Integrin-mediated type II TGF-β receptor tyrosine dephosphorylation controls SMAD-dependent profibrotic signaling

Journal of Clinical Investigation

Volumn 124, Issue 8, 2014, Pages 3295-3310

  Chen, Xiwu ^a   Wang, Hongtao ^a,b   Liao, Hong Jun ^a   Hu, Wen ^a   Gewin, Leslie ^a,c   Mernaugh, Glenda ^a   Zhang, Sheng ^d   Zhang, Zhong Yin ^d   Vega Montoto, Lorenzo ^a   Vanacore, Roberto M ^a   Fässler, Reinhard ^e   Zent, Roy ^a,c   Pozzi, Ambra ^a,c  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d INDIANA UNIVERSITY   (United States)

^e MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRIN; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 2; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA2; TYROSINE; VERY LATE ACTIVATION ANTIGEN 1; ALPHA1 INTEGRIN; COLLAGEN; PROTEIN SERINE THREONINE KINASE; SMAD2 PROTEIN; SMAD2 PROTEIN, MOUSE; SMAD3 PROTEIN; SMAD3 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR-BETA TYPE II RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHOSPHORYLATION; CONTROLLED STUDY; CROSS LINKING; DEPHOSPHORYLATION; KIDNEY FIBROSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; URETER OBSTRUCTION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CHEMISTRY; EPITHELIAL MESENCHYMAL TRANSITION; FIBROSIS; GENETICS; KIDNEY; KNOCKOUT MOUSE; MALE; METABOLISM; PATHOLOGY; PHOSPHORYLATION;

ANIMALS; COLLAGEN; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROSIS; INTEGRIN ALPHA1; INTEGRIN ALPHA1BETA1; KIDNEY; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 2; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMAD PROTEINS; SMAD2 PROTEIN; SMAD3 PROTEIN; TYROSINE; URETERAL OBSTRUCTION;

EID: 84905460014     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI71668     Document Type: Article

References (57)

1. Pozzi A, Voziyan PA, Hudson BG, Zent R. Regulation of matrix synthesis, remodeling and accumulation in glomerulosclerosis. Curr Pharm Des. 2009;15(12):1318-1333.
2. Pozzi AI, Zent R. Integrins in kidney disease. J Am Soc Nephrol. 2013;24(7):1034-1039.
3. Xu P, Liu J, Derynck R. Post-translational regulation of TGF-beta receptor and Smad signaling. FEBS Lett. 2012;586(14):1871-1884.
4. Massague J, Xi Q. TGF-β control of stem cell differentiation genes. FEBS Lett. 2012;586(14):1953-1958.
5. Luo K, Lodish HF. Positive and negative regulation of type II TGF-β receptor signal transduction by autophosphorylation on multiple serine residues. EMBO J. 1997;16(8):1970-1981.
6. Lawler S, et al. The type II transforming growth factor-β receptor autophosphorylates not only on serine and threonine but also on tyrosine residues. J Biol Chem. 1997;272(23):14850-14859.
7. Galliher AJ, Schiemann WP. Src phosphorylates Tyr284 in TGF-beta type II receptor and regulates TGF-β stimulation of p38 MAPK during breast cancer cell proliferation and invasion. Cancer Res. 2007;67(8):3752-3758.
8. Harburger DS, Calderwood DA. Integrin signalling at a glance. J Cell Sci. 2009;122(pt 2):159-163.
9. Moser M, Legate KR, Zent R, Fassler R. The tail of integrins, talin, and kindlins. Science. 2009;324(5929):895-899.
10. Borza CM, Pozzi A. The role of cell-extracellular matrix interactions in glomerular injury. Exp Cell Res. 2012;318(9):1001-1010.
11. Munger JS, et al. The integrin alpha v beta 6 binds and activates latent TGF β 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell. 1999;96(3):319-328.
12. Mu D, et al. The integrin α (v) β8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-β1. J Cell Biol. 2002;157(3):493-507.
13. Khan S, et al. Mesangial cell integrin alphavbeta8 provides glomerular endothelial cell cytoprotection by sequestering TGF-β and regulating PECAM-1. Am J Pathol. 2011;178(2):609-620.
14. Hayashida T, Jones JC, Lee CK, Schnaper HW. Loss of beta1-integrin enhances TGF-β1-induced collagen expression in epithelial cells via increased αvβ3-integrin and Rac1 activity. J Biol Chem. 2010;285(40):30741-30751.
15. Girgert R, et al. Integrin α2-deficient mice provide insights into specific functions of collagen receptors in the kidney. Fibrogenesis Tissue Repair. 2010;3:19.
16. Galliher AJ, Schiemann WP. β3 integrin and Src facilitate transforming growth factor-β mediated induction of epithelial-mesenchymal transition in mammary epithelial cells. Breast Cancer Res. 2006;8(4):R42.
17. Gewin L, Zent R. How does TGF-β mediate tubulointerstitial fibrosis? Semin Nephrol. 2012;32(3):228-235.
18. Ma LJ, et al. Transforming growth factor-β-dependent and -independent pathways of induction of tubulointerstitial fibrosis in β6 (-/-) mice. Am J Pathol. 2003;163(4):1261-1273.
19. Zhang X, et al. β1 integrin is necessary for ureteric bud branching morphogenesis and maintenance of collecting duct structural integrity. Development. 2009;136(19):3357-3366.
20. Chen D, et al. Differential expression of collagenand laminin-binding integrins mediates ureteric bud and inner medullary collecting duct cell tubulogenesis. Am J Physiol Renal Physiol. 2004;287(4):F602-F611.
21. Chen X, et al. Lack of integrin alpha1beta1 leads to severe glomerulosclerosis after glomerular injury. Am J Pathol. 2004;165(2):617-630.
22. Gardner H, Broberg A, Pozzi A, Laato M, Heino J. Absence of integrin α1β1 in the mouse causes loss of feedback regulation of collagen synthesis in normal and wounded dermis. J Cell Sci. 1999;112(pt 3):263-272.
23. Zent R, et al. Glomerular injury is exacerbated in diabetic integrin α1-null mice. Kidney Int. 2006;70(3):460-470.
24. Borza CM, et al. Integrin α1β1 promotes caveolin-1 dephosphorylation by activating T cell protein-tyrosine phosphatase. J Biol Chem. 2010;285(51):40114-40124.
25. Chen X, et al. Integrin α1β1 controls reactive oxygen species synthesis by negatively regulating epidermal growth factor receptor-mediated Rac activation. Mol Cell Biol. 2007;27(9):3313-3326.
26. Chen X, et al. Integrin α1β1 regulates epidermal growth factor receptor activation by controlling peroxisome proliferator-activated receptor γ-dependent caveolin-1 expression. Mol Cell Biol. 2010;30(12):3048-3058.
27. Postigo AA. Opposing functions of ZEB proteins in the regulation of the TGFβ/BMP signaling pathway. EMBO J. 2003;22(10):2443-2452.
28. Xiong M, et al. The miR-200 family regulates TGF-β1-induced renal tubular epithelial to mesenchymal transition through Smad pathway by targeting ZEB1 and ZEB2 expression. Am J Physiol Renal Physiol. 2012;302(3):F369-F379.
29. Xu J, Lamouille S, Derynck R. TGF-β-induced epithelial to mesenchymal transition. Cell Res. 2009;19(2):156-172.
30. Sato M, Muragaki Y, Saika S, Roberts AB, Ooshima A. Targeted disruption of TGF-β1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J Clin Invest. 2003;112(10):1486-1494.
31. Mattila E, Pellinen T, Nevo J, Vuoriluoto K, Arjonen A, Ivaska J. Negative regulation of EGFR signalling through integrin-α1β1-mediated activation of protein tyrosine phosphatase TCPTP. Nat Cell Biol. 2005;7(1):78-85.
32. Mattila E, Auvinen K, Salmi M, Ivaska J. The protein tyrosine phosphatase TCPTP controls VEGFR2 signalling. J Cell Sci. 2008;121(pt 21):3570-3580.
33. Mattila E, et al. Inhibition of receptor tyrosine kinase signalling by small molecule agonist of T-cell protein tyrosine phosphatase. BMC Cancer. 2010;10:7.
34. Zhang S, Chen L, Luo Y, Gunawan A, Lawrence DS, Zhang ZY. Acquisition of a potent and selective TCPTP inhibitor via a stepwise fluorophore-tagged combinatorial synthesis and screening strategy. J Am Chem Soc. 2009;131(36):13072-13079.
35. Krieglstein CF, et al. Collagen-binding integrin α1β1 regulates intestinal inflammation in experimental colitis. J Clin Invest. 2002;110(12):1773-1782.
36. Becker HM, et al. α1β1 integrin-mediated adhesion inhibits macrophage exit from a peripheral inflammatory lesion. J Immunol. 2013;190(8):4305-4314.
37. Zhu S, et al. Spermine protects mice against lethal sepsis partly by attenuating surrogate inflammatory markers. Mol Med. 2009;15(7-8):275-282.
38. Meng XM, Chung AC, Lan HY. Role of the TGF-β/BMP-7/Smad pathways in renal diseases. Clin Sci (Lond). 2013;124(4):243-254.
39. Carthy JM, Garmaroudi FS, Luo Z, McManus BM. Wnt3a induces myofibroblast differentiation by upregulating TGF-β signaling through SMAD2 in a beta-catenin-dependent manner. PLoS One. 2011;6(5):e19809.
40. Ren M, et al. Smad2 and Smad3 as mediators of the response of adventitial fibroblasts induced by transforming growth factor β1. Mol Med Report. 2011;4(3):561-567.
41. Zhong X, Chung AC, Chen HY, Meng XM, Lan HY. Smad3-mediated upregulation of miR-21 promotes renal fibrosis. J Am Soc Nephrol. 2011;22(9):1668-1681.
42. Gewin L, et al. TGF-β receptor deletion in the renal collecting system exacerbates fibrosis. J Am Soc Nephrol. 2010;21(8):1334-1343.
43. Liu T, Feng XH. Regulation of TGF-β signalling by protein phosphatases. Biochem J. 2010;430(2):191-198.
44. Bennett D, Alphey L. PP1 binds Sara and negatively regulates Dpp signaling in Drosophila melanogaster. Nat Genet. 2002;31(4):419-423.
45. Tang WB, Ling GH, Sun L, Liu FY. Smad anchor for receptor activation (SARA) in TGF-beta signaling. Front Biosci (Elite Ed). 2010;2:857-860.
46. Heikkinen PT, et al. Hypoxia-activated Smad3-specific dephosphorylation by PP2A. J Biol Chem. 2010;285(6):3740-3749.
47. Yu J, et al. MTMR4 attenuates transforming growth factor beta (TGFβ) signaling by dephos dephosphorylating R-Smads in endosomes. J Biol Chem. 2010;285(11):8454-8462.
48. Lin X, et al. PPM1A functions as a Smad phosphatase to terminate TGFβ signaling. Cell. 2006;125(5):915-928.
49. Lorenzen JA, Dadabay CY, Fischer EH. COOHterminal sequence motifs target the T cell protein tyrosine phosphatase to the ER and nucleus. J Cell Biol. 1995;131(3):631-643.
50. Lam MH, Michell BJ, Fodero-Tavoletti MT, Kemp BE, Tonks NK, Tiganis T. Cellular stress regulates the nucleocytoplasmic distribution of the protein-tyrosine phosphatase TCPTP. J Biol Chem. 2001;276(40):37700-37707.
51. Soda K, Kano Y, Chiba F, Koizumi K, Miyaki Y. Increased polyamine intake inhibits age-associated alteration in global DNA methylation and 1, 2-dimethylhydrazine-induced tumorigenesis. PLoS One. 2013;8(5):e64357.
52. Soda K, Kano Y, Chiba F. Food polyamine and cardiovascular disease - an epidemiological study. Glob J Health Sci. 2012;4(6):170-178.
53. Goek ON, et al. Metabolites associate with kidney function decline and incident chronic kidney disease in the general population. Nephrol Dial Transplant. 2013;28(8):2131-2138.
54. Gardner H, Kreidberg J, Koteliansky V, Jaenisch R. Deletion of integrin α 1 by homologous recombination permits normal murine development but gives rise to a specific deficit in cell adhesion. Dev Biol. 1996;175(2):301-313.
55. Shi M, et al. Enhancing integrin α1 inserted (I) domain affinity to ligand potentiates integrin α1β1-mediated down-regulation of collagen synthesis. J Biol Chem. 2012;287(42):35139-35152.
56. Yamashita M, Fatyol K, Jin C, Wang X, Liu Z, Zhang YE. TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-β. Mol Cell. 2008;31(6):918-924.
57. Abe M, Harpel JG, Metz CN, Nunes I, Loskutoff DJ, Rifkin DB. An assay for transforming growth factor-β using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal Biochem. 1994;216(2):276-284.