Honokiol ameliorates renal fibrosis by inhibiting extracellular matrix and pro-inflammatory factors in vivo and in vitro

British Journal of Pharmacology

Volumn 163, Issue 3, 2011, Pages 586-597

  Chiang, Chih Kang ^a,c   Sheu, Meei Ling ^b   Lin, Yi Wei ^a   Wu, Cheng Tien ^a   Yang, Chin Ching ^a   Chen, Min Wei ^a   Hung, Kuan Yu ^c   Wu, Kuan Dun ^c   Liu, Shing Hwa ^a,c  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

chronic kidney disease; honokiol; inflammation; renal fibrosis; transforming growth factor 1; unilateral ureteral obstruction

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; COLLAGEN TYPE 1ALPHA; CONNECTIVE TISSUE GROWTH FACTOR; FIBRINOGEN; FIBRONECTIN; FIBRONECTIN 1; FIREFLY LUCIFERASE; HONOKIOL; INTERCELLULAR ADHESION MOLECULE 1; MACROPHAGE DERIVED CHEMOKINE; MESSENGER RNA; PLASMINOGEN ACTIVATOR INHIBITOR 1; SCLEROPROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL LINE; CELL STIMULATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISEASE MODEL; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; KIDNEY FIBROSIS; KIDNEY TUBULE CELL; MALE; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; RAT; TRANSCRIPTION REGULATION; TUBULOINTERSTITIAL FIBROSIS; UPREGULATION; URETER OBSTRUCTION; WESTERN BLOTTING;

ACTINS; ANIMALS; BIPHENYL COMPOUNDS; CELL LINE; CHEMOKINE CCL2; CONNECTIVE TISSUE GROWTH FACTOR; EXTRACELLULAR MATRIX PROTEINS; FIBROSIS; GENES, REPORTER; INTERCELLULAR ADHESION MOLECULE-1; KIDNEY; KIDNEY TUBULES; LIGNANS; LUCIFERASES; MALE; PHOSPHORYLATION; RATS; RATS, WISTAR; RNA, MESSENGER; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; URETERAL OBSTRUCTION;

EID: 79955888192     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01242.x     Document Type: Article

References (44)

1. Alpers CE, Hudkins KL, Floege J, Johnson RJ, (1994). Human renal cortical interstitial cells with some features of smooth muscle cells participate in tubulointerstitial and crescentic glomerular injury. J Am Soc Nephrol 5: 201-209.
2. Brenner BM, Cooper ME, de Zeeuw D, Keane WF, Mitch WE, Parving HH, et al,. (2001). Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N Engl J Med 345: 861-869.
3. Burns WC, Twigg SM, Forbes JM, Pete J, Tikellis C, Thallas-Bonke V, et al,. (2006). Connective tissue growth factor plays an important role in advanced glycation end product-induced tubular epithelial-to-mesenchymal transition: implications for diabetic renal disease. J Am Soc Nephrol 17: 2484-2494. (Pubitemid 44300964)
4. Castro AF, Coresh J, (2009). CKD surveillance using laboratory data from the population-based National Health and Nutrition Examination Survey (NHANES). Am J Kidney Dis 53 (Suppl. 3): S46-S55.
5. Chiang CK, Sheu ML, Hung KY, Wu KD, Liu SH, (2006). Honokiol, a small molecular weight natural product, alleviates experimental mesangial proliferative glomerulonephritis. Kidney Int 70: 682-689.
6. Derynck R, Zhang Y, Feng XH, (1998). Smads: transcriptional activators of TGF-beta responses. Cell 95: 737-740. (Pubitemid 29014453)
7. Eddy AA, Fogo AB, (2006). Plasminogen activator inhibitor-1 in chronic kidney disease: evidence and mechanisms of action. J Am Soc Nephrol 17: 2999-3012. (Pubitemid 44707760)
8. Eknoyan G, Lameire N, Barsoum R, Eckardt KU, Levin A, Levin N, et al,. (2004). The burden of kidney disease: improving global outcomes. Kidney Int 66: 1310-1314. (Pubitemid 39302630)
9. Fan JM, Ng YY, Hill PA, Nikolic-Paterson DJ, Mu W, Atkins RC, et al,. (1999). Transforming growth factor-beta regulates tubular epithelial- myofibroblast transdifferentiation in vitro. Kidney Int 56: 1455-1467. (Pubitemid 29451252)
10. Fogo AB, (1999). Mesangial matrix modulation and glomerulosclerosis. Exp Nephrol 7: 147-159. (Pubitemid 29210177)
11. Fogo AB, (2003). Renal fibrosis: not just PAI-1 in the sky. J Clin Invest 112: 326-328. (Pubitemid 38063760)
12. Garcia-Sanchez O, Lopez-Hernandez FJ, Lopez-Novoa JM, (2010). An integrative view on the role of TGF-beta in the progressive tubular deletion associated with chronic kidney disease. Kidney Int 77: 950-955.
13. Gore-Hyer E, Shegogue D, Markiewicz M, Lo S, Hazen-Martin D, Greene EL, et al,. (2002). TGF-beta and CTGF have overlapping and distinct fibrogenic effects on human renal cells. Am J Physiol Renal Physiol 283: F707-F716. (Pubitemid 35033958)
14. Grande MT, Perez-Barriocanal F, Lopez-Novoa JM, (2010). Role of inflammation in tubulo-interstitial damage associated to obstructive nephropathy. J Inflamm (Lond) 7: 19.
15. Grupp C, Lottermoser J, Cohen DI, Begher M, Franz HE, Muller GA, (1997). Transformation of rat inner medullary fibroblasts to myofibroblasts in vitro. Kidney Int 52: 1279-1290. (Pubitemid 27496057)
16. Gupta S, Clarkson MR, Duggan J, Brady HR, (2000). Connective tissue growth factor: potential role in glomerulosclerosis and tubulointerstitial fibrosis. Kidney Int 58: 1389-1399.
17. Heldin CH, Miyazono K, Dijke P, (1997). TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390: 465-471. (Pubitemid 28013118)
18. Hewitson TD, (2009). Renal tubulointerstitial fibrosis: common but never simple. Am J Physiol Renal Physiol 296: F1239-F1244.
19. Hou FF, Zhang X, Zhang GH, Xie D, Chen PY, Zhang WR, et al,. (2006). Efficacy and safety of benazepril for advanced chronic renal insufficiency. N Engl J Med 354: 131-140. (Pubitemid 43076710)
20. Iwano M, Plieth D, Danoff TM, Xue C, Okada H, Neilson EG, (2002). Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 110: 341-350. (Pubitemid 34847966)
21. Izuhara Y, Nangaku M, Inagi R, Tominaga N, Aizawa T, Kurokawa K, et al,. (2005). Renoprotective properties of angiotensin receptor blockers beyond blood pressure lowering. J Am Soc Nephrol 16: 3631-3641. (Pubitemid 46211284)
22. Kaneto H, Morrissey J, Klahr S, (1993). Increased expression of TGF-beta 1 mRNA in the obstructed kidney of rats with unilateral ureteral ligation. Kidney Int 44: 313-321. (Pubitemid 23228685)
23. Keeton MR, Curriden SA, van Zonneveld AJ, Loskutoff DJ, (1991). Identification of regulatory sequences in the type 1 plasminogen activator inhibitor gene responsive to transforming growth factor beta. J Biol Chem 266: 23048-23052. (Pubitemid 21908758)
24. Klahr S, Morrissey J, (2002). Obstructive nephropathy and renal fibrosis. Am J Physiol Renal Physiol 283: F861-F875. (Pubitemid 35192452)
25. Lee J, Jung E, Park J, Jung K, Lee S, Hong S, et al,. (2005). Anti-inflammatory effects of magnolol and honokiol are mediated through inhibition of the downstream pathway of MEKK-1 in NF-kappaB activation signaling. Planta Med 71: 338-343. (Pubitemid 40676458)
26. Li JH, Zhu HJ, Huang XR, Lai KN, Johnson RJ, Lan HY, (2002). Smad7 inhibits fibrotic effect of TGF-Beta on renal tubular epithelial cells by blocking Smad2 activation. J Am Soc Nephrol 13: 1464-1472. (Pubitemid 34579235)
27. Lin SL, Chen RH, Chen YM, Chiang WC, Lai CF, Wu KD, et al,. (2005). Pentoxifylline attenuates tubulointerstitial fibrosis by blocking Smad3/4-activated transcription and profibrogenic effects of connective tissue growth factor. J Am Soc Nephrol 16: 2702-2713.
28. Liou KT, Shen YC, Chen CF, Tsao CM, Tsai SK, (2003). The anti-inflammatory effect of honokiol on neutrophils: mechanisms in the inhibition of reactive oxygen species production. Eur J Pharmacol 475: 19-27.
29. Liu Y, (2004). Epithelial to mesenchymal transition in renal fibrogenesis: pathologic significance, molecular mechanism, and therapeutic intervention. J Am Soc Nephrol 15: 1-12. (Pubitemid 38020692)
30. Liu Y, (2006). Renal fibrosis: new insights into the pathogenesis and therapeutics. Kidney Int 69: 213-217. (Pubitemid 43323069)
31. Liu Y, (2010). New insights into epithelial-mesenchymal transition in kidney fibrosis. J Am Soc Nephrol 21: 212-222.
32. Noronha IL, Fujihara CK, Zatz R, (2002). The inflammatory component in progressive renal disease-are interventions possible? Nephrol Dial Transplant 17: 363-368. (Pubitemid 34211128)
33. Park EJ, Zhao YZ, Kim YH, Lee BH, Sohn DH, (2005). Honokiol induces apoptosis via cytochrome c release and caspase activation in activated rat hepatic stellate cells in vitro. Planta Med 71: 82-84. (Pubitemid 40223358)
34. Remuzzi G, Bertani T, (1998). Pathophysiology of progressive nephropathies. N Engl J Med 339: 1448-1456. (Pubitemid 28516069)
35. Remuzzi G, Zoja C, Gagliardini E, Corna D, Abbate M, Benigni A, (1999). Combining an antiproteinuric approach with mycophenolate mofetil fully suppresses progressive nephropathy of experimental animals. J Am Soc Nephrol 10: 1542-1549. (Pubitemid 29297529)
36. Rerolle JP, Hertig A, Nguyen G, Sraer JD, Rondeau EP, (2000). Plasminogen activator inhibitor type 1 is a potential target in renal fibrogenesis. Kidney Int 58: 1841-1850.
37. Risdon RA, Sloper JC, De Wardener HE, (1968). Relationship between renal function and histological changes found in renal-biopsy specimens from patients with persistent glomerular nephritis. Lancet 2: 363-366.
38. Seo JY, Park J, Yu MR, Kim YS, Ha H, Lee HB, (2009). Positive feedback loop between plasminogen activator inhibitor-1 and transforming growth factor-beta1 during renal fibrosis in diabetes. Am J Nephrol 30: 481-490.
39. Sheu ML, Ho FM, Yang RS, Chao KF, Lin WW, Lin-Shiau SY, et al,. (2005). High glucose induces human endothelial cell apoptosis through a phosphoinositide 3-kinase-regulated cyclooxygenase-2 pathway. Arterioscler Thromb Vasc Biol 25: 539-545. (Pubitemid 40315675)
40. Sheu ML, Liu SH, Lan KH, (2007). Honokiol induces calpain-mediated glucose-regulated protein-94 cleavage and apoptosis in human gastric cancer cells and reduces tumor growth. PLoS ONE 2: e1096.
41. Sheu ML, Chiang CK, Tsai KS, Ho FM, Weng TI, Wu HY, et al,. (2008). Inhibition of NADPH oxidase-related oxidative stress-triggered signaling by honokiol suppresses high glucose-induced human endothelial cell apoptosis. Free Radic Biol Med 44: 2043-2050.
42. Son HJ, Lee HJ, Yun-Choi HS, Ryu JH, (2000). Inhibitors of nitric oxide synthesis and TNF-alpha expression from Magnolia obovata in activated macrophages. Planta Med 66: 469-471. (Pubitemid 30413511)
43. Subramanian SV, Polikandriotis JA, Kelm RJ, Jr, David JJ, Orosz CG, Strauch AR, (2004). Induction of vascular smooth muscle alpha-actin gene transcription in transforming growth factor beta1-activated myofibroblasts mediated by dynamic interplay between the Pur repressor proteins and Sp1/Smad coactivators. Mol Biol Cell 15: 4532-4543. (Pubitemid 39299102)
44. Yu CC, Hsu MJ, Kuo ML, Chen RF, Chen MC, Bai KJ, et al,. (2009). Thrombin-induced connective tissue growth factor expression in human lung fibroblasts requires the ASK1/JNK/AP-1 pathway. J Immunol 182: 7916-7927.