Quercetin prevents progression of disease in elastase/LPS-exposed mice by negatively regulating MMP expression

Respiratory Research

Volumn 11, Issue , 2010, Pages

  Ganesan, Shyamala ^a   Faris, Andrea N ^a   Comstock, Adam T ^a   Chattoraj, Sangbrita S ^a   Chattoraj, Asamanja ^a   Burgess, John R ^c   Curtis, Jeffrey L ^b   Martinez, Fernando J ^b   Zick, Suzanna ^b   Hershenson, Marc B ^a,b   Sajjan, Uma S ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; ELASTASE; GELATINASE B; HISTONE DEACETYLASE; HISTONE DEACETYLASE SIRT 1; HISTONE H4; LIPOPOLYSACCHARIDE; MACROPHAGE ELASTASE; MATRIX METALLOPROTEINASE; MESSENGER RNA; MUCIN 5AC; QUERCETIN; SIRTINOL; THIOBARBITURIC ACID REACTIVE SUBSTANCE; UNCLASSIFIED DRUG; PANCREATIC ELASTASE;

ANIMAL EXPERIMENT; ARTICLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLINICAL FEATURE; COMPLIANCE (PHYSICAL); CONTROLLED STUDY; DISEASE COURSE; DRUG EFFECT; ENZYME ACTIVITY; ENZYME REGULATION; GOBLET CELL METAPLASIA; LIPID PEROXIDATION; LUNG EMPHYSEMA; LUNG FUNCTION; MACROPHAGE; METAPLASIA; MOUSE; NONHUMAN; OXIDATIVE STRESS; PNEUMONIA; PROTEIN EXPRESSION; RESPIRATORY TRACT INFLAMMATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CHEMICALLY INDUCED DISORDER; COMPARATIVE STUDY; DRUG ANTAGONISM; ENZYMOLOGY; GENE EXPRESSION REGULATION; SWINE;

ANIMALS; CELLS, CULTURED; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LIPOPOLYSACCHARIDES; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED C57BL; PANCREATIC ELASTASE; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; QUERCETIN; SWINE;

EID: 79551577067     PISSN: 14659921     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/1465-9921-11-131     Document Type: Article

References (64)

1. Rahman I, Adcock IM. Oxidative stress and redox regulation of lung inflammation in COPD. Eur Respir J 2006, 28:219-242. 10.1183/09031936.06.00053805, 16816350.
2. MacNee W, Rahman I. Is oxidative stress central to the pathogenesis of chronic obstructive pulmonary disease?. Trends Mol Med 2001, 7:55-62. 10.1016/S1471-4914(01)01912-8, 11286755.
3. Sydbom A, Blomberg A, Parnia S, Stenfors N, Sandstrom T, Dahlen SE. Health effects of diesel exhaust emissions. Eur Respir J 2001, 17:733-746. 10.1183/09031936.01.17407330, 11401072.
4. Nowak D, Kasielski M, Antczak A, Pietras T, Bialasiewicz P. Increased content of thiobarbituric acid-reactive substances and hydrogen peroxide in the expired breath condensate of patients with stable chronic obstructive pulmonary disease: no significant effect of cigarette smoking. Respir Med 1999, 93:389-396. 10.1053/rmed.1999.0574, 10464820.
5. Chung KF, Adcock IM. Multifaceted mechanisms in COPD: inflammation, immunity, and tissue repair and destruction. Eur Respir J 2008, 31:1334-1356. 10.1183/09031936.00018908, 18515558.
6. Ito K, Ito M, Elliott WM, Cosio B, Caramori G, Kon OM, Barczyk A, Hayashi S, Adcock IM, Hogg JC, et al. Decreased histone deacetylase activity in chronic obstructive pulmonary disease. N Engl J Med 2005, 352:1967-1976. 10.1056/NEJMoa041892, 15888697.
7. Nakamaru Y, Vuppusetty C, Wada H, Milne JC, Ito M, Rossios C, Elliot M, Hogg J, Kharitonov S, Goto H, et al. A protein deacetylase SIRT1 is a negative regulator of metalloproteinase-9. FASEB J 2009, 23:2810-2819. 10.1096/fj.08-125468, 19376817.
8. Hasday JD, Bascom R, Costa JJ, Fitzgerald T, Dubin W. Bacterial endotoxin is an active component of cigarette smoke. Chest 1999, 115:829-835. 10.1378/chest.115.3.829, 10084499.
9. Larsson L, Szponar B, Pehrson C. Tobacco smoking increases dramatically air concentrations of endotoxin. Indoor Air 2004, 14:421-424. 10.1111/j.1600-0668.2004.00290.x, 15500635.
10. Sebastian A, Pehrson C, Larsson L. Elevated concentrations of endotoxin in indoor air due to cigarette smoking. J Environ Monit 2006, 8:519-522. 10.1039/b600706f, 16688352.
11. Jagielo PJ, Thorne PS, Watt JL, Frees KL, Quinn TJ, Schwartz DA. Grain dust and endotoxin inhalation challenges produce similar inflammatory responses in normal subjects. Chest 1996, 110:263-270. 10.1378/chest.110.1.263, 8681637.
12. Michel O, Duchateau J, Plat G, Cantinieaux B, Hotimsky A, Gerain J, Sergysels R. Blood inflammatory response to inhaled endotoxin in normal subjects. Clin Exp Allergy 1995, 25:73-79. 10.1111/j.1365-2222.1995.tb01005.x, 7728626.
13. Kaneko Y, Takashima K, Suzuki N, Yamana K. Effects of theophylline on chronic inflammatory lung injury induced by LPS exposure in Guinea pigs. Allergol Int 2007, 56:445-456. 10.2332/allergolint.O-07-490, 17965584.
14. Vernooy JH, Dentener MA, van Suylen RJ, Buurman WA, Wouters EF. Long-term intratracheal lipopolysaccharide exposure in mice results in chronic lung inflammation and persistent pathology. Am J Respir Cell Mol Biol 2002, 26:152-159.
15. Sajjan U, Ganesan S, Comstock AT, Shim J, Wang Q, Nagarkar DR, Zhao Y, Goldsmith AM, Sonstein J, Linn MJ, et al. Elastase- and LPS-exposed mice display altered responses to rhinovirus infection. Am J Physiol Lung Cell Mol Physiol 2009, 297:L931-944. 10.1152/ajplung.00150.2009, 2777490, 19748999.
16. Kandaswami C, Middleton E. Free radical scavenging and antioxidant activity of plant flavonoids. Adv Exp Med Biol 1994, 366:351-376.
17. Robak J, Gryglewski RJ. Flavonoids are scavengers of superoxide anions. Biochem Pharmacol 1988, 37:837-841. 10.1016/0006-2952(88)90169-4, 2830882.
18. Walker EH, Pacold ME, Perisic O, Stephens L, Hawkins PT, Wymann MP, Williams RL. Structural determinants of phosphoinositide 3-kinase inhibition by wortmannin, LY294002, quercetin, myricetin, and staurosporine. Mol Cell 2000, 6:909-919. 10.1016/S1097-2765(05)00089-4, 11090628.
19. Nanua S, Zick SM, Andrade JE, Sajjan US, Burgess JR, Lukacs NW, Hershenson MB. Quercetin blocks airway epithelial cell chemokine expression. Am J Respir Cell Mol Biol 2006, 35:602-610. 10.1165/rcmb.2006-0149OC, 2643278, 16794257.
20. Rogerio AP, Kanashiro A, Fontanari C, da Silva EV, Lucisano-Valim YM, Soares EG, Faccioli LH. Anti-inflammatory activity of quercetin and isoquercitrin in experimental murine allergic asthma. Inflamm Res 2007, 56:402-408. 10.1007/s00011-007-7005-6, 18026696.
21. Hwang MK, Song NR, Kang NJ, Lee KW, Lee HJ. Activation of phosphatidylinositol 3-kinase is required for tumor necrosis factor-alpha-induced upregulation of matrix metalloproteinase-9: its direct inhibition by quercetin. Int J Biochem Cell Biol 2009, 41:1592-1600. 10.1016/j.biocel.2009.01.014, 19401153.
22. Newcomb DC, Sajjan US, Nagarkar DR, Wang Q, Nanua S, Zhou Y, McHenry CL, Hennrick KT, Tsai WC, Bentley JK, et al. Human rhinovirus 1B exposure induces phosphatidylinositol 3-kinase-dependent airway inflammation in mice. Am J Respir Crit Care Med 2008, 177:1111-1121. 10.1164/rccm.200708-1243OC, 2383993, 18276942.
23. Mercer PF, Shute JK, Bhowmik A, Donaldson GC, Wedzicha JA, Warner JA. MMP-9, TIMP-1 and inflammatory cells in sputum from COPD patients during exacerbation. Respir Res 2005, 6:151. 10.1186/1465-9921-6-151, 1351193, 16372907.
24. Louhelainen N, Rytila P, Haahtela T, Kinnula VL, Djukanovic R. Persistence of oxidant and protease burden in the airways after smoking cessation. BMC Pulm Med 2009, 9:25. 10.1186/1471-2466-9-25, 2697135, 19473482.
25. Finlay GA, O'Driscoll LR, Russell KJ, D'Arcy EM, Masterson JB, FitzGerald MX, O'Connor CM. Matrix metalloproteinase expression and production by alveolar macrophages in emphysema. Am J Respir Crit Care Med 1997, 156:240-247.
26. Segura-Valdez L, Pardo A, Gaxiola M, Uhal BD, Becerril C, Selman M. Upregulation of gelatinases A and B, collagenases 1 and 2, and increased parenchymal cell death in COPD. Chest 2000, 117:684-694. 10.1378/chest.117.3.684, 10712992.
27. Zheng T, Zhu Z, Wang Z, Homer RJ, Ma B, Riese RJ, Chapman HA, Shapiro SD, Elias JA. Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase- and cathepsin-dependent emphysema. J Clin Invest 2000, 106:1081-1093. 10.1172/JCI10458, 301418, 11067861.
28. Hwang JW, Chung S, Sundar IK, Yao H, Arunachalam G, McBurney MW, Rahman I. Cigarette smoke-induced autophagy is regulated by SIRT1-PARP-1-dependent mechanism: Implication in pathogenesis of COPD. Aarch Biochem Biophy 2010, 500:203-209.
29. Tabak C, Arts IC, Smit HA, Heederik D, Kromhout D. Chronic obstructive pulmonary disease and intake of catechins, flavonols, and flavones: the MORGEN Study. Am J Respir Crit Care Med 2001, 164:61-64.
30. Santus P, Sola A, Carlucci P, Fumagalli F, Di Gennaro A, Mondoni M, Carnini C, Centanni S, Sala A. Lipid peroxidation and 5-lipoxygenase activity in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2005, 171:838-843. 10.1164/rccm.200404-558OC, 15579728.
31. Walda IC, Tabak C, Smit HA, Rasanen L, Fidanza F, Menotti A, Nissinen A, Feskens EJ, Kromhout D. Diet and 20-year chronic obstructive pulmonary disease mortality in middle-aged men from three European countries. Eur J Clin Nutr 2002, 56:638-643. 10.1038/sj.ejcn.1601370, 12080403.
32. Culpitt SV, Rogers DF, Fenwick PS, Shah P, De Matos C, Russell RE, Barnes PJ, Donnelly LE. Inhibition by red wine extract, resveratrol, of cytokine release by alveolar macrophages in COPD. Thorax 2003, 58:942-946. 10.1136/thorax.58.11.942, 1746526, 14586044.
33. Kode A, Rajendrasozhan S, Caito S, Yang SR, Megson IL, Rahman I. Resveratrol induces glutathione synthesis by activation of Nrf2 and protects against cigarette smoke-mediated oxidative stress in human lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 2008, 294:L478-488. 10.1152/ajplung.00361.2007, 18162601.
34. Biswas SK, McClure D, Jimenez LA, Megson IL, Rahman I. Curcumin induces glutathione biosynthesis and inhibits NF-kappaB activation and interleukin-8 release in alveolar epithelial cells: mechanism of free radical scavenging activity. Antioxidants & redox signaling 2005, 7:32-41.
35. Meja KK, Rajendrasozhan S, Adenuga D, Biswas SK, Sundar IK, Spooner G, Marwick JA, Chakravarty P, Fletcher D, Whittaker P, et al. Curcumin restores corticosteroid function in monocytes exposed to oxidants by maintaining HDAC2. Am J Respir Cell Mol Biol 2008, 39:312-323. 10.1165/rcmb.2008-0012OC, 2542449, 18421014.
36. Shishodia S, Potdar P, Gairola CG, Aggarwal BB. Curcumin (diferuloylmethane) down-regulates cigarette smoke-induced NF-kappaB activation through inhibition of IkappaBalpha kinase in human lung epithelial cells: correlation with suppression of COX-2, MMP-9 and cyclin D1. Carcinogenesis 2003, 24:1269-1279. 10.1093/carcin/bgg078, 12807725.
37. Suzuki M, Betsuyaku T, Ito Y, Nagai K, Odajima N, Moriyama C, Nasuhara Y, Nishimura M. Curcumin attenuates elastase- and cigarette smoke-induced pulmonary emphysema in mice. Am J Physiol Lung Cell Mol Physiol 2009, 296:L614-623. 10.1152/ajplung.90443.2008, 19168576.
38. Kasielski M, Nowak D. Long-term administration of N-acetylcysteine decreases hydrogen peroxide exhalation in subjects with chronic obstructive pulmonary disease. Respir Med 2001, 95:448-456. 10.1053/rmed.2001.1066, 11421501.
39. Maestrelli P, Paska C, Saetta M, Turato G, Nowicki Y, Monti S, Formichi B, Miniati M, Fabbri LM. Decreased haem oxygenase-1 and increased inducible nitric oxide synthase in the lung of severe COPD patients. Eur Respir J 2003, 21:971-976. 10.1183/09031936.03.00098203, 12797490.
40. Ichinose M, Sugiura H, Yamagata S, Koarai A, Shirato K. Increase in reactive nitrogen species production in chronic obstructive pulmonary disease airways. Am J Respir Crit Care Med 2000, 162:701-706.
41. Shinohara T, Kaneko T, Nagashima Y, Ueda A, Tagawa A, Ishigatsubo Y. Adenovirus-mediated transfer and overexpression of heme oxygenase 1 cDNA in lungs attenuates elastase-induced pulmonary emphysema in mice. Hum Gene Ther 2005, 16:318-327. 10.1089/hum.2005.16.318, 15812227.
42. Chen JC, Ho FM, Pei-Dawn Lee C, Chen CP, Jeng KC, Hsu HB, Lee ST, Wen Tung W, Lin WW. Inhibition of iNOS gene expression by quercetin is mediated by the inhibition of IkappaB kinase, nuclear factor-kappa B and STAT1, and depends on heme oxygenase-1 induction in mouse BV-2 microglia. Eur J Pharmacol 2005, 521:9-20. 10.1016/j.ejphar.2005.08.005, 16171798.
43. Comalada M, Ballester I, Bailon E, Sierra S, Xaus J, Galvez J, de Medina FS, Zarzuelo A. Inhibition of pro-inflammatory markers in primary bone marrow-derived mouse macrophages by naturally occurring flavonoids: analysis of the structure-activity relationship. Biochem Pharmacol 2006, 72:1010-1021. 10.1016/j.bcp.2006.07.016, 16934226.
44. Mu MM, Chakravortty D, Sugiyama T, Koide N, Takahashi K, Mori I, Yoshida T, Yokochi T. The inhibitory action of quercetin on lipopolysaccharide-induced nitric oxide production in RAW 264.7 macrophage cells. J Endotoxin Res 2001, 7:431-438. 10.1179/096805101101533034, 11753212.
45. Minamoto K, Harada H, Lama VN, Fedarau MA, Pinsky DJ. Reciprocal regulation of airway rejection by the inducible gas-forming enzymes heme oxygenase and nitric oxide synthase. J Exp Med 2005, 202:283-294. 10.1084/jem.20050377, 2213014, 16027238.
46. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 2000, 351:95-105. 10.1042/0264-6021:3510095, 1221339, 10998351.
47. Agullo G, Gamet-Payrastre L, Manenti S, Viala C, Remesy C, Chap H, Payrastre B. Relationship between flavonoid structure and inhibition of phosphatidylinositol 3-kinase: A comparison with tyrosine kinase and protein kinase C inhibition. Biochem Pharmocol 1997, 53:1649-1657.
48. Huang Y-T, Hwang J-J, Lee P-P, Ke F-C, Huang J-H, Huang C-J, Kandaswami C, Middleton E, Lee M-T. Effects of luteolin and quercetin, inhibitors of tyrosine kinase, on cell growth and metastasis-associated properties in A431 cells overexpressing epidermal growth factor receptor. Br J Pharmacol 1999, 128:999-1010. 10.1038/sj.bjp.0702879, 1571723, 10556937.
49. Peet GW, Li J. IkappaB kinases alpha and beta show a random sequential kinetic mechanism and are inhibited by staurosporine and quercetin. J Biol Chem 1999, 274:32655-32661. 10.1074/jbc.274.46.32655, 10551820.
50. Vlahos CJ, Matter WF, Hui KY, Brown RF. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 1994, 269:5241-5248.
51. Babusyte A, Stravinskaite K, Jeroch J, Lotvall J, Sakalauskas R, Sitkauskiene B. Patterns of airway inflammation and MMP-12 expression in smokers and ex-smokers with COPD. Respir Res 2007, 8:81. 10.1186/1465-9921-8-81, 2200652, 18001475.
52. Demedts IK, Morel-Montero A, Lebecque S, Pacheco Y, Cataldo D, Joos GF, Pauwels RA, Brusselle GG. Elevated MMP-12 protein levels in induced sputum from patients with COPD. Thorax 2006, 61:196-201. 10.1136/thx.2005.042432, 2080750, 16308335.
53. Ohnishi K, Takagi M, Kurokawa Y, Satomi S, Konttinen YT. Matrix metalloproteinase-mediated extracellular matrix protein degradation in human pulmonary emphysema. Lab Invest 1998, 78:1077-1087.
54. Deshmukh HS, McLachlan A, Atkinson JJ, Hardie WD, Korfhagen TR, Dietsch M, Liu Y, Di PY, Wesselkamper SC, Borchers MT, et al. Matrix metalloproteinase-14 mediates a phenotypic shift in the airways to increase mucin production. Am J Respir Crit Care Med 2009, 180:834-845. 10.1164/rccm.200903-0328OC, 2773913, 19661247.
55. Deshmukh HS, Shaver C, Case LM, Dietsch M, Wesselkamper SC, Hardie WD, Korfhagen TR, Corradi M, Nadel JA, Borchers MT, et al. Acrolein-activated matrix metalloproteinase 9 contributes to persistent mucin production. Am J Respir Cell Mol Biol 2008, 38:446-454. 10.1165/rcmb.2006-0339OC, 2274947, 18006877.
56. Park HJ, Lee CM, Jung ID, Lee JS, Jeong YI, Chang JH, Chun SH, Kim MJ, Choi IW, Ahn SC, et al. Quercetin regulates Th1/Th2 balance in a murine model of asthma. Internat Immunopharmacol 2009, 9:261-267.
57. Conquer JA, Maiani G, Azzini E, Raguzzini A, Holub BJ. Supplementation with quercetin markedly increases plasma quercetin concentration without effect on selected risk factors for heart disease in healthy subjects. J Nutr 1998, 128:593-597.
58. Hollman PC, van Trijp JM, Mengelers MJ, de Vries JH, Katan MB. Bioavailability of the dietary antioxidant flavonol quercetin in man. Cancer Lett 1997, 114:139-140. 10.1016/S0304-3835(97)04644-2, 9103273.
59. Harwood M, Danielewska-Nikiel B, Borzelleca JF, Flamm GW, Williams GM, Lines TC. A critical review of the data related to the safety of quercetin and lack of evidence of in vivo toxicity, including lack of genotoxic/carcinogenic properties. Food Chem Toxicol 2007, 45:2179-2205. 10.1016/j.fct.2007.05.015, 17698276.
60. Boots AW, Li H, Schins RP, Duffin R, Heemskerk JW, Bast A, Haenen GR. The quercetin paradox. Toxicol Appl Pharmacol 2007, 222:89-96. 10.1016/j.taap.2007.04.004, 17537471.
61. Biasutto L, Sassi N, Mattarei A, Marotta E, Cattelan P, Toninello A, Garbisa S, Zoratti M, Paradisi C. Impact of mitochondriotropic quercetin derivatives on mitochondria. Biochim Biophys Acta 2010, 1797:189-196. 10.1016/j.bbabio.2009.10.001, 19835835.
62. Papi A, Bellettato CM, Braccioni F, Romagnoli M, Casolari P, Caramori G, Fabbri LM, Johnston SL. Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. Am J Respir Crit Care Med 2006, 173:1114-1121. 10.1164/rccm.200506-859OC, 16484677.
63. Rajendrasozhan S, Yang SR, Kinnula VL, Rahman I. SIRT1, an antiinflammatory and antiaging protein, is decreased in lungs of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2008, 177:861-870. 10.1164/rccm.200708-1269OC, 2292827, 18174544.
64. Mahadeva R, Shapiro SD. Chronic obstructive pulmonary disease 3: Experimental animal models of pulmonary emphysema. Thorax 2002, 57:908-914. 10.1136/thorax.57.10.908, 1746206, 12324680.