Pressure activates epidermal growth factor receptor leading to the induction of iNOS via NFκB and STAT3 in human proximal tubule cells

American Journal of Physiology - Renal Physiology

Volumn 297, Issue 1, 2009, Pages

  Broadbelt, Nalini V ^a   Chen, Jie ^a   Silver, Randi B ^a   Poppas, Dix P ^a   Felsen, Diane ^a  

^a WEILL CORNELL MEDICAL CENTER   (United States)

Author keywords

Cycloheximide; Cytokine mix

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; PROTEIN INHIBITOR; STAT3 PROTEIN; SYNAPTOTAGMIN I;

ARTICLE; CELL STRAIN; CELL STRAIN HKC 8; CONTROLLED STUDY; GENE EXPRESSION; GENE INDUCTION; HUMAN; HUMAN CELL; HYPERBARISM; KIDNEY PROXIMAL TUBULE; PRESSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; URETER OBSTRUCTION;

EID: 67650660035     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.90752.2008     Document Type: Article

References (63)

1. Bhat NR, Feinstein DL, Shen Q, Bhat AN. p38 MAPK-mediated transcriptional activation of inducible nitric-oxide synthase in glial cells. Roles of nuclear factors, nuclear factor-κB, cAMP response elementbinding protein, CCAAT/enhancer-binding protein-β, and activating transcription factor-2. J Biol Chem 277: 29584-29592, 2002.
2. Bild AH, Turkson J, Jove R. Cytoplasmic transport of Stat3 by receptormediated endocytosis. EMBO J 21: 3255-3263, 2002.
3. Bor MV, Shi Y, Sorensen BS, Wen JG, Frokiaer J, Djurhuus JC, Nexo E. Increased TGF-α and EGF receptor mRNA expression in response to neonatal unilateral partial ureter obstruction in rats. Nephron Exp Nephrol 104: e76-e82, 2006.
4. Broadbelt NV, Stahl PJ, Chen J, Mizrahi M, Lal A, Bozkurt A, Poppas DP, Felsen D. Early upregulation of iNOS mRNA expression and increase in NO metabolites in pressurized renal epithelial cells. Am J Physiol Renal Physiol 293: F1877-F1888, 2007.
5. Burova E, Vassilenko K, Dorosh V, Gonchar I, Nikolsky N. Interferon-γ-dependent transactivation of epidermal growth factor receptor. FEBS Lett 581: 1475-1480, 2007.
6. Chen CF, Yeh SU, Chien CT, Wu MS. Renal response during acute unilateral ureteral obstruction in rats. Neurourol Urodyn 20: 125-137, 2001.
7. Chertin B, Rolle U, Solari V, Cascio S, Puri P. The role of nitric oxide in bladder urothelial injury after bladder outlet obstruction. BJU Int 94: 392-399, 2004.
8. Chevalier RL. Molecular and cellular pathophysiology of obstructive nephropathy. Pediatr Nephrol 13: 612-619, 1999.
9. Chevalier RL. Obstructive nephropathy: lessons from cystic kidney disease. Nephron 84: 6-12, 2000.
10. Chevalier RL. Pathogenesis of renal injury in obstructive uropathy. Curr Opin Pediatr 18: 153-160, 2006.
11. Coffer PJ, Kruijer W. EGF receptor deletions define a region specifically mediating STAT transcription factor activation. Biochem Biophys Res Commun 210: 74-81, 1995.
12. Cohen S, Fava RA. Internalization of functional epidermal growth factor: receptor/kinase complexes in A-431 cells. J Biol Chem 260: 12351-12358, 1985.
13. David M, Wong L, Flavell R, Thompson SA, Wells A, Larner AC, Johnson GR. STAT activation by epidermal growth factor (EGF) and amphiregulin. Requirement for the EGF receptor kinase but not for tyrosine phosphorylation sites or JAK1. J Biol Chem 271: 9185-9188, 1996.
14. Felsen D, Schulsinger D, Gross SS, Kim FY, Marion D, Vaughan ED Jr. Renal hemodynamic and ureteral pressure changes in response to ureteral obstruction: the role of nitric oxide. J Urol 169: 373-376, 2003.
15. Fermor B, Weinberg JB, Pisetsky DS, Misukonis MA, Banes AJ, Guilak F. The effects of static and intermittent compression on nitric oxide production in articular cartilage explants. J Orthop Res 19: 729-737, 2001.
16. Fitzgerald J, Chou SY, Wahid A, Porush JG. Regional expression of inducible nitric oxide synthase in the kidney in dogs with unilateral ureteral obstruction. J Urol 166: 1524-1529, 2001.
17. Ganster RW, Guo Z, Shao L, Geller DA. Differential effects of TNF-α and IFN-γ on gene transcription mediated by NF-κB-Stat1 interactions. J Interferon Cytokine Res 25: 707-719, 2005.
18. Gesualdo L, Di Paolo S, Calabro A, Milani S, Maiorano E, Ranieri E, Pannarale G, Schena FP. Expression of epidermal growth factor and its receptor in normal and diseased human kidney: an immunohistochemical and in situ hybridization study. Kidney Int 49: 656-665, 1996.
19. Giulietti A, Overbergh L, Valckx D, Decallonne B, Bouillon R, Mathieu C. An overview of real-time quantitative PCR: applications to quantify cytokine gene expression. Methods 25: 386-401, 2001.
20. Habib AA, Chatterjee S, Park SK, Ratan RR, Lefebvre S, Vartanian T. The epidermal growth factor receptor engages receptor interacting protein and nuclear factor-κB (NF-κB)-inducing kinase to activate NF-κB. Identification of a novel receptor-tyrosine kinase signalosome. J Biol Chem 276: 8865-8874, 2001.
21. Harada S, Nakata T, Oguni A, Kido H, Hatta T, Fukuyama R, Fushiki S, Sasaki S, Takeda K. Contrasting effects of angiotensin type 1 and 2 receptors on nitric oxide release under pressure. Hypertens Res 25: 779-786, 2002.
22. Haussler U, von Wichert G, Schmid RM, Keller F, Schneider G. Epidermal growth factor activates nuclear factor-κB in human proximal tubule cells. Am J Physiol Renal Physiol 289: F808-F815, 2005.
23. Hegarty NJ, Watson RW, Young LS, O'Neill AJ, Brady HR, Fitzpatrick JM. Cytoprotective effects of nitrates in a cellular model of hydronephrosis. Kidney Int 62: 70-77, 2002.
24. Hegarty NJ, Young LS, Kirwan CN, O'Neill AJ, Bouchier-Hayes DM, Sweeney P, Watson RW, Fitzpatrick JM. Nitric oxide in unilateral ureteral obstruction: effect on regional renal blood flow. Kidney Int 59: 1059-1065, 2001.
25. Hirota K, Murata M, Itoh T, Yodoi J, Fukuda K. Redox-sensitive transactivation of epidermal growth factor receptor by tumor necrosis factor confers the NF-κB activation. J Biol Chem 276: 25953-25958, 2001.
26. Islam N, Haqqi TM, Jepsen KJ, Kraay M, Welter JF, Goldberg VM, Malemud CJ. Hydrostatic pressure induces apoptosis in human chondrocytes from osteoarthritic cartilage through up-regulation of tumor necrosis factor-α, inducible nitric oxide synthase, p53, c-myc, and bax-α, and suppression of bcl-2. J Cell Biochem 87: 266-278, 2002.
27. Ito K, Chen J, Khodadadian JJ, Seshan SV, Eaton C, Zhao X, Vaughan ED Jr, Lipkowitz M, Poppas DP, Felsen D. Liposome-mediated transfer of nitric oxide synthase gene improves renal function in ureteral obstruction in rats. Kidney Int 66: 1365-1375, 2004.
28. Ito K, Chen J, Vaughan, ED Jr, Seshan SV, Poppas DP, Felsen D. Dietary L-arginine supplementation improves the glomerular filtration rate and renal blood flow after 24 h of unilateral ureteral obstruction in rats. J Urol 171: 926-930, 2004.
29. Kiley SC, Thornhill BA, Belyea BC, Neale K, Forbes MS, Luetteke NC, Lee DC, Chevalier RL. Epidermal growth factor potentiates renal cell death in hydronephrotic neonatal mice, but cell survival in rats. Kidney Int 68: 504-514, 2005.
30. Klahr S, Morrissey JJ. The role of growth factors, cytokines, and vasoactive compounds in obstructive nephropathy. Semin Nephrol 18: 622-632, 1998.
31. Kleinert H, Pautz A, Linker K, Schwarz PM. Regulation of the expression of inducible nitric oxide synthase. Eur J Pharmacol 500: 255-266, 2004.
32. Kone BC, Schwobel J, Turner P, Mohaupt MG, Cangro CB. Role of NF-κB in the regulation of inducible nitric oxide synthase in an MTAL cell line. Am J Physiol Renal Fluid Electrolyte Physiol 269: F718-F729, 1995.
33. Kuratsune M, Masaki T, Hirai T, Kiribayashi K, Yokoyama Y, Arakawa T, Yorioka N, Kohno N. Signal transducer and activator of transcription 3 involvement in the development of renal interstitial fibrosis after unilateral ureteral obstruction. Nephrology (Carlton) 12: 565-571, 2007.
34. Lin SY, Makino K, Xia W, Matin A, Wen Y, Kwong KY, Bourguignon L, Hung MC. Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat Cell Biol 3: 802-808, 2001.
35. Liu B, Neufeld AH. Nitric oxide synthase-2 in human optic nerve head astrocytes induced by elevated pressure in vitro. Arch Ophthalmol 119: 240-245, 2001.
36. Liu B, Neufeld AH. Activation of epidermal growth factor receptor signals induction of nitric oxide synthase-2 in human optic nerve head astrocytes in glaucomatous optic neuropathy. Neurobiol Dis 13: 109-123, 2003.
37. Lo HW, Hsu SC, Ali-Seyed M, Gunduz M, Xia W, Wei Y, Bartholomeusz G, Shih JY, Hung MC. Nuclear interaction of EGFR and STAT3 in the activation of the iNOS/NO pathway. Cancer Cell 7: 575-589, 2005.
38. Marks-Konczalik J, Chu SC, Moss J. Cytokine-mediated transcriptional induction of the human inducible nitric oxide synthase gene requires both activator protein 1 and nuclear factor-κB-binding sites. J Biol Chem 273: 22201-22208, 1998.
39. Meldrum KK, Metcalfe P, Leslie JA, Misseri R, Hile KL, Meldrum DR. TNF-α neutralization decreases nuclear factor-κB activation and apoptosis during renal obstruction. J Surg Res 131: 182-188, 2006.
40. Miyajima A, Chen J, Lawrence C, Ledbetter S, Soslow RA, Stern J, Jha S, Pigato J, Lemer ML, Poppas DP, et al. Antibody to transforming growth factor-β ameliorates tubular apoptosis in unilateral ureteral obstruction. Kidney Int 58: 2301-2313, 2000.
41. Morrison JC, Moore CG, Deppmeier LM, Gold BG, Meshul CK, Johnson EC. A rat model of chronic pressure-induced optic nerve damage. Exp Eye Res 64: 85-96, 1997.
42. Morrissey J, Klahr S. Transcription factor NF-κB regulation of renal fibrosis during ureteral obstruction. Semin Nephrol 18: 603- 611, 1998.
43. Neufeld AH, Liu B. Comparison of the signal transduction pathways for the induction of gene expression of nitric oxide synthase-2 in response to two different stimuli. Nitric Oxide 8: 95-102, 2003.
44. Neuvians TP, Gashaw I, Sauer CG, von Ostau C, Kliesch S, Bergmann M, Hacker A, Grobholz R. Standardization strategy for quantitative PCR in human seminoma and normal testis. J Biotechnol 117: 163-171, 2005.
45. Obata H, Biro S, Arima N, Kaieda H, Kihara T, Eto H, Miyata M, Tanaka H. NF-κB is induced in the nuclei of cultured rat aortic smooth muscle cells by stimulation of various growth factors. Biochem Biophys Res Commun 224: 27-32, 1996.
46. Park OK, Schaefer TS, Nathans D. In vitro activation of Stat3 by epidermal growth factor receptor kinase. Proc Natl Acad Sci USA 93: 13704-13708, 1996.
47. Poljakovic M, Nygren JM, Persson K. Signalling pathways regulating inducible nitric oxide synthase expression in human kidney epithelial cells. Eur J Pharmacol 469: 21-28, 2003.
48. Poljakovic M, Svensson L, Persson K. The influence of uropathogenic Escherichia coli and proinflammatory cytokines on the inducible nitric oxide synthase response in human kidney epithelial cells. J Urol 173: 1000-1003, 2005.
49. Rao KM. Molecular mechanisms regulating iNOS expression in various cell types. J Toxicol Environ Health B Crit Rev 3: 27-58, 2000.
50. Shao H, Cheng HY, Cook RG, Tweardy DJ. Identification and characterization of signal transducer and activator of transcription 3 recruitment sites within the epidermal growth factor receptor. Cancer Res 63: 3923-3930, 2003.
51. Shareef S, Sawada A, Neufeld AH. Isoforms of nitric oxide synthase in the optic nerves of rat eyes with chronic moderately elevated intraocular pressure. Invest Ophthalmol Vis Sci 40: 2884-2891, 1999.
52. Sun L, Carpenter G. Epidermal growth factor activation of NF-κB is mediated through IκBα degradation and intracellular free calcium. Oncogene 16: 2095-2102, 1998.
53. Taylor BS, de Vera ME, Ganster RW, Wang Q, Shapiro RA, Morris, SM Jr, Billiar TR, Geller DA. Multiple NF-κB enhancer elements regulate cytokine induction of the human inducible nitric oxide synthase gene. J Biol Chem 273: 15148-15156, 1998.
54. Tschumperlin DJ, Dai G, Maly IV, Kikuchi T, Laiho LH, McVittie AK, Haley KJ, Lilly CM, So PT, Lauffenburger DA, et al. Mechanotransduction through growth-factor shedding into the extracellular space. Nature 429: 83-86, 2004.
55. Unger T. Blood pressure lowering and renin-angiotensin system blockade. J Hypertens Suppl 21: S3-S7, 2003.
56. Valles PG, Pascual L, Manucha W, Carrizo L, Ruttler M. Role of endogenous nitric oxide in unilateral ureteropelvic junction obstruction in children. Kidney Int 63: 1104-1115, 2003.
57. Vergarajauregui S, San Miguel A, Puertollano R. Activation of p38 mitogen-activated protein kinase promotes epidermal growth factor receptor internalization. Traffic 7: 686-698, 2006.
58. Vodovotz Y, Geiser AG, Chesler L, Letterio JJ, Campbell A, Lucia MS, Sporn MB, Roberts AB. Spontaneously increased production of nitric oxide and aberrant expression of the inducible nitric oxide synthase in vivo in the transforming growth factor-β1 null mouse. J Exp Med 183: 2337-2342, 1996.
59. Woolf AS. A molecular and genetic view of human renal and urinary tract malformations. Kidney Int 58: 500-512, 2000.
60. Yu Z, Kone BC. The STAT3 DNA-binding domain mediates interaction with NF-κB p65 and inducible nitric oxide synthase transrepression in mesangial cells. J Am Soc Nephrol 15: 585-591, 2004.
61. Yu Z, Zhang W, Kone BC. Signal transducers and activators of transcription 3 (STAT3) inhibits transcription of the inducible nitric oxide synthase gene by interacting with nuclear factor-κB. Biochem J 367: 97-105, 2002.
62. Zhuang S, Dang Y, Schnellmann RG. Requirement of the epidermal growth factor receptor in renal epithelial cell proliferation and migration. Am J Physiol Renal Physiol 287: F365-F372, 2004.
63. Zwang Y, Yarden Y. p38 MAP kinase mediates stress-induced internalization of EGFR: implications for cancer chemotherapy. EMBO J 25: 4195-4206, 2006.