, U. Seay, O. Eickelberg, W. Kummer, C. Schwencke, R. H. Strasser, H. Tillmanns, and R. C. Braun-Dullaeus. 2005. Caveolin-1 facilitates mechanosensitive protein kinase B (Akt) signaling in vitro and in vivo. Circ. Res. 96:635–642.
  • Shi, F., and J. Sottile. 2008. Caveolin-1-dependent beta1 integrin endocytosis is a critical regulator of fibronectin turnover. J. Cell Sci. 121:2360–2371.
  • Sieg, D. J., C. R. Hauck, D. Ilic, C. K. Klingbeil, E. Schaefer, C. H. Damsky, and D. D. Schlaepfer. 2000. FAK integrates growth-factor and integrin signals to promote cell migration. Nat. Cell Biol. 2:249–256.
  • Sime, P. J. 2008. The antifibrogenic potential of PPARgamma ligands in pulmonary fibrosis. J. Investig. Med. 56:534–538.
  • Singh, A. B., and R. C. Harris. 2004. Epidermal growth factor receptor activation differentially regulates claudin expression and enhances transepithelial resistance in Madin-Darby canine kidney cells. J. Biol. Chem. 279:3543–3552.
  • Soldi, R., S. Mitola, M. Strasly, P. Defilippi, G. Tarone, and F. Bussolino. 1999. Role of alphavbeta3 integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J. 18:882–892.
  • Tencer, L., E. Burgermeister, M. P. Ebert, and M. Liscovitch. 2008. Rosiglitazone induces caveolin-1 by PPARgamma-dependent and PPRE-independent mechanisms: the role of EGF receptor signaling and its effect on cancer cell drug resistance. Anticancer Res. 28:895–906.
  • Terzi, F., M. Burtin, M. Hekmati, P. Federici, G. Grimber, P. Briand, and G. Friedlander. 2000. Targeted expression of a dominant-negative EGF-R in the kidney reduces tubulo-interstitial lesions after renal injury. J. Clin. Invest. 106:225–234.
  • Thomas, C. M., and E. J. Smart. 2008. Caveolae structure and function. J. Cell. Mol. Med. 12:796–809.
  • Tourkina, E., P. Gooz, J. Pannu, M. Bonner, D. Scholz, S. Hacker, R. M. Silver, M. Trojanowska, and S. Hoffman. 2005. Opposing effects of protein kinase Calpha and protein kinase Cepsilon on collagen expression by human lung fibroblasts are mediated via MEK/ERK and caveolin-1 signaling. J. Biol. Chem. 280:13879–13887.
  • Upla, P., V. Marjomaki, P. Kankaanpaa, J. Ivaska, T. Hyypia, F. G. Van Der Goot, and J. Heino. 2004. Clustering induces a lateral redistribution of alpha 2 beta 1 integrin from membrane rafts to caveolae and subsequent protein kinase C-dependent internalization. Mol. Biol. Cell 15:625–636.
  • van den Heuvel, A. P., A. Schulze, and B. M. Burgering. 2005. Direct control of caveolin-1 expression by FOXO transcription factors. Biochem. J. 385:795–802.
  • Wang, X. M., Y. Zhang, H. P. Kim, Z. Zhou, C. A. Feghali-Bostwick, F. Liu, E. Ifedigbo, X. Xu, T. D. Oury, N. Kaminski, and A. M. Choi. 2006. Caveolin-1: a critical regulator of lung fibrosis in idiopathic pulmonary fibrosis. J. Exp. Med. 203:2895–2906.
  • Wang, X. Q., P. Sun, and A. S. Paller. 2002. Ganglioside induces caveolin-1 redistribution and interaction with the epidermal growth factor receptor. J. Biol. Chem. 277:47028–47034.
  • Wang, X. Q., Q. Yan, P. Sun, J. W. Liu, L. Go, S. M. McDaniel, and A. S. Paller. 2007. Suppression of epidermal growth factor receptor signaling by protein kinase C-alpha activation requires CD82, caveolin-1, and ganglioside. Cancer Res. 67:9986–9995.
  • Wang, Z., J. K. Chen, S. W. Wang, G. Moeckel, and R. C. Harris. 2003. Importance of functional EGF receptors in recovery from acute nephrotoxic injury. J. Am. Soc. Nephrol. 14:3147–3154.
  • Werner, E., and Z. Werb. 2002. Integrins engage mitochondrial function for signal transduction by a mechanism dependent on Rho GTPases. Eur. J. Cell Biol. 158:357–368.
  • Woodard, A. S., G. Garcia-Cardena, M. Leong, J. A. Madri, W. C. Sessa, and L. R. Languino. 1998. The synergistic activity of alphavbeta3 integrin and PDGF receptor increases cell migration. J. Cell Sci. 111:469–478.
  • Zent, R., X. Yan, Y. Su, B. G. Hudson, D. B. Borza, G. W. Moeckel, Z. Qi, Y. Sado, M. D. Breyer, P. Voziyan, and A. Pozzi. 2006. Glomerular injury is exacerbated in diabetic integrin alpha1-null mice. Kidney Int. 70:460–470.
  • Zhang, B., F. Peng, D. Wu, A. J. Ingram, B. Gao, and J. C. Krepinsky. 2007. Caveolin-1 phosphorylation is required for stretch-induced EGFR and Akt activation in mesangial cells. Cell. Signal. 19:1690–1700.
  • Zhang, G. Y., C. G. Yi, X. Li, B. Ma, Z. J. Li, X. L. Chen, S. Z. Guo, and W. Y. Gao. 2009. Troglitazone suppresses transforming growth factor-beta1-induced collagen type I expression in keloid fibroblasts. Br. J. Dermatol. 160:762–770.

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