Phosphatidylinositol 3-kinases pathway mediates lung caspase-1 activation and high mobility group box 1 production in a toluene-diisocyanate induced murine asthma model

Toxicology Letters

Volumn 236, Issue 1, 2015, Pages 25-33

  Liang, Junjie ^a   Zhao, Haijin ^a   Yao, Lihong ^a   Tang, Haixiong ^a   Dong, Hangming ^a   Wu, Yue ^a   Liu, Laiyu ^a   Zou, Fei ^a   Cai, Shaoxi ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Asthma; Caspase 1; HMGB1; PI3K; Toluene diisocyanate

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; IMMUNOGLOBULIN E; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 4; LUNG ENZYME; PHOSPHATIDYLINOSITOL 3 KINASE; TOLUENE DIISOCYANATE; CARRIER PROTEIN; CIAS1 PROTEIN, MOUSE; ENZYME INHIBITOR; HIGH MOBILITY GROUP B1 PROTEIN; HMGB1 PROTEIN, MOUSE;

AIRWAY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; CONTROLLED STUDY; ENZYME ACTIVATION; EOSINOPHIL; HYPERSENSITIVITY; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOREACTIVITY; LYMPHOCYTE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SUPERNATANT; AIRWAY RESISTANCE; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; DISEASE MODEL; DRUG EFFECTS; GERMFREE ANIMAL; IMMUNOLOGY; INHALATIONAL DRUG ADMINISTRATION; LUNG; METABOLISM; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; PROTEIN TRANSPORT; RANDOMIZATION; RESPIRATORY TRACT MUCOSA;

MURINAE; MUS;

ADMINISTRATION, INHALATION; AIRWAY RESISTANCE; ANIMALS; ASTHMA; CARRIER PROTEINS; CASPASE 1; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; ENZYME INHIBITORS; HMGB1 PROTEIN; INFLAMMASOMES; LUNG; MALE; MICE, INBRED BALB C; NEUTROPHIL INFILTRATION; PHOSPHATIDYLINOSITOL 3-KINASE; PROTEIN TRANSPORT; RANDOM ALLOCATION; RESPIRATORY MUCOSA; SIGNAL TRANSDUCTION; SPECIFIC PATHOGEN-FREE ORGANISMS; TOLUENE 2,4-DIISOCYANATE;

EID: 84929658680     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2015.04.011     Document Type: Article

References (48)

1. Andrei C., Margiocco P., Poggi A., Lotti L.V., Torrisi M.R., Rubartelli A. Phospholipases C and A2 control lysosome-mediated IL-1 beta secretion: implications for inflammatory processes. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9745-9750.
2. Ather J.L., Ckless K., Martin R., Foley K.L., Suratt B.T., Boyson J.E., Fitzgerald K.A., Flavell R.A., Eisenbarth S.C., Poynter M.E. Serum amyloid A activates the NLRP3 inflammasome and promotes Th17 allergic asthma in mice. J. Immunol. 2011, 187:64-73.
3. Bauer R.N., Brighton L.E., Mueller L., Xiang Z., Rager J.E., Fry R.C., Peden D.B., Jaspers I. Influenza enhances caspase-1 in bronchial epithelial cells from asthmatic volunteers and is associated with pathogenesis. J. Allergy Clin. Immunol. 2012, 130:958-967.
4. Besnard A.G., Guillou N., Tschopp J., Erard F., Couillin I., Iwakura Y., Quesniaux V., Ryffel B., Togbe D. NLRP3 inflammasome is required in murine asthma in the absence of aluminum adjuvant. Allergy 2011, 66:1047-1057.
5. Bonaldi T., Talamo F., Scaffidi P., Ferrera D., Porto A., Bachi A., Rubartelli A., Agresti A., Bianchi M.E. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J. 2003, 22:5551-5560.
6. Castiglioni A., Canti V., Rovere-Querini P., Manfredi A.A. High-mobility group box 1 (HMGB1) as a master regulator of innate immunity. Cell Tissue Res. 2011, 343(1):189-199.
7. Denes A., Lopez-Castejon G., Brough D. Caspase-1: is IL-1 just the tip of the ICEberg?. Cell Death Dis. 2012, 3:e338.
8. Gauley J., Pisetsky D.S. The translocation of HMGB1 during cell activation and cell death. Autoimmunity 2009, 42:299-301.
9. Harris H.E., Raucci A. Alarmin(g) news about danger: workshop on innate danger signals and HMGB1. EMBO Rep. 2006, 7:774-778.
10. Hirota J.A., Hirota S.A., Warner S.M., Stefanowicz D., Shaheen F., Beck P.L., Macdonald J.A., Hackett T.L., Sin D.D., Van Eeden S., Knight D.A. The airway epithelium nucleotide-binding domain and leucine-rich repeat protein 3 inflammasome is activated by urban particulate matter. J. Allergy Clin. Immunol. 2012, 129:1116-1125.
11. Hou C., Zhao H., Liu L., Li W., Zhou X., Lv Y., Shen X., Liang Z., Cai S., Zou F. High mobility group protein B1 (HMGB1) in asthma: comparison of patients with chronic obstructive pulmonary disease and healthy controls. Mol. Med. 2011, 17:807-815.
12. Iwata A., Nishio K., Winn R.K., Chi E.Y., Henderson W.J., Harlan J.M. A broad-spectrum caspase inhibitor attenuates allergic airway inflammation in murine asthma model. J. Immunol. 2003, 170:3386-3391.
13. Johnson V.J., Yucesoy B., Luster M.I. Prevention of IL-1 signaling attenuates airway hyperresponsiveness and inflammation in a murine model of toluene diisocyanate-induced asthma. J. Allergy Clin. Immunol. 2005, 116:851-858.
14. Kampe M., Lampinen M., Stolt I., Janson C., Stalenheim G., Carlson M. PI3-kinase regulates eosinophil and neutrophil degranulation in patients with allergic rhinitis and allergic asthma irrespective of allergen challenge model. Inflammation 2012, 35:230-239.
15. Kang H.J., Lee H., Choi H.J., Youn J.H., Shin J.S., Ahn Y.H., Yoo J.S., Paik Y.K., Kim H. Non-histone nuclear factor HMGB1 is phosphorylated and secreted in colon cancers. Lab. Invest. 2009, 89:948-959.
16. Keller M., Ruegg A., Werner S., Beer H.D. Active caspase-1 is a regulator of unconventional protein secretion. Cell 2008, 132:818-831.
17. Keyel P.A. How is inflammation initiated? Individual influences of IL-1, IL-18 and HMGB1. Cytokine 2014, 69(1):136-145.
18. Kim J., Ahn H., Woo H.M., Lee E., Lee G.S. Characterization of porcine NLRP3 inflammasome activation and its upstream mechanism. Vet. Res. Commun. 2014, 38(3):193-200.
19. Lamkanfi M. Emerging inflammasome effector mechanisms. Nat. Rev. Immunol. 2011, 11:213-220.
20. Lamkanfi M., Dixit V.M. Manipulation of host cell death pathways during microbial infections. Cell Host Microbe. 2010, 8:44-54.
21. Lamkanfi M., Sarkar A., Walle L.V., Vitari A.C., Amer A.O., Wewers M.D., Tracey K.J., Kanneganti T., Dixit V.M. Inflammasome-dependent release of the alarmin HMGB1 in endotoxemia. J. Immunol. 2010, 185:4385-4392.
22. Lee K.S., Lee H.K., Hayflick J.S., Lee Y.C., Puri K.D. Inhibition of phosphoinositide 3-kinase delta attenuates allergic airway inflammation and hyperresponsiveness in murine asthma model. FASEB J. 2006, 20:455-465.
23. Lee Y.C., Song C.H., Lee H.B., Oh J.L., Rhee Y.K., Park H.S., Koh G.Y. A murine model of toluene diisocyanate-induced asthma can be treated with matrix metalloproteinase inhibitor. J. Allergy Clin. Immunol. 2001, 108:1021-1026.
24. Lu B., Nakamura T., Inouye K., Li J., Tang Y., Lundback P., Valdes-Ferrer S.I., Olofsson P.S., Kalb T., Roth J., Zou Y., Erlandsson-Harris H., Yang H., Ting J.P., Wang H., Andersson U., Antoine D.J., Chavan S.S., Hotamisligil G.S., Tracey K.J. Novel role of PKR in inflammasome activation and HMGB1 release. Nature 2012, 488:670-674.
25. Lu B., Wang H., Andersson U., Tracey K.J. Regulation of HMGB1 release by inflammasomes. Protein Cell 2013, 4(3):163-167.
26. Lundblad L.K., Irvin C.G., Adler A., Bates J.H. A reevaluation of the validity of unrestrained plethysmography in mice. J. Appl. Physiol. (1985) 2002, 93:1198-1207.
27. Martin R.A., Ather J.L., Lundblad L.K., Suratt B.T., Boyson J.E., Budd R.C., Alcorn J.F., Flavell R.A., Eisenbarth S.C., Poynter M.E. Interleukin-1 receptor and caspase-1 are required for the Th17 response in nitrogen dioxide-promoted allergic airway disease. Am. J. Respir. Cell Mol. Biol. 2013, 48:655-664.
28. Marwick J.A., Caramori G., Stevenson C.S., Casolari P., Jazrawi E., Barnes P.J., Ito K., Adcock I.M., Kirkham P.A., Papi A. Inhibition of PI3Kdelta restores glucocorticoid function in smoking-induced airway inflammation in mice. Am. J. Respir. Crit. Care Med. 2009, 179:542-548.
29. Milutinovic P.S., Alcorn J.F., Englert J.M., Crum L.T., Oury T.D. The receptor for advanced glycation end products is a central mediator of asthma pathogenesis. Am. J. Pathol. 2012, 181:1215-1225.
30. Oh Y.J., Youn J.H., Ji Y., Lee S.E., Lim K.J., Choi J.E., Shin J.S. HMGB1 is phosphorylated by classical protein kinase C and is secreted by a calcium-dependent mechanism. J. Immunol. 2009, 182:5800-5809.
31. Oh Y.J., Youn J.H., Min H.J., Kim D.H., Lee S.S., Choi I.H., Shin J.S. CKD712, (S)-1-(alpha-naphthylmethyl)-6,7-dihydroxy-1,2,3,4-tetrahydroisoquinoline, inhibits the lipopolysaccharide-stimulated secretion of HMGB1 by inhibiting PI3K and classical protein kinase C. Int. Immunopharmacol. 2011, 11:1160-1165.
32. Papaiahgari S., Zhang Q., Kleeberger S.R., Cho H.Y., Reddy S.P. Hyperoxia stimulates an Nrf2-ARE transcriptional response via ROS-EGFR-PI3K-Akt/ERK MAP kinase signaling in pulmonary epithelial cells. Antioxid. Redox Signal. 2006, 8:43-52.
33. Peeters P.M., Perkins T.N., Wouters E.F., Mossman B.T., Reynaert N.L. Silica induces NLRP3 inflammasome activation in human lung epithelial cells. Part. Fibre Toxicol. 2013, 10:3.
34. Rauvala H., Rouhiainen A. Physiological and pathophysiological outcomes of the interactions of HMGB1 with cell surface receptors. Biochim. Biophys. Acta. 2010, 1799:164-170.
35. Ro E.J., Cha P.H., Kim H.Y., Cho Y.H., Park J.W., Han J.S., Choi K.Y. House dust mite allergen Der f 2 induces interleukin-13 expression by activating the PI3K/Akt pathway. Immunol. Res. 2013, 56:181-188.
36. Satoh T., Kambe N., Matsue H. NLRP3 activation induces ASC-dependent programmed necrotic cell death, which leads to neutrophilic inflammation. Cell Death Dis. 2013, 4:e644.
37. Shin Y.S., Kim M.A., Pham L., Park H. Cells and mediators in diisocyanate-induced occupational asthma. Curr. Opin. Allergy. Clin. Immunol. 2013, 13:125-131.
38. Simpson J.L., Phipps S., Baines K.J., Oreo K.M., Gunawardhana L., Gibson P.G. Elevated expression of the NLRP3 inflammasome in neutrophilic asthma. Eur. Respir. J. 2014, 43:1067-1076.
39. Song J., Zhao H., Dong H., Zhang D., Zou M., Tang H., Liu L., Liang Z., Lv Y., Zou F., Cai S. Mechanism of E-cadherin redistribution in bronchial airway epithelial cells in a TDI-induced asthma model. Toxicol. Lett. 2013, 220:8-14.
40. Takeda M., Ito W., Tanabe M., Ueki S., Kihara J., Kato H., Tanigai T., Kayaba H., Sasaki T., Chihara J. The pathophysiological roles of PI3Ks and therapeutic potential of selective inhibitors in allergic inflammation. Int. Arch. Allergy Immunol. 2010, 152(Suppl 1):90-95.
41. Tang H., Zhao H., Song J., Dong H., Yao L., Liang Z., LV Y., Zou F., Cai S. Ethyl pyruvate decreases airway neutrophil infiltration partly through a high mobility group box 1-dependent mechanism in a chemical-induced murine asthma model. Int. Immunopharmacol. 2014, 21:163-170.
42. Tapia-Abellan A., Ruiz-Alcaraz A.J., Anton G., Miras-Lopez M., Frances R., Such J., Martinez-Esparza M., Garcia-Penarrubia P. Regulatory role of PI3K-Akt on the release of IL-1beta in peritoneal macrophages from the ascites of cirrhotic patients. Clin. Exp. Immunol. 2014, 178(3):525-536.
43. Toker A., Cantley L.C. Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature 1997, 387:673-676.
44. Tran H.B., Lewis M.D., Tan L.W., Lester S.E., Baker L.M., Ng J., Hamilton-Bruce M.A., Hill C.L., Koblar S.A., Rischmueller M., Ruffin R.E., Wormald P.J., Zalewski P.D., Lang C.J. Immunolocalization of NLRP3 inflammasome in normal murine airway epithelium and changes following induction of ovalbumin-induced airway inflammation. J. Allergy (Cairo) 2012, 2012:819176.
45. Ullah M.A., Loh Z., Gan W.J., Zhang V., Yang H., Li J.H., Yamamoto Y., Schmidt A.M., Armour C.L., Hughes J.M., Phipps S., Sukkar M.B. Receptor for advanced glycation end products and its ligand high-mobility group box-1 mediate allergic airway sensitization and airway inflammation. J. Allergy Clin. Immunol. 2014, 134:440-450.
46. Watanabe T., Asai K., Fujimoto H., Tanaka H., Kanazawa H., Hirata K. Increased levels of HMGB-1 and endogenous secretory RAGE in induced sputum from asthmatic patients. Respir. Med. 2011, 105:519-525.
47. Zhang W., Nie Y., Chong L., Cai X., Zhang H., Lin B., Liang Y., Li C. PI3K and Notch signal pathways coordinately regulate the activation and proliferation of T lymphocytes in asthma. Life Sci. 2013, 92:890-895.
48. Zhou J.R., Zhang L.D., Wei H.F., Wang X., Ni H.L., Yang F., Zhang T., Jiang C.L. Neuropeptide Y induces secretion of high-mobility group box 1 protein in mouse macrophage via PKC/ERK dependent pathway. J. Neuroimmunol. 2013, 260:55-59.