Browse > Article
http://dx.doi.org/10.4196/kjpp.2021.25.5.413

Curcumin attenuates renal ischemia reperfusion injury via JNK pathway with the involvement of p300/CBP-mediated histone acetylation  

Yang, Lu (Department of Anesthesiology, The First Affiliated Hospital of Sun Yat-sen University)
Chen, Xiaoxiang (Department of Anesthesiology, The First Affiliated Hospital of Sun Yat-sen University)
Bi, Zirong (Department of Organ Transplantation, The First Affiliated Hospital of Sun Yat-sen University)
Liao, Jun (Department of Organ Transplantation, Zhujiang Hospital of Southern Medical University)
Zhao, Weian (Department of Anesthesiology, The First Affiliated Hospital of Sun Yat-sen University)
Huang, Wenqi (Department of Anesthesiology, The First Affiliated Hospital of Sun Yat-sen University)
Publication Information
The Korean Journal of Physiology and Pharmacology / v.25, no.5, 2021 , pp. 413-423 More about this Journal
Abstract
Apoptosis is proved responsible for renal damage during ischemia/reperfusion. The regulation for renal apoptosis induced by ischemia/reperfusion injury (IRI) has still been unclearly characterized to date. In the present study, we investigated the regulation of histone acetylation on IRI-induced renal apoptosis and the molecular mechanisms in rats with the application of curcumin possessing a variety of biological activities involving inhibition of apoptosis. Sprague-Dawley rats were randomized into four experimental groups (SHAM, IRI, curcumin, SP600125). Results showed that curcumin significantly decreased renal apoptosis and caspase-3/-9 expression and enhanced renal function in IRI rats. Treatment with curcumin in IRI rats also led to the decrease in expression of p300/cyclic AMP response element-binding protein (CBP) and activity of histone acetyltransferases (HATs). Reduced histone H3 lysine 9 (H3K9) acetylation was found near the promoter region of caspase-3/-9 after curcumin treatment. In a similar way, SP600125, an inhibitor of c-Jun N-terminal kinase (JNK), also attenuated renal apoptosis and enhanced renal function in IRI rats. In addition, SP600125 suppressed the binding level of p300/CBP and H3K9 acetylation near the promoter region of caspase-3/-9, and curcumin could inhibit JNK phosphorylation like SP600125. These results indicate that curcumin could attenuate renal IRI via JNK/p300/CBP-mediated anti-apoptosis signaling.
Keywords
Curcumin; Histone acetylation; MAP kinase signaling system; p300/CBP; Reperfusion Injury for Renal IRI;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Hoste EAJ, Kellum JA, Selby NM, Zarbock A, Palevsky PM, Bagshaw SM, Goldstein SL, Cerda J, Chawla LS. Global epidemiology and outcomes of acute kidney injury. Nat Rev Nephrol. 2018;14:607-625.   DOI
2 Kelly KJ. Distant effects of experimental renal ischemia/reperfusion injury. J Am Soc Nephrol. 2003;14:1549-1558.   DOI
3 Bonegio R, Lieberthal W. Role of apoptosis in the pathogenesis of acute renal failure. Curr Opin Nephrol Hypertens. 2002;11:301-308.   DOI
4 Zhao Y, Ding C, Xue W, Ding X, Zheng J, Gao Y, Xia X, Li S, Liu J, Han F, Zhu F, Tian P. Genome-wide DNA methylation analysis in renal ischemia reperfusion injury. Gene. 2017;610:32-43.   DOI
5 Basile DP, Anderson MD, Sutton TA. Pathophysiology of acute kidney injury. Compr Physiol. 2012;2:1303-1353.   DOI
6 Wu J, Pan X, Fu H, Zheng Y, Dai Y, Yin Y, Chen Q, Hao Q, Bao D, Hou D. Effect of curcumin on glycerol-induced acute kidney injury in rats. Sci Rep. 2017;7:10114.   DOI
7 Yu W, Zha W, Ke Z, Min Q, Li C, Sun H, Liu C. Curcumin protects neonatal rat cardiomyocytes against high glucose-induced apoptosis via PI3K/Akt signalling pathway. J Diabetes Res. 2016;2016:4158591.
8 Wu J, Zhang X, Nauta HJ, Lin Q, Li J, Fang L. JNK1 regulates histone acetylation in trigeminal neurons following chemical stimulation. Biochem Biophys Res Commun. 2008;376:781-786.   DOI
9 Bayrak O, Uz E, Bayrak R, Turgut F, Atmaca AF, Sahin S, Yildirim ME, Kaya A, Cimentepe E, Akcay A. Curcumin protects against ischemia/reperfusion injury in rat kidneys. World J Urol. 2008;26:285-291.   DOI
10 Xu YF, Liu M, Peng B, Che JP, Zhang HM, Yan Y, Wang GC, Wu YC, Zheng JH. Protective effects of SP600125 on renal ischemiareperfusion injury in rats. J Surg Res. 2011;169:e77-e84.   DOI
11 Zhou W, Jiang D, Tian J, Liu L, Lu T, Huang X, Sun H. Acetylation of H3K4, H3K9, and H3K27 mediated by p300 regulates the expression of GATA4 in cardiocytes. Genes Dis. 2018;6:318-325.   DOI
12 Gupta SC, Patchva S, Aggarwal BB. Therapeutic roles of curcumin: lessons learned from clinical trials. AAPS J. 2013;15:195-218.   DOI
13 Hasan ST, Zingg JM, Kwan P, Noble T, Smith D, Meydani M. Curcumin modulation of high fat diet-induced atherosclerosis and steatohepatosis in LDL receptor deficient mice. Atherosclerosis. 2014;232:40-51.   DOI
14 Cekmen M, Ilbey YO, Ozbek E, Simsek A, Somay A, Ersoz C. Curcumin prevents oxidative renal damage induced by acetaminophen in rats. Food Chem Toxicol. 2009;47:1480-1484.   DOI
15 Zhang J, Tang L, Li GS, Wang J. The anti-inflammatory effects of curcumin on renal ischemia-reperfusion injury in rats. Ren Fail. 2018;40:680-686.   DOI
16 Yeh CH, Chen TP, Wu YC, Lin YM, Jing Lin P. Inhibition of NFkappaB activation with curcumin attenuates plasma inflammatory cytokines surge and cardiomyocytic apoptosis following cardiac ischemia/reperfusion. J Surg Res. 2005;125:109-116.   DOI
17 Mokhtari-Zaer A, Marefati N, Atkin SL, Butler AE, Sahebkar A. The protective role of curcumin in myocardial ischemia-reperfusion injury. J Cell Physiol. 2018;234:214-222.   DOI
18 Boyanapalli SS, Kong AT. "Curcumin, the King of Spices": epigenetic regulatory mechanisms in the prevention of cancer, neurological, and inflammatory diseases. Curr Pharmacol Rep. 2015;1:129-139.   DOI
19 Tessarz P, Kouzarides T. Histone core modifications regulating nucleosome structure and dynamics. Nat Rev Mol Cell Biol. 2014;15:703-708.   DOI
20 Fontecha-Barriuso M, Martin-Sanchez D, Ruiz-Andres O, Poveda J, Sanchez-Nino MD, Valino-Rivas L, Ruiz-Ortega M, Ortiz A, Sanz AB. Targeting epigenetic DNA and histone modifications to treat kidney disease. Nephrol Dial Transplant. 2018;33:1875-1886.   DOI
21 Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, Peterson CL. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science. 2006;311:844-847.   DOI
22 Tang J, Zhuang S. Histone acetylation and DNA methylation in ischemia/reperfusion injury. Clin Sci (Lond). 2019;133:597-609.   DOI
23 Bomsztyk K, Denisenko O. Epigenetic alterations in acute kidney injury. Semin Nephrol. 2013;33:327-340.
24 Audia JE, Campbell RM. Histone modifications and cancer. Cold Spring Harb Perspect Biol. 2016;8:a019521.   DOI
25 Zager RA, Johnson AC, Becker K. Acute unilateral ischemic renal injury induces progressive renal inflammation, lipid accumulation, histone modification, and "end-stage" kidney disease. Am J Physiol Renal Physiol. 2011;301:F1334-F1345.   DOI
26 Bomsztyk K, Flanagin S, Mar D, Mikula M, Johnson A, Zager R, Denisenko O. Synchronous recruitment of epigenetic modifiers to endotoxin synergistically activated Tnf-α gene in acute kidney injury. PLoS One. 2013;8:e70322.   DOI
27 Kanellis J, Ma FY, Kandane-Rathnayake R, Dowling JP, Polkinghorne KR, Bennett BL, Friedman GC, Nikolic-Paterson DJ. JNK signalling in human and experimental renal ischaemia/reperfusion injury. Nephrol Dial Transplant. 2010;25:2898-2908.   DOI
28 Evankovich J, Cho SW, Zhang R, Cardinal J, Dhupar R, Zhang L, Klune JR, Zlotnicki J, Billiar T, Tsung A. High mobility group box 1 release from hepatocytes during ischemia and reperfusion injury is mediated by decreased histone deacetylase activity. J Biol Chem. 2010;285:39888-39897.   DOI
29 Yan X, Pan B, Lv T, Liu L, Zhu J, Shen W, Huang X, Tian J. Inhibition of histone acetylation by curcumin reduces alcohol-induced fetal cardiac apoptosis. J Biomed Sci. 2017;24:1.   DOI
30 Tesch GH, Ma FY, Nikolic-Paterson DJ. ASK1: a new therapeutic target for kidney disease. Am J Physiol Renal Physiol. 2016;311:F373-F381.   DOI
31 Wang Y, Wang Y, Luo M, Wu H, Kong L, Xin Y, Cui W, Zhao Y, Wang J, Liang G, Miao L, Cai L. Novel curcumin analog C66 prevents diabetic nephropathy via JNK pathway with the involvement of p300/CBP-mediated histone acetylation. Biochim Biophys Acta. 2015;1852:34-46.   DOI
32 Li J, Chen P, Sinogeeva N, Gorospe M, Wersto RP, Chrest FJ, Barnes J, Liu Y. Arsenic trioxide promotes histone H3 phosphoacetylation at the chromatin of CASPASE-10 in acute promyelocytic leukemia cells. J Biol Chem. 2002;277:49504-49510.   DOI
33 Bao L, Diao H, Dong N, Su X, Wang B, Mo Q, Yu H, Wang X, Chen C. Histone deacetylase inhibitor induces cell apoptosis and cycle arrest in lung cancer cells via mitochondrial injury and p53 up-acetylation. Cell Biol Toxicol. 2016;32:469-482.   DOI
34 Li D, Zeng Z. Epigenetic regulation of histone H3 in the process of hepatocellular tumorigenesis. Biosci Rep. 2019;39:BSR20191815.   DOI
35 Ibrahim SG, El-Emam SZ, Mohamed EA, Abd Ellah MF. Dimethyl fumarate and curcumin attenuate hepatic ischemia/reperfusion injury via Nrf2/HO-1 activation and anti-inflammatory properties. Int Immunopharmacol. 2020;80:106131.   DOI
36 Guo C, Dong G, Liang X, Dong Z. Epigenetic regulation in AKI and kidney repair: mechanisms and therapeutic implications. Nat Rev Nephrol. 2019;15:220-239.   DOI
37 Ammon HP, Wahl MA. Pharmacology of Curcuma longa. Planta Med. 1991;57:1-7.   DOI
38 Marcu MG, Jung YJ, Lee S, Chung EJ, Lee MJ, Trepel J, Neckers L. Curcumin is an inhibitor of p300 histone acetylatransferase. Med Chem. 2006;2:169-174.   DOI
39 Wang X, Muhammad I, Sun X, Han M, Hamid S, Zhang X. Protective role of curcumin in ameliorating AFB1-induced apoptosis via mitochondrial pathway in liver cells. Mol Biol Rep. 2018;45:881-891.   DOI
40 Zhao W, Wu X, Wang Z, Pan B, Liu L, Liu L, Huang X, Tian J. Epigenetic regulation of phosphodiesterase 4d in restrictive cardiomyopathy mice with cTnI mutations. Sci China Life Sci. 2020;63:563-570.   DOI
41 Rewa O, Bagshaw SM. Acute kidney injury-epidemiology, outcomes and economics. Nat Rev Nephrol. 2014;10:193-207.   DOI
42 Awad AS, El-Sharif AA. Curcumin immune-mediated and anti-apoptotic mechanisms protect against renal ischemia/reperfusion and distant organ induced injuries. Int Immunopharmacol. 2011;11:992-996.   DOI
43 Kunduzova OR, Bianchi P, Pizzinat N, Escourrou G, Seguelas MH, Parini A, Cambon C. Regulation of JNK/ERK activation, cell apoptosis, and tissue regeneration by monoamine oxidases after renal ischemia-reperfusion. FASEB J. 2002;16:1129-1131.   DOI
44 Jankauskas SS, Pevzner IB, Andrianova NV, Zorova LD, Popkov VA, Silachev DN, Kolosova NG, Plotnikov EY, Zorov DB. The age-associated loss of ischemic preconditioning in the kidney is accompanied by mitochondrial dysfunction, increased protein acetylation and decreased autophagy. Sci Rep. 2017;7:44430.   DOI
45 Peng C, Zhang W, Zhao W, Zhu J, Huang X, Tian J. Alcohol-induced histone H3K9 hyperacetylation and cardiac hypertrophy are reversed by a histone acetylases inhibitor anacardic acid in developing murine hearts. Biochimie. 2015;113:1-9.   DOI
46 Fiorillo C, Becatti M, Pensalfini A, Cecchi C, Lanzilao L, Donzelli G, Nassi N, Giannini L, Borchi E, Nassi P. Curcumin protects cardiac cells against ischemia-reperfusion injury: effects on oxidative stress, NF-kappaB, and JNK pathways. Free Radic Biol Med. 2008;45:839-846.   DOI
47 Saat TC, van den Akker EK, IJzermans JN, Dor FJ, de Bruin RW. Improving the outcome of kidney transplantation by ameliorating renal ischemia reperfusion injury: lost in translation? J Transl Med. 2016;14:20.   DOI
48 Ditonno P, Impedovo SV, Palazzo S, Bettocchi C, Gesualdo L, Grandaliano G, Selvaggi FP, Battaglia M. Effects of ischemia-reperfusion injury in kidney transplantation: risk factors and early and longterm outcomes in a single center. Transplant Proc. 2013;45:2641-2644.   DOI