Pseudomonas aeruginosa elastase causes transient disruption of tight junctions and downregulation of PAR-2 in human nasal epithelial cells

Respiratory Research

Volumn 15, Issue 1, 2014, Pages

  Nomura, Kazuaki ^a   Obata, Kazufumi ^a   Keira, Takashi ^a   Miyata, Ryo ^a   Hirakawa, Satoshi ^a   Takano, Ken ichi ^a   Kohno, Takayuki ^a   Sawada, Norimasa ^a   Himi, Tetsuo ^a   Kojima, Takashi ^a  

^a SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Barrier function; Human nasal epithelial cells; PAR 2; Pseudomonas aeruginosa elastase; Signal transduction; Tight junctions

Indexed keywords

BACTERIAL ENZYME; BETA CATENIN; CLAUDIN 1; CLAUDIN 4; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; OCCLUDIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEASOME; PROTEIN KINASE C; PROTEIN ZO1; PROTEIN ZO2; PROTEINASE ACTIVATED RECEPTOR 2; PSEUDOMONAS AERUGINOSA ELASTASE; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TELOMERASE REVERSE TRANSCRIPTASE; TRICELLULIN; UNCLASSIFIED DRUG; UVOMORULIN; BACTERIAL PROTEIN; METALLOPROTEINASE; PANCREATIC ELASTASE; PSEUDOLYSIN, PSEUDOMONAS AERUGINOSA;

ARTICLE; CELL DISRUPTION; CELL FUNCTION; CELL STRUCTURE; EPITHELIUM CELL; FREEZE FRACTURE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; NOSE MUCOSA; PRIMARY CULTURE; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; TIGHT JUNCTION; WESTERN BLOTTING; BIOSYNTHESIS; CELL CULTURE; DOWN REGULATION; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENE SILENCING; GENETICS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

BACTERIAL PROTEINS; CELLS, CULTURED; DOWN-REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; METALLOENDOPEPTIDASES; NASAL MUCOSA; PANCREATIC ELASTASE; RECEPTOR, PAR-2; TIGHT JUNCTIONS;

EID: 84896700990     PISSN: 14659921     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/1465-9921-15-21     Document Type: Article

References (31)

1. Dulon S, Leduc D, Cottrell GS, D'Alayer J, Hansen KK, Bunnett NW, Hollenberg MD, Pidard D, Chignard M. Pseudomonas aeruginosa elastase disables proteinase-activated receptor 2 in respiratory epithelial cells. Am J Respir Cell Mol Biol 2005, 32:411-419. 10.1165/rcmb.2004-0274OC, 15705968.
2. Clark CA, Thomas LK, Azghani AO. Inhibition of protein kinase C attenuates Pseudomonas aeruginosa elastase-induced epithelial barrier disruption. Am J Respir Cell Mol Biol 2011, 45:1263-1271. 10.1165/rcmb.2010-0459OC, 21757681.
3. Ramakrishnan JB, Kingdom TT, Ramakrishnan VR. Allergic rhinitis and chronic rhinosinusitis: their impact on lower airways. Immunol Allergy Clin North Am 2013, 33:45-60. 10.1016/j.iac.2012.10.009, 23337064.
4. Döring G, Goldstein W, Röll A, Schiøtz PO, Høiby N, Botzenhart K. Role of Pseudomonas aeruginosa exoenzymes in lung infections of patients with cystic fibrosis. Infect Immun 1985, 49:557-562. 261205, 3928491.
5. Woods DE, Lam JS, Paranchych W, Speert DP, Campbell M, Godfrey AJ. Correlation of Pseudomonas aeruginosa virulence factors from clinical and environmental isolates with pathogenicity in the neutropenic mouse. Can J Microbiol 1997, 43:541-551. 10.1139/m97-077, 9226874.
6. Azghani AO, Miller EJ, Peterson BT. Virulence factors from Pseudomonas aeruginosa increase lung epithelial permeability. Lung 2000, 178:261-269. 10.1007/s004080000031, 11147311.
7. Azghani AO, Baker JW, Shetty S, Miller EJ, Bhat GJ. Pseudomonas aeruginosa elastase stimulates ERK signaling pathway and enhances IL-8 production by alveolar epithelial cells in culture. Inflamm Res 2002, 51:506-510. 10.1007/PL00012420, 12477080.
8. Leduc D, Beaufort N, de Bentzmann S, Rousselle JC, Namane A, Chignard M, Pidard D. The Pseudomonas aeruginosa LasB metalloproteinase regulates the human urokinase-type plasminogen activator receptor through domain-specific endoproteolysis. Infect Immun 2007, 75:3848-3858. 10.1128/IAI.00015-07, 1951998, 17517866.
9. Beaufort N, Seweryn P, de Bentzmann S, Tang A, Kellermann J, Grebenchtchikov N, Schmitt M, Sommerhoff CP, Pidard D, Magdolen V. Activation of human pro-urokinase by unrelated proteases secreted by Pseudomonas aeruginosa. Biochem J 2010, 428:473-482. 10.1042/BJ20091806, 20337595.
10. Kida Y, Higashimoto Y, Inoue H, Shimizu T, Kuwano K. A novel secreted protease from Pseudomonas aeruginosa activates NF-kappaB through protease-activated receptors. Cell Microbiol 2008, 10:1491-1504. 10.1111/j.1462-5822.2008.01142.x, 18331590.
11. Cosgrove S, Chotirmall SH, Greene CM, McElvaney NG. Pulmonary proteases in the cystic fibrosis lung induce interleukin 8 expression from bronchial epithelial cells via a heme/meprin/epidermal growth factor receptor/Toll-like receptor pathway. J Biol Chem 2011, 286:7692-7704. 10.1074/jbc.M110.183863, 3045023, 21193404.
12. Cocks TM, Fong B, Chow JM, Anderson GP, Frauman AG, Goldie RG, Henry PJ, Carr MJ, Hamilton JR, Moffatt JD. A protective role for protease-activated receptors in the airways. Nature 1999, 398:156-160. 10.1038/18223, 10086357.
13. Ebeling C, Forsythe P, Ng J, Gordon JR, Hollenberg M, Vliagoftis H. Proteinase-activated receptor 2 activation in the airways enhances antigen-mediated airway inflammation and airway hyperresponsiveness through different pathways. J Allergy Clin Immunol 2005, 115:623-630.
14. Knight DA, Lim S, Scaffidi AK, Roche N, Chung KF, Stewart GA, Thompson PJ. Protease-activated receptors in human airways: upregulation of PAR-2 in respiratory epithelium from patients with asthma. J Allergy Clin Immunol 2001, 108:797-803.
15. Yoshida T, Matsuwaki Y, Asaka D, Hama T, Otori N, Moriyama H. The expression of protease-activated receptors in chronic rhinosinusitis. Int Arch Allergy Immunol 2013, 161:138-146. 10.1159/000350386, 23711865.
16. Yeoh S, Church M, Lackie P, McGill J, Mota M, Hossain P. Increased conjunctival expression of protease activated receptor 2 (PAR-2) in seasonal allergic conjunctivitis: a role for abnormal conjunctival epithelial permeability in disease pathogenesis?. Br J Ophthalmol 2011, 95:1304-1308. 10.1136/bjo.2010.191221, 21558289.
17. Takano K, Kojima T, Go M, Murata M, Ichimiya S, Himi T, Sawada N. HLA-DR- and CD11c-positive dendritic cells penetrate beyond well-developed epithelial tight junctions in human nasal mucosa of allergic rhinitis. J Histochem Cytochem 2005, 53:611-619. 10.1369/jhc.4A6539.2005, 15872054.
18. Holgate ST. Epithelium dysfunction in asthma. J Allergy Clin Immunol 2007, 120:1233-1244.
19. Schleimer RP, Kato A, Kern R, Kuperman D, Avila PC. Epithelium: at the interface of innate and adaptive immune responses. J Allergy Clin Immunol 2007, 120:1279-1284. 2810155, 17949801.
20. Tsukita S, Furuse M, Itoh M. Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2001, 2:285-293. 10.1038/35067088, 11283726.
21. Sawada N, Murata M, Kikuchi K, Osanai M, Tobioka H, Kojima T, Chiba H. Tight junctions and human diseases. Med Elecron Microsc 2003, 36:147-156.
22. Schneeberger EE, Lynch RD. The tight junction: a multifunctional complex. Am J Physiol Cell Physiol 2004, 286:1213-1228.
23. Kojima T, Murata M, Yamamoto T, Lan M, Imamura M, Son S, Takano K, Yamaguchi H, Ito T, Tanaka S, Chiba H, Hirata K, Sawada N. Tight junction proteins and signal transduction pathways in hepatocytes. Histol Histopathol 2009, 24:1463-1472.
24. Ohkuni T, Kojima T, Ogasawara N, Masaki T, Ninomiya T, Kikuchi S, Go M, Takano K, Himi T, Sawada N. Expression and localization of tricellulin in human nasal epithelial cells in vivo and in vitro. Med Mol Morphol 2009, 42:204-211. 10.1007/s00795-009-0470-y, 20033365.
25. Kojima T, Go M, Takano K, Kurose M, Ohkuni T, Koizumi J, Kamekura R, Ogasawara N, Masaki T, Fuchimoto J, Obata K, Hirakawa S, Nomura K, Keira T, Miyata R, Fujii N, Tsutsumi H, Himi T, Sawada N. Regulation of tight junctions in upper airway epithelium. Biomed Res Int 2013, 2013:947072. 3591135, 23509817.
26. Kurose M, Kojima T, Koizumi JI, Kamekura R, Ninomiya T, Murata M, Ichimiya S, Osanai M, Chiba H, Himi T, Sawada N. Induction of claudins in passaged hTERT-transfected human nasal epithelial cells with an extended life span. Cell Tissue Res 2007, 330:63-74. 10.1007/s00441-007-0453-z, 17701057.
27. Koizumi J, Kojima T, Ogasawara N, Kamekura R, Kurose M, Go M, Harimaya A, Murata M, Osanai M, Chiba H, Himi T, Sawada N. Protein kinase C enhances tight junction barrier function of human nasal epithelial cells in primary culture by transcriptional regulation. Mol Pharmacol 2008, 74:432-442. 10.1124/mol.107.043711, 18477669.
28. Ohkuni T, Kojima T, Ogasawara N, Masaki T, Fuchimoto J, Kamekura R, Koizumi JI, Ichimiya S, Murata M, Tanaka S, Himi T, Sawada N. Poly(I:C) reduces expression of JAM-A and induces secretion of IL-8 and TNF-α via distinct NF-κB pathways in human nasal epithelial cells. Toxicol Appl Pharmacol 2011, 250:29-38. 10.1016/j.taap.2010.09.023, 20932985.
29. Obata K, Kojima T, Masaki T, Okabayashi T, Yokota S, Hirakawa S, Nomura K, Takasawa A, Murata M, Tanaka S, Fuchimoto J, Fujii N, Tsutsumi H, Himi T, Sawada N. Curcumin prevents replication of respiratory syncytial virus and the epithelial responses to it in human nasal epithelial cells. PLoS One 2013, 8:e70225. 10.1371/journal.pone.0070225, 3776807, 24058438.
30. Kooi C, Hodges RS, Sokol PA. Identification of neutralizing epitopes on Pseudomonas aeruginosa elastase and effects of cross-reactions on other thermolysin-like proteases. Infect Immun 1997, 65:472-477. 176082, 9009299.
31. Gonzalez-Mariscal L, Hernández S, Vega J. Inventions designed to enhance drug delivery across epithelial and endothelial cells through the paracellular pathway. Recent Pat Drug Deliv Formul 2008, 2:145-176. 10.2174/187221108784534117, 19075905.