Chemical chaperon 4-phenylbutyrate protects against the endoplasmic reticulum stress-mediated renal fibrosis in vivo and in vitro

Oncotarget

Volumn 7, Issue 16, 2016, Pages 22116-22127

  Liu, Shing Hwa ^a,b,c   Yang, Ching Chin ^a   Chan, Ding Cheng ^a,b   Wu, Cheng Tien ^a   Chen, Li Ping ^d   Huang, Jenq Wen ^a   Hung, Kuan Yu ^a   Chiang, Chih Kang ^a,b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Endoplasmic reticulum stress; Renal fibrosis; Sodium 4 phenylbutyrate; Unilateral ureteral obstruction

Indexed keywords

4 PHENYLBUTYRIC ACID; ACTIVATING TRANSCRIPTION FACTOR 4; ALPHA SMOOTH MUSCLE ACTIN; CCAAT ENHANCER BINDING PROTEIN; CONNECTIVE TISSUE GROWTH FACTOR; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA; X BOX BINDING PROTEIN 1; 4-PHENYLBUTYRIC ACID; ARYLBUTYRIC ACID DERIVATIVE; CHAPERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; ENDOPLASMIC RETICULUM STRESS; ENZYME PHOSPHORYLATION; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CELL; KIDNEY FIBROSIS; MALE; NONHUMAN; NRK 52E CELL; OBSTRUCTION-INDUCED RENAL FIBROSIS; PROTEIN EXPRESSION; RAT; RENAL PROTECTION; ANIMAL; CHRONIC KIDNEY FAILURE; COMPLICATION; DRUG EFFECTS; FIBROSIS; PATHOLOGY; SIGNAL TRANSDUCTION; URETER OBSTRUCTION; WISTAR RAT;

ANIMALS; ENDOPLASMIC RETICULUM STRESS; FIBROSIS; KIDNEY FAILURE, CHRONIC; MALE; MOLECULAR CHAPERONES; PHENYLBUTYRATES; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; URETERAL OBSTRUCTION;

EID: 84965076058     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7904     Document Type: Article

References (47)

1. 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. 1968; 2:363-366.
2. Hewitson TD. Renal tubulointerstitial fibrosis: common but never simple. Am J Physiol Renal Physiol. 2009; 296:F1239-1244.
3. Eddy AA. Molecular insights into renal interstitial fibrosis. J Am Soc Nephrol. 1996; 7:2495-2508.
4. Border WA, Noble NA. TGF-beta in kidney fibrosis: a target for gene therapy. Kidney Int. 1997; 51:1388-1396.
5. Isaka Y, Tsujie M, Ando Y, Nakamura H, Kaneda Y, Imai E, Hori M. Transforming growth factor-beta 1 antisense oligodeoxynucleotides block interstitial fibrosis in unilateral ureteral obstruction. Kidney Int. 2000; 58:1885-1892.
6. Liu Y. Renal fibrosis: new insights into the pathogenesis and therapeutics. Kidney Int. 2006; 69:213-217.
7. Grotendorst GR. Connective tissue growth factor: a mediator of TGF-beta action on fibroblasts. Cytokine Growth Factor Rev. 1997; 8:171-179.
8. Liu Y. New insights into epithelial-mesenchymal transition in kidney fibrosis. J Am Soc Nephrol. 2010; 21:212-222.
9. Inoue T, Okada H, Kobayashi T, Watanabe Y, Kanno Y, Kopp JB, Nishida T, Takigawa M, Ueno M, Nakamura T, Suzuki H. Hepatocyte growth factor counteracts transforming growth factor-beta1, through attenuation of connective tissue growth factor induction, and prevents renal fibrogenesis in 5/6 nephrectomized mice. FASEB J. 2003; 17:268-270.
10. Yokoi H, Mukoyama M, Nagae T, Mori K, Suganami T, Sawai K, Yoshioka T, Koshikawa M, Nishida T, Takigawa M, Sugawara A, Nakao K. Reduction in connective tissue growth factor by antisense treatment ameliorates renal tubulointerstitial fibrosis. J Am Soc Nephrol. 2004; 15:1430-1440.
11. Lin SL, Chen RH, Chen YM, Chiang WC, Lai CF, Wu KD, Tsai TJ. Pentoxifylline attenuates tubulointerstitial fibrosis by blocking Smad3/4-activated transcription and profibrogenic effects of connective tissue growth factor. J Am Soc Nephrol. 2005; 16:2702-2713.
12. Inagi R, Nangaku M, Onogi H, Ueyama H, Kitao Y, Nakazato K, Ogawa S, Kurokawa K, Couser WG, Miyata T. Involvement of endoplasmic reticulum (ER) stress in podocyte injury induced by excessive protein accumulation. Kidney Int. 2005; 68:2639-2650.
13. Inagi R, Ishimoto Y, Nangaku M. Proteostasis in endoplasmic reticulum-new mechanisms in kidney disease. Nat Rev Nephrol. 2014; 10:369-378.
14. Hotamisligil GS. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell. 2010; 140:900-917.
15. Tabas I, Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol. 2011; 13:184-190.
16. Haas IG. BiP (GRP78), an essential hsp70 resident protein in the endoplasmic reticulum. Experientia. 1994; 50:1012-1020.
17. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, Prywes R, Brown MS, Goldstein JL. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell. 2000; 6:1355-1364.
18. Oyadomari S, Araki E, Mori M. Endoplasmic reticulum stress-mediated apoptosis in pancreatic beta-cells. Apoptosis. 2002; 7:335-345.
19. Lee GH, Oh HW, Lim HD, Lee W, Chae HJ, Kim HR. 4-phenylbutyric Acid Regulates Collagen Synthesis and Secretion Induced by High Concentrations of Glucose in Human Gingival Fibroblasts. Korean J Physiol Pharmacol. 2011; 15:345-351.
20. Liu G, Beri R, Mueller A, Kamp DW. Molecular mechanisms of asbestos-induced lung epithelial cell apoptosis. Chemico-biological interactions. 2010; 188:309-318.
21. Inagi R. Endoplasmic reticulum stress in the kidney as a novel mediator of kidney injury. Nephron Experimental nephrology. 2009; 112:e1-9.
22. Hiramatsu N, Chiang WC, Kurt TD, Sigurdson CJ, Lin JH. Multiple Mechanisms of Unfolded Protein Response-Induced Cell Death. The American journal of pathology. 2015; 185:1800-1808.
23. Maestri NE, Brusilow SW, Clissold DB, Bassett SS. Longterm treatment of girls with ornithine transcarbamylase deficiency. N Engl J Med. 1996; 335:855-859.
24. Collins AF, Pearson HA, Giardina P, McDonagh KT, Brusilow SW, Dover GJ. Oral sodium phenylbutyrate therapy in homozygous beta thalassemia: a clinical trial. Blood. 1995; 85:43-49.
25. Warrell RP, Jr., He LZ, Richon V, Calleja E, PandolfiPP. Therapeutic targeting of transcription in acute promyelocytic leukemia by use of an inhibitor of histone deacetylase. J Natl Cancer Inst. 1998; 90:1621-1625.
26. Vilatoba M, Eckstein C, Bilbao G, Smyth CA, Jenkins S, Thompson JA, EckhoffDE, Contreras JL. Sodium 4-phenylbutyrate protects against liver ischemia reperfusion injury by inhibition of endoplasmic reticulum-stress mediated apoptosis. Surgery. 2005; 138:342-351.
27. Singh OV, Vij N, Mogayzel PJ, Jr., Jozwik C, Pollard HB, Zeitlin PL. Pharmacoproteomics of 4-phenylbutyratetreated IB3-1 cystic fibrosis bronchial epithelial cells. J Proteome Res. 2006; 5:562-571.
28. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Gorgun CZ, Hotamisligil GS. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science. 2006; 313:1137-1140.
29. Chiang CK, Hsu SP, Wu CT, Huang JW, Cheng HT, Chang YW, Hung KY, Wu KD, Liu SH. Endoplasmic reticulum stress implicated in the development of renal fibrosis. Molecular medicine. 2011; 17:1295-1305.
30. Lovisa S, LeBleu VS, Tampe B, Sugimoto H, Vadnagara K, Carstens JL, Wu CC, Hagos Y, Burckhardt BC, Pentcheva-Hoang T, Nischal H, Allison JP, Zeisberg M, Kalluri R. Epithelial-to-mesenchymal transition induces cell cycle arrest and parenchymal damage in renal fibrosis. Nat Med. 2015; 21:998-1009.
31. Nangaku M. Mechanisms of tubulointerstitial injury in the kidney: final common pathways to end-stage renal failure. Intern Med. 2004; 43:9-17.
32. Thomas GL, Yang B, Wagner BE, Savill J, El Nahas AM. Cellular apoptosis and proliferation in experimental renal fibrosis. Nephrol Dial Transplant. 1998; 13:2216-2226.
33. Kawakami T, Inagi R, Wada T, Tanaka T, Fujita T, Nangaku M. Indoxyl sulfate inhibits proliferation of human proximal tubular cells via endoplasmic reticulum stress. Am J Physiol Renal Physiol. 2010; 299:F568-576.
34. Kaneto H, Morrissey J, Klahr S. Increased expression of TGF-beta 1 mRNA in the obstructed kidney of rats with unilateral ureteral ligation. Kidney Int. 1993; 44:313-321.
35. Heldin CH, Miyazono K, ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature. 1997; 390:465-471.
36. Miyazono K, ten Dijke P, Heldin CH. TGF-beta signaling by Smad proteins. Adv Immunol. 2000; 75:115-157.
37. Jang CW, Chen CH, Chen CC, Chen JY, Su YH, Chen RH. TGF-beta induces apoptosis through Smad-mediated expression of DAP-kinase. Nat Cell Biol. 2002; 4:51-58.
38. Schuster N, Krieglstein K. Mechanisms of TGF-betamediated apoptosis. Cell Tissue Res. 2002; 307:1-14.
39. Schiffer M, Bitzer M, Roberts IS, Kopp JB, ten Dijke P, Mundel P, Bottinger EP. Apoptosis in podocytes induced by TGF-beta and Smad7. J Clin Invest. 2001; 108:807-816.
40. Yamaguchi K, Shirakabe K, Shibuya H, Irie K, Oishi I, Ueno N, Taniguchi T, Nishida E, Matsumoto K. Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science. 1995; 270:2008-2011.
41. Chiang CK, Sheu ML, Lin YW, Wu CT, Yang CC, Chen MW, Hung KY, Wu KD, Liu SH. Honokiol ameliorates renal fibrosis by inhibiting extracellular matrix and proinflammatory factors in vivo and in vitro. British journal of pharmacology. 2011; 163:586-597.
42. Frazier KS, Paredes A, Dube P, Styer E. Connective tissue growth factor expression in the rat remnant kidney model and association with tubular epithelial cells undergoing transdifferentiation. Veterinary pathology. 2000; 37:328-335.
43. Geng H, Lan R, Singha PK, Gilchrist A, Weinreb PH, Violette SM, Weinberg JM, Saikumar P, Venkatachalam MA. Lysophosphatidic acid increases proximal tubule cell secretion of profibrotic cytokines PDGF-B and CTGF through LPA2-and Galphaq-mediated Rho and alphavbeta6 integrin-dependent activation of TGF-beta. The American journal of pathology. 2012; 181:1236-1249.
44. Luo ZF, Feng B, Mu J, Qi W, Zeng W, Guo YH, Pang Q, Ye ZL, Liu L, Yuan FH. Effects of 4-phenylbutyric acid on the process and development of diabetic nephropathy induced in rats by streptozotocin: regulation of endoplasmic reticulum stress-oxidative activation. Toxicology and applied pharmacology. 2010; 246:49-57.
45. Zhu S, Wang Y, Jin J, Guan C, Li M, Xi C, Ouyang Z, Chen M, Qiu Y, Huang M, Huang Z. Endoplasmic reticulum stress mediates aristolochic acid I-induced apoptosis in human renal proximal tubular epithelial cells. Toxicology in vitro. 2012; 26:663-671.
46. Chiang CK, Tanaka T, Inagi R, Fujita T, Nangaku M. Indoxyl sulfate, a representative uremic toxin, suppresses erythropoietin production in a HIF-dependent manner. Laboratory investigation. 2011; 91:1564-1571.
47. Yu CC, Hsu MJ, Kuo ML, Chen RF, Chen MC, Bai KJ, Yu MC, Chen BC, Lin CH. Thrombin-induced connective tissue growth factor expression in human lung fibroblasts requires the ASK1/JNK/AP-1 pathway. J Immunol. 2009; 182:7916-7927.