Necrotic renal epithelial cell inhibits renal interstitial fibroblast activation: Role of protein tyrosine phosphatase 1B

American Journal of Physiology - Renal Physiology

Volumn 304, Issue 6, 2013, Pages

  Ponnusamy, Murugavel ^a   Ma, Li ^a   Zhuang, Shougang ^a,b  

^a BROWN UNIVERSITY   (United States)

^b TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

EGFR; PTP1B; Renal epithelial cells; Renal interstitial fibroblasts

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBRONECTIN; GEFITINIB; MITOGEN ACTIVATED PROTEIN KINASE 1; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN KINASE B; PROTEIN TYROSINE PHOSPHATASE 1B; SMALL INTERFERING RNA; STAT3 PROTEIN; VANADATE SODIUM; EGFR PROTEIN, RAT; PTPN1 PROTEIN, RAT; PURINERGIC P2X7 RECEPTOR; STAT3 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL CULTURE; CELL DEATH; CONTROLLED STUDY; EPITHELIUM CELL; FIBROBLAST; GENE SILENCING; IN VITRO STUDY; INCUBATION TIME; KIDNEY EPITHELIUM; KIDNEY INTERSTITIUM; KIDNEY NECROSIS; KIDNEY PROXIMAL TUBULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SUPERNATANT; ACUTE KIDNEY FAILURE; ANIMAL; CELL LINE; CELL PROLIFERATION; ENZYMOLOGY; KIDNEY; METABOLISM; MYOFIBROBLAST; NECROSIS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACUTE KIDNEY INJURY; ANIMALS; CELL LINE; CELL PROLIFERATION; KIDNEY; KIDNEY TUBULES, PROXIMAL; MICE; MYOFIBROBLASTS; NECROSIS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 1; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, PURINERGIC P2X7; STAT3 TRANSCRIPTION FACTOR;

MLCS; MLOWN;

EID: 84877929839     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00564.2012     Document Type: Article

References (49)

1. Asada N, Takase M, Nakamura J, Oguchi A, Asada M, Suzuki N, Yamamura K, Nagoshi N, Shibata S, Rao TN, Fehling HJ, Fukatsu A, Minegishi N, Kita T, Kimura T, Okano H, Yamamoto M, Yanagita M. Dysfunction of fibroblasts of extrarenal origin underlies renal fibrosis and renal anemia in mice. J Clin Invest 121: 3981-3990, 2011.
2. Bachmann S, Le Hir M, Eckardt KU. Co-localization of erythropoietin mRNA and ecto-5'-nucleotidase immunoreactivity in peritubular cells of rat renal cortex indicates that fibroblasts produce erythropoietin. J His-tochem Cytochem 41: 335-341, 1993.
3. Bonner JC. Regulation of PDGF and its receptors in fibrotic diseases. Cytokine Growth Factor Rev 15: 255-273, 2004.
4. Bourdeau A, Dube N, Tremblay ML. Cytoplasmic protein tyrosine phosphatases, regulation and function: the roles of PTP1B and TC-PTP. Curr Opin Cell Biol 17: 203-209, 2005.
5. Chang Y, Ceacareanu B, Zhuang D, Zhang C, Pu Q, Ceacareanu AC, Hassid A. Counterregulatory function of protein tyrosine phosphatase 1B in platelet-derived growth factor- or fibroblast growth factor-induced motility and proliferation of cultured smooth muscle cells and in neointima formation. Arterioscler Thromb Vasc Biol 26: 501-507, 2006.
6. Chen SC, Guh JY, Lin TD, Chiou SJ, Hwang CC, Ko YM, Chuang LY. Gefitinib attenuates transforming growth factor-beta1-activated mi-togen-activated protein kinases and mitogenesis in NRK-49F cells. Transl Res 158: 214-224, 2011.
7. Docherty NG, O'Sullivan OE, Healy DA, Murphy M, O'Neill AJ, Fitzpatrick JM, Watson RW. TGF-fj1-induced EMT can occur independently of its proapoptotic effects and is aided by EGF receptor activation. Am J Physiol Renal Physiol 290: F1202-F1212, 2006.
8. Eden ER, White IJ, Tsapara A, Futter CE. Membrane contacts between endosomes and ER provide sites for PTP1B-epidermal growth factor receptor interaction. Nat Cell Biol 12: 267-272, 2010.
9. Erslev AJ, Besarab A. Erythropoietin in the pathogenesis and treatment of the anemia of chronic renal failure. Kidney Int 51: 622-630, 1997.
10. Fagone E, Conte E, Gili E, Fruciano M, Pistorio MP, Lo Furno D, Giuffrida R, Crimi N, Vancheri C. Resveratrol inhibits transforming growth factor-beta-induced proliferation and differentiation of ex vivo human lung fibroblasts into myofibroblasts through ERK/Akt inhibition and PTEN restoration. Exp Lung Res 37: 162-174, 2011.
11. Floege J, Eitner F, Alpers CE. A new look at platelet-derived growth factor in renal disease. J Am Soc Nephrol 19: 12-23, 2008.
12. Fougeray S, Bouvier N, Beaune P, Legendre C, Anglicheau D, Thervet E, Pallet N. Metabolic stress promotes renal tubular inflammation by triggering the unfolded protein response. Cell Death Dis 2: e143, 2011.
13. Fujigaki Y, Muranaka Y, Sun D, Goto T, Zhou H, Sakakima M, Fukasawa H, Yonemura K, Yamamoto T, Hishida A. Transient myofibroblast differentiation of interstitial fibroblastic cells relevant to tubular dilatation in uranyl acetate-induced acute renal failure in rats. Virchows Arch 446: 164-176, 2005.
14. Gobeil S, Boucher CC, Nadeau D, Poirier GG. Characterization of the necrotic cleavage of poly(ADP-ribose) polymerase (PARP-1): implication of lysosomal proteases. Cell Death Differ 8: 588-594, 2001.
15. Gu F, Dube N, Kim JW, Cheng A, Ibarra-Sanchez MJ, Tremblay ML, Boisclair YR. Protein tyrosine phosphatase 1B attenuates growth hormone-mediated JAK2-STAT signaling. Mol Cell Biol 23: 3753-3762, 2003.
16. Haj FG, Markova B, Klaman LD, Bohmer FD, Neel BG. Regulation of receptor tyrosine kinase signaling by protein tyrosine phosphatase-1B. J Biol Chem 278: 739-744, 2003.
17. Ito Y, Banno R, Hagimoto S, Ozawa Y, Arima H, Oiso Y. TNFalpha increases hypothalamic PTP1B activity via the NFkappaB pathway in rat hypothalamic organotypic cultures. Regul Pept 174: 58-64, 2012.
18. Kaissling B, Le Hir M. The renal cortical interstitium: morphological and functional aspects. Histochem Cell Biol 130: 247-262, 2008.
19. Lautrette A, Li S, Alili R, Sunnarborg SW, Burtin M, Lee DC, Friedlander G, Terzi F. Angiotensin II and EGF receptor cross-talk in chronic kidney diseases: a new therapeutic approach. Nat Med 11: 867-874, 2005.
20. LeBleu VS, Kalluri R. Blockade of PDGF receptor signaling reduces myofibroblast number and attenuates renal fibrosis. Kidney Int 80: 1119 - 1121, 2011.
21. Liu F, Chernoff J. Protein tyrosine phosphatase 1B interacts with and is tyrosine phosphorylated by the epidermal growth factor receptor. Biochem J 327: 139-145, 1997.
22. Liu N, Guo JK, Pang M, Tolbert E, Ponnusamy M, Gong R, Bayliss G, Dworkin LD, Yan H, Zhuang S. Genetic or pharmacologic blockade of EGFR inhibits renal fibrosis. J Am Soc Nephrol 23: 854-867, 2012.
23. Lo HW, Hsu SC, Xia W, Cao X, Shih JY, Wei Y, Abbruzzese JL, Hortobagyi GN, Hung MC. Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via upregulation of TWIST gene expression. Cancer Res 67: 9066-9076, 2007.
24. Ludewig D, Kosmehl H, Sommer M, Bohmer FD, Stein G. PDGF receptor kinase blocker AG1295 attenuates interstitial fibrosis in rat kidney after unilateral obstruction. Cell Tissue Res 299: 97-103, 2000.
25. Maxwell PH, Ferguson DJ, Nicholls LG, Johnson MH, Ratcliffe PJ. The interstitial response to renal injury: fibroblast-like cells show pheno-typic changes and have reduced potential for erythropoietin gene expression. Kidney Int 52: 715-724, 1997.
26. Meldrum KK, Meldrum DR, Hile KL, Yerkes EB, Ayala A, Cain MP, Rink RC, Casale AJ, Kaefer MA. p38 MAPK mediates renal tubular cell TNF-a production and TNF-a-dependent apoptosis during simulated ischemia. Am J Physiol Cell Physiol 281: C563-C570, 2001.
27. Melenhorst WB, Mulder GM, Xi Q, Hoenderop JG, Kimura K, Eguchi S, van Goor H. Epidermal growth factor receptor signaling in the kidney: key roles in physiology and disease. Hypertension 52: 987-993, 2008.
28. Meng LQ, Tang JW, Wang Y, Zhao JR, Shang MY, Zhang M, Liu SY, Qu L, Cai SQ, Li XM. Astragaloside IV synergizes with ferulic acid to inhibit renal tubulointerstitial fibrosis in rats with obstructive nephropathy. Br J Pharmacol 162: 1805-1818, 2011.
29. Meran S, Steadman R. Fibroblasts and myofibroblasts in renal fibrosis. Int J Exp Pathol 92: 158-167, 2011.
30. Nieto-Vazquez I, Fernandez-Veledo S, de Alvaro C, Lorenzo M. Dual role of interleukin-6 in regulating insulin sensitivity in murine skeletal muscle. Diabetes 57: 3211-3221, 2008.
31. Nieto-Vazquez I, Fernandez-Veledo S, de Alvaro C, Rondinone CM, Valverde AM, Lorenzo M. Protein-tyrosine phosphatase 1B-deficient myocytes show increased insulin sensitivity and protection against tumor necrosis factor-alpha-induced insulin resistance. Diabetes 56: 404-413, 2007.
32. Pang M, Kothapally J, Mao H, Tolbert E, Ponnusamy M, Chin YE, Zhuang S. Inhibition of histone deacetylase activity attenuates renal fibroblast activation and interstitial fibrosis in obstructive nephropathy. Am J Physiol Renal Physiol 297: F996-F1005, 2009.
33. Pang M, Ma L, Gong R, Tolbert E, Mao H, Ponnusamy M, Chin YE, Yan H, Dworkin LD, Zhuang S. A novel STAT3 inhibitor, S3I-201, attenuates renal interstitial fibroblast activation and interstitial fibrosis in obstructive nephropathy. Kidney Int 78: 257-268, 2010.
34. Ponnusamy M, Liu N, Gong R, Yan H, Zhuang S. ERK pathway mediates P2X7 expression and cell death in renal interstitial fibroblasts exposed to necrotic renal epithelial cells. Am J Physiol Renal Physiol 301: F650-F659, 2011.
35. Ponnusamy M, Liu N, Sellamuthu R, Zhao TC, Mao H, Zhuang S. Autophagy protects against necrotic renal epithelial cell-induced death of renal interstitial fibroblasts. Am J Physiol Renal Physiol 303: F83-F91, 2012.
36. Ponnusamy M, Ma L, Gong R, Pang M, Chin YE, Zhuang S. P2X7 receptors mediate deleterious renal epithelial-fibroblast cross talk. Am J Physiol Renal Physiol 300: F62-F70, 2011.
37. Qu X, Zhang X, Yao J, Song J, Nikolic-Paterson DJ, Li J. Resolvins E1 and D1 inhibit interstitial fibrosis in the obstructed kidney via inhibition of local fibroblast proliferation. J Pathol 228: 506-519, 2012.
38. Sorenson CM, Sheibani N. Altered regulation of SHP-2 and PTP 1B tyrosine phosphatases in cystic kidneys from bcl-2 -/- mice. Am J Physiol Renal Physiol 282: F442-F450, 2002.
39. Terzi F, Burtin M, Hekmati M, Federici P, Grimber G, Briand P, Friedlander G. Targeted expression of a dominant-negative EGF-R in the kidney reduces tubulo-interstitial lesions after renal injury. J Clin Invest 106: 225-234, 2000.
40. Thurman JM. Triggers of inflammation after renal ischemia/reperfusion. Clin Immunol 123: 7-13, 2007.
41. Tiganis T. Protein tyrosine phosphatases: dephosphorylating the epidermal growth factor receptor. IUBMB Life 53: 3-14, 2002.
42. van Kooten C, Daha MR. Cytokine cross-talk between tubular epithelial cells and interstitial immunocompetent cells. Curr Opin Nephrol Hyper-tens 10: 55-59, 2001.
43. van Kooten C, Daha MR, van Es LA. Tubular epithelial cells: a critical cell type in the regulation of renal inflammatory processes. Exp Nephrol 7: 429-437, 1999.
44. Wang WQ, Sun JP, Zhang ZY. An overview of the protein tyrosine phosphatase superfamily. Curr Top Med Chem 3: 739-748, 2003.
45. Wen LT, Caldwell CC, Knowles AF. Poly(ADP-ribose) polymerase activation and changes in Bax protein expression associated with extracellular ATP-mediated apoptosis in human embryonic kidney 293-P2X7 cells. Mol Pharmacol 63: 706-713, 2003.
46. Yang L, Besschetnova TY, Brooks CR, Shah JV, Bonventre JV. Epithelial cell cycle arrest in G2/M mediates kidney fibrosis after injury. Nat Med 16: 535-543, 2010.
47. Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2: 127-137, 2001.
48. Zabolotny JM, Kim YB, Welsh LA, Kershaw EE, Neel BG, Kahn BB. Protein-tyrosine phosphatase 1B expression is induced by inflammation in vivo. J Biol Chem 283: 14230-14241, 2008.
49. Zhang ZY. Mechanistic studies on protein tyrosine phosphatases. Prog Nucleic Acid Res Mol Biol 73: 171-220, 2003.