Stat3 controls tubulointerstitial communication during CKD

Journal of the American Society of Nephrology

Volumn 27, Issue 12, 2016, Pages 3690-3705

  Bienaimé, Frank ^a,b   Muorah, Mordi ^a   Yammine, Lucie ^a   Burtin, Martine ^a   Nguyen, Clément ^a   Baron, Willian ^a   Garbay, Serge ^c   Viau, Amandine ^a   Broueilh, Mélanie ^a   Blanc, Thomas ^a   Peters, Dorien ^d   Poli, Valeria ^e   Anglicheau, Dany ^a,f   Friedlander, Gérard ^a,b   Pontoglio, Marco ^c   Gallazzini, Morgan ^a   Terzi, Fabiola ^a  

^a INSTITUT NECKER ENFANTS MALADES   (France)

^b Service d'Explorations Fonctionnelles   (France)

^c CNRS   (France)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e UNIVERSITY OF TURIN   (Italy)

^f HÔPITAL NECKER ENFANTS MALADES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PDGR BETA POLYPEPTIDE; POLYPEPTIDE; STAT3 PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CHRONIC KIDNEY FAILURE; CONTROLLED STUDY; DNA MODIFICATION; FEMALE; FIBROBLAST; FIBROSING ALVEOLITIS; GENETIC BACKGROUND; IN VITRO STUDY; KIDNEY TUBULE CELL; LEYDIG CELL; MOUSE; NEPHRON; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ANIMAL; CELL COMMUNICATION; CYTOLOGY; KIDNEY TUBULE; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CELL COMMUNICATION; FEMALE; KIDNEY TUBULES; MICE; RENAL INSUFFICIENCY, CHRONIC; STAT3 TRANSCRIPTION FACTOR;

EID: 85020082127     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2015091014     Document Type: Article

References (65)

1. Zhang QL, Rothenbacher D: Prevalence of chronic kidney disease in population-based studies: Systematic review. BMC Public Health 8: 117, 2008
2. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY: Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med 351: 1296-1305, 2004
3. Wen CP, Cheng TY, Tsai MK, Chang YC, Chan HT, Tsai SP, Chiang PH, Hsu CC, Sung PK, Hsu YH, Wen SF: All-cause mortality attributable to chronic kidney disease: A prospective cohort study based on 462 293 adults in Taiwan. Lancet 371: 2173-2182, 2008
4. Risdon RA, Sloper JC, De Wardener HE: Relationship between renal function and histological changes found in renal-biopsy specimens from patients with persistent glomerular nephritis. Lancet 2: 363-366, 1968
5. Coppo R, D'Amico G: Factors predicting progression of IgA nephropathies. J Nephrol 18: 503-512, 2005
6. Serón D, Moreso F: Protocol biopsies in renal transplantation: Prognostic value of structural monitoring. Kidney Int 72: 690-697, 2007
7. Kramann R, Dirocco DP, Maarouf OH, Humphreys BD: Matrix producing cells in chronic kidney disease: Origin, regulation, and activation. Curr Pathobiol Rep 1: 1, 2013
8. Santos CI, Costa-Pereira AP: Signal transducers and activators of transcription-from cytokine signalling to cancer biology. Biochim Biophys Acta 1816: 38-49, 2011
9. ReichNC, Liu L: Tracking STAT nuclear traffic.Nat Rev Immunol 6: 602-612, 2006
10. Frank DA: STAT3 as a central mediator of neoplastic cellular transformation. Cancer Lett 251: 199-210, 2007
11. Takeda K, Noguchi K, Shi W, Tanaka T, Matsumoto M, Yoshida N, Kishimoto T, Akira S: Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc Natl Acad Sci U S A 94: 3801-3804, 1997
12. Kidder BL, Yang J, Palmer S: Stat3 and c-Myc genome-wide promoter occupancy in embryonic stem cells. PLoS One 3: e3932, 2008
13. Langlais D, Couture C, Balsalobre A, Drouin J: Regulatory network analyses reveal genome-wide potentiation of LIF signaling by glucocorticoids and define an innate cell defense response. PLoS Genet 4: e1000224, 2008
14. Ouyang Z, Zhou Q, Wong WH: ChIP-Seq of transcription factors predicts absolute and differential gene expression in embryonic stem cells. Proc Natl Acad Sci U S A 106: 21521-21526, 2009
15. Vallania F, Schiavone D, Dewilde S, Pupo E, Garbay S, Calogero R, Pontoglio M, Provero P, Poli V: Genome-wide discovery of functional transcription factor binding sites by comparative genomics: The case of Stat3. Proc Natl Acad Sci U S A 106: 5117-5122, 2009
16. Choy MK, Movassagh M, Siggens L, Vujic A, Goddard M, S'nchez A, Perkins N, Figg N, Bennett M, Carroll J, Foo R: High-throughput sequencing identifies STAT3 as the DNA-associated factor for p53-NFkappaB-complex-dependent gene expression in human heart failure. Genome Med 2: 37, 2010
17. Gao SP, Bromberg JF: Touched and moved by STAT3. Sci STKE 2006: pe30, 2006
18. Gough DJ, Corlett A, Schlessinger K, Wegrzyn J, Larner AC, Levy DE: Mitochondrial STAT3 supports Ras-dependent oncogenic transformation. Science 324: 1713-1716, 2009
19. Wegrzyn J, Potla R, Chwae YJ, Sepuri NB, Zhang Q, Koeck T, Derecka M, Szczepanek K, SzelagM, Gornicka A,MohA,Moghaddas S,Chen Q, Bobbili S,Cichy J, Dulak J, Baker DP,Wolfman A, StuehrD,HassanMO, Fu XY, Avadhani N, Drake JI, Fawcett P, Lesnefsky EJ, Larner AC: Function of mitochondrial Stat3 in cellular respiration. Science 323: 793-797, 2009
20. Hern'ndez-Vargas P, López-Franco O, Sanju'n G, Rupérez M, Ortiz-Muñoz G, Suzuki Y, Aguado-Roncero P, Pérez-Tejerizo G, Blanco J, Egido J, Ruiz-Ortega M, Gómez-Guerrero C: Suppressors of cytokine signaling regulate angiotensin II-activated Janus kinase-signal transducers and activators of transcription pathway in renal cells. J AmSoc Nephrol 16: 1673-1683, 2005
21. 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
22. Arakawa T, Masaki T, Hirai T, Doi S, Kuratsune M, Arihiro K, Kohno N, Yorioka N: Activation of signal transducer and activator of transcription 3 correlates with cell proliferation and renal injury in human glomerulonephritis. Nephrol Dial Transplant 23: 3418-3426, 2008
23. Lu TC, Wang ZH, Feng X, Chuang PY, Fang W, Shen Y, Levy DE, Xiong H, Chen N, He JC: Knockdown of Stat3 activity in vivo prevents diabetic glomerulopathy. Kidney Int 76: 63-71, 2009
24. BerthierCC, ZhangH, SchinM,Henger A,Nelson RG, Yee B, Boucherot A, Neusser MA, Cohen CD, Carter-Su C, Argetsinger LS, Rastaldi MP, Brosius FC, Kretzler M: Enhanced expression of Janus kinase-signal transducer and activator of transcription pathway members in human diabetic nephropathy. Diabetes 58: 469-477, 2009
25. Feng X, Lu TC, Chuang PY, Fang W, Ratnam K, Xiong H, Ouyang X, Shen Y, LevyDE, HyinkD, Klotman M,D'Agati V, Iyengar R, Klotman PE, He JC: Reduction of Stat3 activity attenuatesHIV-induced kidney injury. J Am Soc Nephrol 20: 2138-2146, 2009
26. Ortiz-Muñoz G, Lopez-Parra V, Lopez-Franco O, Fernandez-Vizarra P, Mallavia B, Flores C, Sanz A, Blanco J, Mezzano S, Ortiz A, Egido J, Gomez-Guerrero C: Suppressors of cytokine signaling abrogate diabetic nephropathy. J Am Soc Nephrol 21: 763-772, 2010
27. Leonhard WN, van der Wal A, Novalic Z, Kunnen SJ, Gansevoort RT, Breuning MH, de Heer E, Peters DJ: Curcumin inhibits cystogenesis by simultaneous interference of multiple signaling pathways: In vivo evidence from a Pkd1-deletion model. Am J Physiol Renal Physiol 300: F1193-F1202, 2011
28. PangM, Ma L,Gong R, Tolbert E,Mao H, PonnusamyM, 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
29. Lim CP, Phan TT, Lim IJ, Cao X: Cytokine profiling and Stat3 phosphorylation in epithelial-mesenchymal interactions between keloid keratinocytes and fibroblasts. J Invest Dermatol 129: 851-861, 2009
30. Lieblein JC, Ball S, Hutzen B, Sasser AK, Lin HJ, Huang TH, Hall BM, Lin J: STAT3 can be activated through paracrine signaling in breast epithelial cells. BMC Cancer 8: 302, 2008
31. Cheng N, Chytil A, Shyr Y, Joly A, Moses HL: Transforming growth factor-beta signaling-deficient fibroblasts enhance hepatocyte growth factor signaling inmammary carcinoma cells to promote scattering and invasion. Mol Cancer Res 6: 1521-1533, 2008
32. Pillebout E, Burtin M, Yuan HT, Briand P,Woolf AS, Friedlander G, Terzi F: Proliferation and remodeling of the peritubular microcirculation after nephron reduction: Association with the progression of renal lesions. Am J Pathol 159: 547-560, 2001
33. Laouari D, Burtin M, Phelep A, Martino C, Pillebout E, Montagutelli X, Friedlander G, Terzi F: TGF-alpha mediates genetic susceptibility to chronic kidney disease. J Am Soc Nephrol 22: 327-335, 2011
34. Lantinga-van Leeuwen IS, LeonhardWN, van derWal A, Breuning MH, de Heer E, Peters DJ: Kidney-specific inactivation of the Pkd1 gene induces rapid cyst formation in developing kidneys and a slow onset of disease in adult mice. Hum Mol Genet 16: 3188-3196, 2007
35. Alonzi T, Maritano D, Gorgoni B, Rizzuto G, Libert C, Poli V: Essential role of STAT3 in the control of the acute-phase response as revealed by inducible gene inactivation [correction of activation] in the liver. Mol Cell Biol 21: 1621-1632, 2001
36. Ma M, Tian X, Igarashi P, Pazour GJ, Somlo S: Loss of cilia suppresses cyst growth in genetic models of autosomal dominant polycystic kidney disease. Nat Genet 45: 1004-1012, 2013
37. Nishio S, HatanoM, NagataM, Horie S, Koike T, Tokuhisa T,Mochizuki T: Pkd1 regulates immortalized proliferation of renal tubular epithelial cells through p53 induction and JNK activation. J Clin Invest 115: 910-918, 2005
38. Fischer E, Legue E, Doyen A, Nato F, Nicolas JF, Torres V, Yaniv M, PontoglioM: Defective planar cell polarity in polycystic kidney disease. Nat Genet 38: 21-23, 2006
39. Miyagi C, Yamashita S, Ohba Y, Yoshizaki H, Matsuda M, Hirano T: STAT3 noncell-autonomously controls planar cell polarity during zebrafish convergence and extension. J Cell Biol 166: 975-981, 2004
40. Lin SL, Kisseleva T, Brenner DA, Duffield JS: Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. Am J Pathol 173: 1617-1627, 2008
41. Le Hir M, Hegyi I, Cueni-Loffing D, Loffing J, Kaissling B: Characterization of renal interstitial fibroblast-specific protein 1/S100A4-positive cells in healthy and inflamed rodent kidneys. Histochem Cell Biol 123: 335-346, 2005
42. Humphreys BD, Lin SL, Kobayashi A, Hudson TE,Nowlin BT, Bonventre JV, Valerius MT, McMahon AP, Duffield JS: Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol 176: 85-97, 2010
43. 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
44. LeBleu VS, Taduri G, O'Connell J, Teng Y, Cooke VG, Woda C, Sugimoto H, Kalluri R: Origin and function of myofibroblasts in kidney fibrosis. Nat Med 19: 1047-1053, 2013
45. Chen YT, Chang FC, Wu CF, Chou YH, Hsu HL, Chiang WC, Shen J, Chen YM, Wu KD, Tsai TJ, Duffield JS, Lin SL: Platelet-derived growth factor receptor signaling activates pericyte-myofibroblast transition in obstructive and post-ischemic kidney fibrosis. Kidney Int 80: 1170-1181, 2011
46. Lu Y, Liu S, Zhang S, Cai G, Jiang H, Su H, Li X, Hong Q, Zhang X, Chen X: Tissue inhibitor of metalloproteinase-1 promotes NIH3T3 fibroblast proliferation by activating p-Akt and cell cycle progression. Mol Cells 31: 225-230, 2011
47. Lovelock JD, Baker AH, Gao F, Dong JF, Bergeron AL, McPheat W, Sivasubramanian N, Mann DL: Heterogeneous effects of tissue inhibitors of matrix metalloproteinases on cardiac fibroblasts. Am J Physiol Heart Circ Physiol 288: H461-H468, 2005
48. Tarjus A, Martínez-Martínez E, Amador C, Latouche C, El Moghrabi S, Berger T,Mak TW, Fay R, FarmanN, Rossignol P, Zannad F, López-Andrés N, Jaisser F: Neutrophil gelatinase-associated lipocalin, a novel mineralocorticoid biotarget, mediates vascular profibrotic effects of mineralocorticoids. Hypertension 66: 158-166, 2015
49. Ma FY, Flanc RS, Tesch GH, Han Y, Atkins RC, Bennett BL, Friedman GC, Fan JH, Nikolic-Paterson DJ: A pathogenic role for c-Jun aminoterminal kinase signaling in renal fibrosis and tubular cell apoptosis. J Am Soc Nephrol 18: 472-484, 2007
50. 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
51. Prunotto M, Budd DC, Gabbiani G,Meier M, Formentini I, Hartmann G, Pomposiello S, Moll S: Epithelial-mesenchymal crosstalk alteration in kidney fibrosis. J Pathol 228: 131-147, 2012
52. Tang WW, Van GY, Qi M: Myofibroblast and alpha 1 (III) collagen expression in experimental tubulointerstitial nephritis. Kidney Int 51: 926-931, 1997
53. Ostendorf T, Eitner F, Floege J: The PDGF family in renal fibrosis. Pediatr Nephrol 27: 1041-1050, 2012
54. Viau A, El Karoui K, Laouari D, Burtin M, Nguyen C, Mori K, Pillebout E, Berger T, Mak TW, Knebelmann B, Friedlander G, Barasch J, Terzi F: Lipocalin 2 is essential for chronic kidney disease progression in mice and humans. J Clin Invest 120: 4065-4076, 2010
55. Cai G, Zhang X, HongQ, Shao F, Shang X, Fu B, Feng Z, Lin H,Wang J, Shi S, Yin Z, Chen X: Tissue inhibitor of metalloproteinase-1 exacerbated renal interstitial fibrosis through enhancing inflammation. Nephrol Dial Transplant 23: 1861-1875, 2008
56. Kim H, Oda T, López-Guisa J, Wing D, Edwards DR, Soloway PD, Eddy AA: TIMP-1 deficiency does not attenuate interstitial fibrosis in obstructive nephropathy. J Am Soc Nephrol 12: 736-748, 2001
57. Ronco P, Chatziantoniou C: Matrix metalloproteinases and matrix receptors in progression and reversal of kidney disease: Therapeutic perspectives. Kidney Int 74: 873-878, 2008
58. Phanish MK, Winn SK, Dockrell ME: Connective tissue growth factor-(CTGF, CCN2)-A marker, mediator and therapeutic target for renal fibrosis. Nephron, Exp Nephrol 114: e83-e92, 2010
59. Declèves AE, Sharma K: Novel targets of antifibrotic and antiinflammatory treatment in CKD. Nat Rev Nephrol 10: 257-267, 2014
60. Denton CP, Merkel PA, Furst DE, Khanna D, Emery P, Hsu VM, Silliman N, Streisand J, Powell J, Akesson A, Coppock J, Hoogen F, Herrick A, Mayes MD, Veale D, Haas J, Ledbetter S, Korn JH, Black CM, Seibold JR; Cat-192 Study Group; Scleroderma Clinical Trials Consortium: Recombinant human anti-transforming growth factor beta1 antibody therapy in systemic sclerosis: A multicenter, randomized, placebocontrolled phase I/II trial of CAT-192. Arthritis Rheum 56: 323-333, 2007
61. Dai Y, Gu L, Yuan W, Yu Q, Ni Z, Ross MJ, Kaufman L, Xiong H, Salant DJ, He JC, Chuang PY: Podocyte-specific deletion of signal transducer and activator of transcription 3 attenuates nephrotoxic serum-induced glomerulonephritis. Kidney Int 84: 950-961, 2013
62. Gu L, Dai Y, Xu J, Mallipattu S, Kaufman L, Klotman PE, He JC, Chuang PY: Deletion of podocyte STAT3 mitigates the entire spectrum of HIV-1-associated nephropathy. AIDS 27: 1091-1098, 2013
63. Pillebout E, Weitzman JB, Burtin M, Martino C, Federici P, Yaniv M, Friedlander G, Terzi F: JunD protects against chronic kidney disease by regulating paracrine mitogens. J Clin Invest 112: 843-852, 2003
64. Lautrette A, Li S, Alili R, Sunnarborg SW, BurtinM, 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
65. Verdeguer F, Le Corre S, Fischer E, Callens C, Garbay S, Doyen A, Igarashi P, Terzi F, Pontoglio M: A mitotic transcriptional switch in polycystic kidney disease. Nat Med 16: 106-110, 2010