Simvastatin inhibits goblet cell hyperplasia and lung arginase in a mouse model of allergic asthma: A novel treatment for airway remodeling?

Translational Research

Volumn 156, Issue 6, 2010, Pages 335-349

  Zeki, Amir A ^a   Bratt, Jennifer M ^a   Rabowsky, Michelle ^a   Last, Jerold A ^a   Kenyon, Nicholas J ^a,b  

^a Center for Comparative Respiratory Biology and Medicine   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; HYDROXYPROLINE; MEVALONIC ACID; OVALBUMIN; SIMVASTATIN; TRANSFORMING GROWTH FACTOR BETA1;

AIRWAY; AIRWAY REMODELING; ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL HYPERPLASIA; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; ENZYME INHIBITION; GOBLET CELL HYPERPLASIA; IMMUNOHISTOCHEMISTRY; LUNG COMPLIANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS INHIBITION; SMOOTH MUSCLE FIBER;

EID: 78649245378     PISSN: 19315244     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.trsl.2010.09.003     Document Type: Article

References (62)

1. A.M. Vignola, F. Mirabella, and G. Costanzo Airway remodeling in asthma Chest 123 2003 417S 422S
2. S. Holgate Pathogenesis of asthma Clin Exp Allergy 38 2008 872 897
3. S.G. Royce, and M. Tang The effects of current therapies on airway remodeling in asthma and new possibilities for treatment and prevention Curr Mol Pharmacol 2 2009 169 181
4. D.N.R. Payne, A.V. Rogers, and E. Adelroth Early thickening of the reticular basement membrane in children with difficult asthma Am J Respir Crit Care Med 167 2003 78 82
5. N. Takeda, M. Kondo, S. Ito, Y. Ito, K. Shimokata, and H. Kume Role of RhoA inactivation in reduced cell proliferation of human airway smooth muscle by simvastatin Am J Respir Cell Mol Biol 35 2006 722 729
6. J.K. Liao, and U. Laufs Pleiotropic effects of statins Annu Rev Pharmacol Toxicol 45 2005 89 118
7. S.E. Alexeeff, A. Litonjua, D. Sparrow, P.S. Vokonas, and J. Schwartz Statin use reduces decline in lung function: VA Normative Aging Study Am J Respir Crit Care Med 176 2007 742 747
8. S. Janda, K. Park, J.M. FitzGerald, M. Etminan, and J. Swiston Statins in COPD: a systematic review Chest 136 2009 734 743
9. B. Camoretti-Mercado Targeting the airway smooth muscle for asthma treatment Transl Res 154 2009 165 174
10. E. Hothersall, C. McSharry, and N.C. Thomson Potential therapeutic role for statins in respiratory disease Thorax 61 2006 729 734
11. E.J. Hothersall, R. Chaudhuri, and C. McSharry Effects of atorvastatin added to inhaled corticosteroids on lung function and sputum cell counts in atopic asthma Thorax 63 2008 1070 1075
12. D. Menzies, A. Nair, K.T. Meldrum, D. Fleming, M. Barnes, and B.J. Lipworth Simvastatin does not exhibit therapeutic anti-inflammatory effects in asthma J Allergy Clin Immunol 119 2007 328 335
13. X.M. Ou, F.Q. Wen, and B.D. Uhal Simvastatin attenuates experimental small airway remodelling in rats Respirology 14 2009 734 745
14. J.H. Lee, D.S. Lee, and E.K. Kim Simvastatin inhibits cigarette smoking-induced emphysema and pulmonary hypertension in rat lungs Am J Respir Crit Care Med 172 2005 987 993
15. A.A. Zeki, L. Franzi, J. Last, and N.J. Kenyon Simvastatin inhibits airway hyperreactivity: implications for the mevalonate pathway and beyond Am J Respir Crit Care Med 180 2009 731 740
16. N.J. Kenyon, and J. Last Reversible and irreversible airway inflammation and fibrosis in mice exposed to inhaled ovalbumin Inflamm Res 54 2005 57 65
17. H. Maarsingh, A. Zuidhof, and I.S.T. Bos Arginase inhibition protects against allergen-induced airway obstruction, hyperresponsiveness, and inflammation Am J Respir Crit Care Med 178 2008 565 573
18. U. Mabalirajan, J. Aich, A. Agrawal, and B. Ghosh Mepacrine inhibits subepithelial fibrosis by reducing the expression of arginase and TGF-b1 in an extended subacute mouse model of allergic asthma Am J Physiol Lung Cell Mol Physiol 297 2009 411 419
19. M.L. North, N. Khanna, P.A. Marsden, H. Grasemann, and J.A. Scott Functionally important role for arginase 1 in the airway hyperresponsiveness of asthma Am J Physiol Lung Cell Mol Physiol 296 2009 911 920
20. K. Takemoto, K. Oginko, and M. Shibamori Transiently, paralleled upregulation of arginase and nitric oxide synthase and the effect of both enzymes on the pathology of asthma Am J Physiol Lung Cell Mol Physiol 293 2007 1419 1426
21. H. Liu, P. Drew, A.C. Gaugler, Y. Cheng, and G.A. Visner Pirfenidone inhibits lung allograft fibrosis through l-arginine-arginase pathway Am J Transplant 5 2005 1256 1263
22. V. Boutard, R. Havouis, B. Fouqueray, C. Philippe, J.P. Moulinoux, and L. Baud Transforming growth factor-beta stimulates arginase activity in macrophages. Implications for the regulation of macrophage cytotoxicity J Immunol 155 1995 2077 2084
23. J. Temelkovski, S. Hogan, D.P. Shepherd, P.S. Foster, and R.K. Kumar An improved murine model of asthma: selective airway inflammation, epithelial lesions and increased methacholine responsiveness following chronic exposure to aerosolized allergen Thorax 53 1998 849 856
24. N.J. Kenyon, R.W. Ward, and J.A. Last Airway fibrosis in a mouse model of airway inflammation Toxicol Appl Pharmacol 186 2003 90 100
25. N.J. Kenyon, J. Bratt, A.L. Linderholm, M.S. Last, and J.A. Last Arginases I and II in lungs of ovalbumin-sensitized mice exposed to ovalbumin: sources and consequences Toxicol Appl Pharmacol 230 2008 269 275
26. P.E. Silkoff, S. Wakita, and J. Chatkin Exhaled nitric oxide after beta2-agonist inhalation and spirometry in asthma Am J Respir Crit Care Med 159 1999 940 944
27. J. McManus Histological and histochemical uses of periodic acid Stain Techn 23 1948 99 108
28. J.M. Bratt, L. Franzi, A.L. Linderholm, M.S. Last, N.J. Kenyon, and J.A. Last Arginase enzymes in isolated airways from normal and nitric oxide synthase 2-knockout mice exposed to ovalbumin Toxicol Appl Pharmacol 234 2009 273 280
29. L. Xu, B. Hilliard, and R.J. Carmody Arginase and autoimmune inflammation in the central nervous system Immunology 110 2003 141 148
30. J.F. Woessner The determination of hydroxyproline in tissue and protein samples containing small proportions of this amino acid Arch Biochem Biophys 93 1961 440 447
31. O. Feron, C. Dessy, J.P. Desager, and J.L. Balligand Hydroxy- methylglutaryl-coenzyme A reductase inhibition promotes endothelial nitric oxide synthase activation through a decrease in caveolin abundance Circulation 103 2001 113 118
32. M. Hausding, A. Witteck, F. Rodriguez-Pascual, C. von Eichel-Streiber, U. Forstermann, and H. Kleinert Inhibition of small G proteins of the rho family by statins or clostridium difficile toxin B enhances cytokine-mediated induction of NO synthase II Br J Pharmacol 131 2000 553 561
33. M. Joyce, C.J. Kelly, G. Chen, and D.J. Bouchier-Hayes Pravastatin attenuates lower torso ischaemia-reperfusioninduced lung injury by upregulating constitutive endothelial nitric oxide synthase Eur J Vasc Endovasc Surg 21 2001 295 300
34. N.E. Kreiselmeier, N. Kraynack, D.A. Corey, and T.J. Kelley Statin-mediated correction of STAT1 signaling and inducible nitric oxide synthase expression in cystic fibrosis epithelial cells Am J Physiol Lung Cell Mol Physiol 285 2003 L1286 L1295
35. U. Laufs Beyond lipid-lowering: effects of statins on endothelial nitric oxide Eur J Clin Pharmacol 58 2003 719 731
36. D.Y. Kim, S. Ryu, J.E. Lim, Y.S. Lee, and J.Y. Ro Anti-inflammatory mechanism of simvastatin in mouse allergic asthma model Eur J Pharmacol 557 2007 76 86
37. X.M. Ou, B.D. Wang, F.Q. Wen, Y.L. Feng, X.Y. Huang, and J. Xiao Simvastatin attenuates lipopolysaccharide-induced airway mucus hypersecretion in rats Chin Med J 121 2008 1680 1687
38. D.R. Curran, and L. Cohn Advances in mucous cell metaplasia: a plug for mucus as a therapeutic focus in chronic airway disease Am J Respir Cell Mol Biol 42 2010 268 275
39. P. Jeffery Remodeling in asthma and chronic obstructive lung disease Am J Respir Crit Care Med 164 2001 S28 S38
40. J.M. Bratt, L. Franzi, A.L. Linderholm, E.M. O'Roark, N.J. Kenyon, and J.A. Last Arginase inhibition in airways from normal and nitric oxide synthase 2-knockout mice exposed to ovalbumin Toxicol Appl Pharmacol 242 2010 1 8
41. H. Maarsingh, J. Zaagsma, and H. Meurs Arginase: a key enzyme in the pathophysiology of allergic asthma opening novel therapeutic perspectives Br J Pharmacol 158 2009 652 664
42. N. Zimmermann, N. King, and J. Laporte Dissection of experimental asthma with DNA microarray analysis identifies arginase in asthma pathogenesis J Clin Invest 111 2003 1863 1874
43. C. Bergeron, L. Boulet, and N. Page Influence of cigarette smoke on the arginine pathway in asthmatic airways: increased expression of arginase I J Allergy Clin Immunol 119 2007 391 397
44. L.H. Wei, A.T. Jacobs, S.M. Morris, and L.J. Ignarro IL-4 and IL-13 upregulate arginase I expression by cAMP and JAK/STAT6 pathways in vascular smooth muscle cells Am J Physiol Cell Physiol 279 2000 248 256
45. M. Imamura, K. Okunishi, and H. Ohtsu Pravastatin attenuates allergic airway inflammation by suppressing antigen sensitization, interleukin 17 production and antigen presentation in the lung Thorax 64 2009 44 49
46. X.F. Ming, C. Barandier, and H. Viswambharan Thrombin stimulates human endothelial arginase enzymatic activity via RhoA/ROCK Pathway: implications for atherosclerotic endothelial dysfunction Circulation 110 2004 3708 3714
47. M.J. Romero, D. Platt, and H.E. Tawfik Diabetes-induced coronary vascular dysfunction involves increased arginase activity Circ Res 102 2008 95 102
48. S. Horowitz, D. Binion, and V.M. Nelson Increased arginase activity and endothelial dysfunction in human inflammatory bowel disease Am J Physiol Gastrointest Liver Physiol 292 2007 1323 1336
49. S. Kotamraju, C. Williams, and B. Kalyanaraman Statin-induced breast cancer cell death: role of inducible nitric oxide and arginase-dependent pathways Cancer Res 67 2007 7386 7394
50. C.Y. Ivashchenko, B.T. Bradley, Z. Ao, J. Leiper, P. Vallance, and D.G. Johns Regulation of the ADMA-DDAH system in endothelial cells: a novel mechanism for the sterol response element binding proteins, SREBP1c and -2 Am J Physiol Heart Circ Physiol 298 2010 251 258
51. A. Oguz, and M. Uzunlulu Short term fluvastatin treatment lowers serum asymmetric dimethylarginine levels in patients with metabolic syndrome Int Heart J 49 2008 303 311
52. T. Akiba, N. Kuroiwa, and A. Shimizu-Yabe expression and regulation of the gene for arginase i in mouse salivary glands: requirement of ccaat/enhancer-binding protein α for the expression in the parotid gland J Biochem 132 2002 621 627
53. J.E. Albina, E.J. Mahoney, J.M. Daley, D.E. Wesche, S.M. Morris, and J.S. Reichner Macrophage arginase regulation by CCAAT/enhancer-binding protein β Shock 23 2005 168 172
54. M.J. Gray, M. Poljakovic, D. Kepka-Lenhart, and S.M. Morris Induction of arginase I transcription by IL-4 requires a composite DNA response element for STAT6 and C/EBPβ Gene 353 2005 98 106
55. J. Dong, S. Fujii, and H. Li Interleukin-6 and mevastatin regulate plasminogen activator inhibitor-1 through CCAAT/enhancer-binding protein-δ Arterioscler Thromb Vasc Biol 25 2005 1078 1084
56. W. Mäuser, N. Perwitz, B. Meier, M. Fasshauer, and J. Klein Direct adipotropic actions of atorvastatin: differentiation state-dependent induction of apoptosis, modulation of endocrine function, and inhibition of glucose uptake Eur J Pharmacol 564 2007 37 46
57. C. Mayer, H. Gruber, and E.M. Landl Rosuvastatin reduces interleukin-6-induced expression of C-reactive protein in human hepatocytes in a STAT3- and C/EBP-dependent fashion Int J Clin Pharmacol Ther 45 2007 319 327
58. D.M. Murphy, I.A. Forrest, and P.A. Corris Simvastatin attenuates release of neutrophilic and remodeling factors from primary bronchial epithelial cells derived from stable lung transplant recipients Am J Physiol Lung Cell Mol Physiol 294 2008 592 599
59. T. Makinde, R. Murphy, and D.K. Agrawal The regulatory role of TGF-β in airway remodeling in asthma Immunol Cell Biol 85 2007 348 356
60. X.M. Ou, L.Y. Feng, and F.Q. Wen Simvastatin attenuates bleomycin-induced pulmonary fibrosis in mice Chin Med J 121 2008 1821 1829
61. J.P. Williams, E. Hernady, and C.J. Johnston Effect of administration of lovastatin on the development of late pulmonary effects after whole-lung irradiation in a murine model Radiat Res 161 2004 560 567
62. S.A. Chang, Y.J. Kim, and H.W. Lee Effect of rosuvastatin on cardiac remodeling, function, and progression to heart failure in hypertensive heart with established left ventricular hypertrophy Hypertension 54 2009 591 597