Effects of Rho-kinase inhibition in lung tissue with chronic inflammation

Respiratory Physiology and Neurobiology

Volumn 192, Issue 1, 2014, Pages 134-146

  Righetti, Renato Fraga ^a   Pigati, Patricia Angeli da Silva ^a   Possa, Samantha Souza ^a   Habrum, Fábio Cetinic ^a   Xisto, Débora Gonçalves ^b   Antunes, Mariana Alves ^b   Leick, Edna Aparecida ^a   Prado, Carla Máximo ^c   Martins, Mílton de Arruda ^a   Rocco, Patrícia Rieken Macedo ^b   Tibério, Iolanda de Fátima Lopes Calvo ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Asthma; Distal lung; Inflammation; Rho kinase; Y 27632

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; 8 ISOPROSTAGLANDIN F2 ALPHA; ACTIN; COLLAGEN; GAMMA INTERFERON; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 13; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; OVALBUMIN; RHO KINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR BETA;

ALLERGIC DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC INFLAMMATION; COMPLIANCE (PHYSICAL); CONTROLLED STUDY; ELASTIC FIBER; ENZYME INHIBITION; EOSINOPHIL; EXTRACELLULAR MATRIX; GUINEA PIG; IMMUNE RESPONSE; LUNG ALVEOLUS WALL; LUNG MECHANICS; LUNG PARENCHYMA; LUNG RESISTANCE; LUNG SLICE; MALE; MORPHOMETRICS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; TH1 CELL; TH2 CELL;

ASTHMA; DISTAL LUNG; INFLAMMATION; RHO-KINASE; Y-27632;

ADMINISTRATION, INHALATION; AMIDES; ANALYSIS OF VARIANCE; ANIMALS; CHRONIC DISEASE; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; GUINEA PIGS; IMMUNOGLOBULIN G; LUNG; MALE; NITRIC OXIDE SYNTHASE TYPE II; OVALBUMIN; PNEUMONIA; PYRIDINES; RHO-ASSOCIATED KINASES; STRESS, MECHANICAL; TISSUE INHIBITOR OF METALLOPROTEINASE-1;

EID: 84892494880     PISSN: 15699048     EISSN: 18781519     Source Type: Journal    
DOI: 10.1016/j.resp.2013.12.012     Document Type: Article

References (66)

1. Aihara M., Dobashi K., Iizuka K., Nakazawa T., Mori M. Effect of Y-27632 on release of cytokines from peripheral T cells in asthmatic patients and normal subjects. Int. Immunopharmacol. 2004, 4:557-561.
2. Andersson C.K., Bergqvist A., Mori M., Mauad T., Bjermer L., Erjefält J.S. Mast cell-associated alveolar inflammation in patients with atopic uncontrolled asthma. J. Allergy Clin. Immunol. 2011, 127(4):905-912.
3. Angeli P., Prado C.M., Xisto D.G., Silva P.L., Pássaro C.P., Nakazato H.D., Leick-Maldonado E.A., Martins M.A., Rocco P.R., Tibério I.F. Effects of chronic l-Name treatment lung tissue mechanics, eosinophilic and extracellular matrix responses induced by chronic pulmonary inflammation. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 294(6):L1197-L1205.
4. Aristoteles L.R., Righetti R.F., Pinheiro N.M., Franco R.B., Starling C.M., da Silva J.C., Pigati P.A., Caperuto L.C., Prado C.M., Dolhnikoff M., Martins M.A., Leick E.A., Tibério I.F. Modulation of the oscillatory mechanics of lung tissue and the oxidative stress response induced by arginase inhibition in a chronic allergic inflammation model. BMC Pulm. Med. 2013, 13:52.
5. Burdyga T., Mitchell R.W., Ragozzino J., Ford L.E. Force and myosin light chain phosphorylation in dog airway smooth muscle activated in different ways. Respir. Physiol. Neurobiol. 2003, 16(137(2-3)):141-149.
6. Cavalcante F.S.A., Ito S., Brewer K., Sakai H., Alencar A.M., Almeida M.P., Andrade J.S., Majumdar A., Ingenito E.P., Suki B. Mechanical interactions between collagen and proteoglycans: implications for the stability of lung tissue. J. Appl. Physiol. 2005, 98:672-679.
7. Chiba Y., Matsusue K., Misawa M. RhoA, a possible target for treatment of airway hyperresponsiveness in bronchial asthma. J. Pharmacol. Sci. 2010, 114(3):239-247.
8. Ckless K., Van der Vliet A., Janssen-Heininger Y. Oxidative nitrosative stress and post-translational protein modifications: implications to lung structure-function relations. Arginase modulates NF-kappaB activity via a nitric oxide-dependent mechanism. Am. J. Respir. Cell Mol. Biol. 2007, 36:645-653.
9. Doussau F., Gasman S., Humeau Y., Vitiello F., Popoff M., Boquet P., Bader M.F., Poulain B. A Rho-related GTPase is involved in Ca(2+)-dependent neurotransmitter exocytosis. J. Biol. Chem. 2000, 275:7764-7770.
10. Fernandes L., D'Aprile A., Self G., McGuire M., Sew T., Henry P., Goldie R. A Rho-kinase inhibitor, Y-27632, reduces cholinergic contraction but not neurotransmitter release. Eur. J. Pharmacol. 2006, 21(550(1-3)):155-161.
11. Fredberg J.J., Bunk, DIngenito E.P., Shore S.A. Tissue resistance and the contractile state of lung parenchyma. J. Appl. Physiol. 1993, 74:1387-1397.
12. Fukata Y., Amano M., Kaibuchi K. Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganisation of non-muscle cells. Trends Pharmacol. Sci. 2001, 22:32-39.
13. Gosens R., Schaafsma D., Grootte Bromhaar M.M., Vrugt B., Zaagsma J., Meur,s H., Nelemans S.A. Growth factor-induced contraction of human bronchial smooth muscle is Rho-kinase-dependent. Eur. J. Pharmacol. 2004, 494:73-76.
14. Greenlee K.J., Werb Z., Kheradmand F. Matrix metalloproteinases in lung: multiple, multifarious, and multifaceted. Physiol. Rev. 2007, 87(1):69-98.
15. Hasan Z., Palani K., Rahman M., Zhang S., Syk I., Jeppsson B., Thorlacius H. Rho-kinase signaling regulates pulmonary infiltration of neutrophils in abdominal sepsis via attenuation of CXC chemokine formation and mac-1 expression on neutrophils. Shock 2012, 37(3):282-288.
16. Heasman S.J., Ridley A.J. Multiple roles for RhoA during T cell transendothelial migration. Small GTPases 2010, 1(3):174-179.
17. Holgate S. Pathogenesis of asthma. Clin. Exp. Allergy 2008, 38:872-897.
18. Hozawa S., Terada M., Hozawa M. Comparison of budesonide/formoterol turbuhaler with fluticasone/salmeterol diskus for treatment effects on small airway impairment and airway inflammation in patients with asthma. Pulm. Pharmacol. Ther. 2011, 24(5):571-576.
19. Iizuka K., Shimizy Y., Tsukagoshi H., Yoshii A., Harada T., Dobashi K. Evaluation of Y-27632, a Rho-kinase inhibitor, as a bronchodilator in guinea pigs. Eur. J. Pharmacol. 2000, 406:273-279.
20. Janssen L.J. Isoprostanes: an overview and putative roles in pulmonary pathophysiology. Am. J. Physiol. Lung Cell. Mol. Physiol. 2001, 280:L1067-L1082.
21. Lambert E., Dassé E., Haye B., Petitfrère E. TIMPs as multifacial proteins. Crit. Rev. Oncol. Hematol. 2004, 49(3):187-198.
22. Lanças T., Kasahara D.I., Prado C.M., Tibério I.F., Martins M.A., Dolhnikoff M. Comparison of early and late responses to antigen of sensitized guinea pig parenchymal lung strips. J. Appl. Physiol. 2006, 100(5):161.
23. Lantz C.S., Min B., Tsai M., Chatterjea D., Dranoff G., Galli S.J. IL-3 is required for increases in blood basophils in nematode infection in mice and can enhance IgE-dependent IL-4 production by basophils in vitro. Lab Invest. 2008, 88(11):1134-1142.
24. Lim D.H., Cho J.Y., Miller M., McElwain K., McElwain S., Broide D.H. Reduced peribronchial fibrosis in allergen-challenged MMP-9-deficient mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006, 291:L265-L271.
25. López-Aguilar J., Romero P.V. Effect of elastase pretreatment on rat lung strip induced constriction. Respir. Physiol. 1998, 113(3):239-246.
26. Kapanci Y., Assimacopoulos, AIrle.C., Zwahlen A., Gabbiani G. Contractile interstitial cells' in pulmonary alveolar septa: a possible regulator of ventilation/perfusion ratio?. J. Cell Biol. 1974, 60:375-392.
27. Kelly E.A., Jarjour N.N. Role of matrix metalloproteinases in asthma. Curr. Opin. Pulm. Med. 2003, 9(1):28-33.
28. Kume H. RhoA/Rho-kinase as a therapeutic target in asthma. Curr. Med. Chem. 2008, 15(27):2876-2885.
29. Martin R.J. Therapeutic significance of distal airway inflammation in asthma. J. Allergy Clin. Immunol. 2002, 109(2 Suppl):S447-S460.
30. Martin R.J. Exploring the distal lung: new direction in asthma. Isr. Med. Assoc. J. 2008, 10(12):846-849.
31. McGown C.M., Brown N.J., Hellewell P.G., Brookes Z.L.S. ROCK induced inflammation of the microcirculation during endotoxemia mediated by nitric oxide synthase. Microvasc. Res. 2011, 81:281-288.
32. Meyer-Schwesinger C., Dehde S., von Ruffer C., Gatzmeier S., Klug P., Wenzel U.O., Stahl R.A., Thaiss F., Meyer T.N. Rho kinase inhibition attenuates LPS-induced renal failure in mice in part by attenuation of NF-κB p65 signaling. Am. J. Physiol. Renal Physiol. 2009, 296:1088-1099.
33. Mijailovich S.M., Stamenovic D., Fredberg J.J. Toward a kinetic theory of connective tissue micromechanics. J. Appl. Physiol. 1993, 74:665-681.
34. Montuschi P., Curro D., Ragazzoni E., Preziosi P., Ciabattoni G. Anaphylasis increases 8-iso-prostaglandin F2alpha release from guinea-pig lung in vitro. Eur. J. Pharmacol. 1999, 365:59-64.
35. Mota I., Perini A. A heat labile mercaptoethanol susceptible homocytotropicantibody in the guinea pig. Life Sci. II 1970, 9:923-930.
36. Murphy G., Docherty A.J.P. The matrix metalloproteinases and their inhibitors. Am. J. Respir. Cell Mol. Biol. 1992, 7:120-125.
37. Nakashima A.S., Prado C.M., Lanças T., Ruiz V.C., Kasahara D.I., Leick-Maldonado E.A., Dolhnikoff M., Martins M.A., Tibério I.F. Oral tolerance attenuates changes in in vitro lung tissue mechanics and extracellular matrix remodeling induced by chronic allergic inflammation in guinea pigs. J. Appl. Physiol. 2008, 1778-1785.
38. Napetschnig J., Wu H. Molecular basis of NF-κB signaling. Annu. Rev. Biophys. 2013, 42:443-468.
39. National Institutes of Health/Health Research Extension Act of 1985, Public Law 99-158, November 20, 1985. "Animals in Research" U.S. Government Principles for the Utilization and Care of Vertebrate Animals Used in Testing, Research, and Training Public Health Service Policy on Humane Care and Use of Laboratory Animals. http://grants.nih.gov/grants/olaw/references/phspol.htm.
40. Olson N., Kasahara D.I., Hristova M., Bernstein R., Janssen-Heininger Y., van der Vliet A. Modulation of NF-κB and hypoxia-inducible factor: 1 by S-nitrosoglutathione does not alter allergic airway inflammation in mice. Am. J. Respir. Cell Mol. Biol. 2011, 44(6):813-823.
41. Pantano C., Ather J.L., Alcorn J.F., Poynter M.E., Brown A.L., Guala A.S., Beuschel S.L., Allen G.B., Whittaker L.A., Bevelander M., Irvin C.G., Janssen-Heininger Y.M.W. Nuclear factor-B activation in airway epithelium induces inflammation and hyperresponsiveness. Am. J. Respir. Crit. Care Med. 2008, 177:959-969.
42. Parks W.C., Shapiro S.D. Matrix metalloproteinases in lung biology. Respir. Res. 2001, 2(1):10-19.
43. Prado C.M., Leick-Maldonado E.A., Kasahara D.I., Capelozzi V.L., Martins M.A., Tibério I.F. Effects of acute and chronic nitric oxide in an experimental model of chronic pulmonary allergicinflammation in guinea pigs. Am. J. Physiol. Lung Cell. Mol. Physiol. 2005, 289(4):L677-L683.
44. Prado C.M., Yano L., Rocha G., Starling C.M., Capelozzi V.L., Leick-Maldonado E.A., Martins M.A., Tibério I.F. Effects of inducible nitric oxide synthase inhibition in bronchial vascular remodeling-induced by chronic allergic pulmonary inflammation. Exp. Lung Res. 2011, 37(5):259-268.
45. Prasain N., Stevens T. The actin cytoskeleton in endothelial cell phenotypes. Microvasc. Res. 2009, 77:53-63.
46. Possa S.S., Charafeddine H.T., Righetti R.F., da Silva P.A., Almeida-Reis R., Saraiva-Romanholo B.M., Perini A., Prado C.M., Leick-Maldonado E.A., Martins M.A., Tibério I.F. Rho-kinase inhibition attenuates airway responsiveness, inflammation, matrix remodeling, and oxidative stress activation induced by chronic inflammation. Am. J. Physiol. Lung Cell. Mol. Physiol. 2012, 303(11):L939-L952.
47. Poynter M.E., Cloots R., Van Woerkom T., Butnor K.J., Vacek P., Taatjes D.J., Irvin C.G., Janssen-Heininger Y.M. NF-κB: activation in airways modulates allergic inflammation but not hyperresponsiveness. J. Immunol. 2004, 173:7003-7009.
48. Reis F.G., Marques R.H., Starling C.M., Almeida-Reis R., Vieira R.P., Cabido C.T., Silva L.F., Lanças T., Dolhnikoff M., Martins M.A., Leick-Maldonado E.A., Prado C.M., Tibério I.F. Stress amplifies lung tissue mechanics, inflammation and oxidative stress induced by chronic inflammation. Exp. Lung Res. 2012, 38(7):344-354.
49. Ricciardolo F.L.M., Sterk P.J., Gaston B., Folkerts G. Nitric oxide in health and disease of the respiratory system. Physiol. Ver. 2004, 84:731-765.
50. Rocco P.R., Negri E.M., Kurtz P.M., Vasconcellos F.P., Silva G.H., Capelozzi V.L., Romero P.V., Zin W.A. Lung tissue mechanics and extracellular matrix remodeling in acute lung injury. Am. J. Respir. Crit. Care Med. 2001, 164:1067-1071.
51. Romero P.V., Rodriguez B., Lopez-Aguilar J., Manresa F. Parallel airways inhomogeneity and lung tissue mechanics in transition to constricted state in rabbits. J. Appl. Physiol. 1998, 84:1040-1047.
52. Romero P.V., Zin W.A., Lopez-Aguilar J. Frequency characteristics of lung tissue strip during passive stretch and induced pneumoconstriction. J. Appl. Physiol. 2001, 91(2):882-890.
53. Ruiz-Schütz V.C., Drewiacki T., Nakashima A.S., Arantes-Costa F.M., Prado C.M., Kasahara D.I., Leick-Maldonado E.A., Martins M.A., Tibério I.F. Oral tolerance attenuates airway inflammation and remodeling in a model of chronic pulmonary allergic inflammation. Respir. Physiol. Neurobiol. 2009, 165:13-21.
54. Salerno F.G., Barbaro M.P., Toungoussova O., Carpagnano E., Guido P., Spanevello A. The extracellular matrix of the lung and airway responsiveness in asthma. Monaldi Arch. Chest Dis. 2009, 71(1):27-30.
55. Schaafsma D., Bos S.T., Zuidhof A.B., Zaagsma J., Meurs H. The inhaled Rho kinase inhibitor Y-27632 protects against allergen-induced acute bropnchoconstriction, airway hyperresponsiveness, and inflammation. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 295:L214-L219.
56. Schaafsma D., Dueck G., Ghavami S., Kroeker A., Mutawe M.M., Hauff K., Xu F.Y., McNeill K.D., Unruh H., Hatch G.M., Halayko A.J. Themevalonate cascade as a target to suppress extracellular matrix synthesis by human airway smooth muscle. Am. J. Respir. Cell. Mol. Biol. 2011, 44:394-403.
57. Simões S.M., dos Santos M.A., da Silva Oliveira M., Fontes E.S., Fernezlian S., Garippo A.L., Castro I., Castro F.F., de Arruda Martins M., Saldiva P.H., Mauad T., Dolhnikoff M. Inflammatory cell mapping of the respiratory tract in fatal asthma. Clin. Exp. Allergy 2005, 35(5):602-611.
58. Starling C.M., Prado C.M., Leick-Maldonado E.A., Lanças T., Reis F.G., Aristóteles L.R., Dolhnikoff M., Martins M.A., Tibério I.F. Inducible nitric oxide synthase inhibition attenuates lung tissue responsiveness and remodeling in a model of chronic pulmonary inflammation in guinea pigs. Respir. Physiol. Neurobiol. 2009, 165(2-3):185-194.
59. Taki F., Kume H., Kobayashi T., Ohta H., Aratake H., Shimokata K. Effects of Rho-kinase inactivation on eosinophilia and hyper-reactivity in murine airways by allergen challenges. Clin. Exp. Allergy 2007, 37:599-607.
60. Tibério I.F., Turco G.M., Leick-Maldonado E.A., Sakae R.S., Paiva S.O., do Patrocínio M., Warth T.N., Lapa e Silva J.R., Saldiva P.H., Martins M.A. Effects of neurokinin depletion on airway inflammation induced by chronic antigen exposure. Am. J. Respir. Crit. Care Med. 1997, 155(5):1739-1747.
61. Uehata M., Ishizaki T., Satoh H., Ono T., Kawahara T., Morishita T. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 1997, 389:990-994.
62. Vignola A.M., Mirabella F., Constanzo G., Di Giorgi R., Gjomarkaj M., Bellia V., Bonsignore G. Airway remodeling in asthma. Chest 2003, 123:417S-422S.
63. Xia Y., Roman L.J., Masters B.S., Zweier J.L. Inducible nitricoxide synthase generates superoxide from the reductase domain. J. Biol. Chem. 1998, 273:22635-22639.
64. Xisto D.G., Farias L.L., Ferreira H.C., Pincanco M.R., Amitrano D., Lapa e Silva J.R., Negri E.M., Carnielli D., Silva L.F., Capelozzi V.L., Faffe D.S., Zin W.A., Rocco P.M. Lung parenchyma remodeling in a murine model of chronic allergic inflammation. Am. J. Respir. Crit. Care Med. 2005, 171:829-837.
65. Yoshii A., Iizuka K., Dobashi K., Horie T., Harada T., Nakazawa T. Relaxation of contracted rabbit tracheal and human bronchial smooth muscle by Y-27632 through inhibition of Ca2+ sensitization. Am. J. Respir. Cell Mol. Biol. 1999, 20:1190-1200.
66. Zhou H., Zhang K.X., Li Y.J., Guo B.Y., Wang M., Wang M. Fasudil hydrochloride hydrate, a Rho-kinase inhibitor, suppresses high glucose-induced proliferation and collagen synthesis in rat cardiac fibroblasts. Clin. Exp. Pharmacol. Physiol. 2011, 38(6):387-394.