Autophagy Enhances Bacterial Clearance during P. aeruginosa Lung Infection

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Junkins, Robert D ^a,b,c   Shen, Ann ^a   Rosen, Kirill ^d   McCormick, Craig ^a,c   Lin, Tong Jun ^a,b,c  

^a DALHOUSIE UNIVERSITY   (Canada)

^b IWK HEALTH CENTRE   (Canada)

^c Beatrice Hunter Cancer Research Institute   (Canada)

^d DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROQUINE; MYELOPEROXIDASE; RAPAMYCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BACTERIAL CLEARANCE; BACTERIAL LOAD; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; BRONCHUS MUCOSA; CELL MANIPULATION; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VIVO STUDY; INFECTION SENSITIVITY; INTERNALIZATION; LUNG INFECTION; MAST CELL; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; SIGNAL TRANSDUCTION; TREATMENT RESPONSE;

ANIMALS; AUTOPHAGY; BRONCHI; CELLS, CULTURED; CHLOROQUINE; HUMANS; MAST CELLS; MICE; MICE, INBRED C57BL; PHAGOSOMES; PNEUMONIA, BACTERIAL; PRIMARY CELL CULTURE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RESPIRATORY MUCOSA;

EID: 84883174355     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072263     Document Type: Article

References (71)

1. Cripps AW, Dunkley ML, Clancy RL, Kyd J, (1995) Pulmonary immunity to Pseudomonas aeruginosa. Immunol Cell Biol 73: 418-424.
2. McIsaac SM, Stadnyk AW, Lin TJ, (2012) Toll-like receptors in the host defense against Pseudomonas aeruginosa respiratory infection and cystic fibrosis. J Leukoc Biol 92: 977-985.
3. Kooguchi K, Hashimoto S, Kobayashi A, Kitamura Y, Kudoh I, et al. (1998) Role of alveolar macrophages in initiation and regulation of inflammation in Pseudomonas aeruginosa pneumonia. Infect Immun 66: 3164-3169.
4. Hashimoto S, Pittet JF, Hong K, Folkesson H, Bagby G, et al. (1996) Depletion of alveolar macrophages decreases neutrophil chemotaxis to Pseudomonas airspace infections. Am J Physiol 270: L819-828.
5. Le BV, Khorsi-Cauet H, Bach V, Gay-Queheillard J, (2012) Mast cells mediate Pseudomonas aeruginosa lipopolysaccharide-induced lung inflammation in rat. Eur J Clin Microbiol Infect Dis 31: 1983-1990.
6. Fox B, Bull TB, Guz A, (1981) Mast cells in the human alveolar wall: an electronmicroscopic study. J Clin Pathol 34: 1333-1342.
7. Tete S, Tripodi D, Rosati M, Conti F, Maccauro G, et al. (2012) Role of mast cells in innate and adaptive immunity. J Biol Regul Homeost Agents 26: 193-201.
8. Lin TJ, Garduno R, Boudreau RT, Issekutz AC, (2002) Pseudomonas aeruginosa activates human mast cells to induce neutrophil transendothelial migration via mast cell-derived IL-1 alpha and beta. J Immunol 169: 4522-4530.
9. Lin TJ, Issekutz TB, Marshall JS, (2000) Human mast cells transmigrate through human umbilical vein endothelial monolayers and selectively produce IL-8 in response to stromal cell-derived factor-1 alpha. J Immunol 165: 211-220.
10. Jenkins CE, Swiatoniowski A, Power MR, Lin TJ, (2006) Pseudomonas aeruginosa-induced human mast cell apoptosis is associated with up-regulation of endogenous Bcl-xS and down-regulation of Bcl-xL. J Immunol 177: 8000-8007.
11. Lin TJ, Maher LH, Gomi K, McCurdy JD, Garduno R, et al. (2003) Selective early production of CCL20, or macrophage inflammatory protein 3alpha, by human mast cells in response to Pseudomonas aeruginosa. Infect Immun 71: 365-373.
12. Hauser AR, Jain M, Bar-Meir M, McColley SA, (2011) Clinical significance of microbial infection and adaptation in cystic fibrosis. Clin Microbiol Rev 24: 29-70.
13. Buchanan PJ, Ernst RK, Elborn JS, Schock B, (2009) Role of CFTR, Pseudomonas aeruginosa and Toll-like receptors in cystic fibrosis lung inflammation. Biochem Soc Trans 37: 863-867.
14. Luciani A, Villella VR, Esposito S, Brunetti-Pierri N, Medina D, et al. (2010) Defective CFTR induces aggresome formation and lung inflammation in cystic fibrosis through ROS-mediated autophagy inhibition. Nat Cell Biol 12: 863-875.
15. Liu G, Bi Y, Wang R, Wang X (2012) Self-eating and self-defense: autophagy controls innate immunity and adaptive immunity. J Leukoc Biol.
16. Patterson NL, Mintern JD, (2012) Intersection of autophagy with pathways of antigen presentation. Protein Cell 3: 911-920.
17. Deretic V, (2012) Autophagy: an emerging immunological paradigm. J Immunol 189: 15-20.
18. Yuan K, Huang C, Fox J, Laturnus D, Carlson E, et al. (2012) Autophagy plays an essential role in the clearance of Pseudomonas aeruginosa by alveolar macrophages. J Cell Sci 125: 507-515.
19. Breidenstein EB, de la Fuente-Nunez C, Hancock RE, (2011) Pseudomonas aeruginosa: all roads lead to resistance. Trends Microbiol 19: 419-426.
20. Obritsch MD, Fish DN, MacLaren R, Jung R, (2005) Nosocomial infections due to multidrug-resistant Pseudomonas aeruginosa: epidemiology and treatment options. Pharmacotherapy 25: 1353-1364.
21. Bradbury R, Champion A, Reid DW, (2008) Poor clinical outcomes associated with a multi-drug resistant clonal strain of Pseudomonas aeruginosa in the Tasmanian cystic fibrosis population. Respirology 13: 886-892.
22. Yang MA, Lee J, Choi EH, Lee HJ, (2011) Pseudomonas aeruginosa bacteremia in children over ten consecutive years: analysis of clinical characteristics, risk factors of multi-drug resistance and clinical outcomes. J Korean Med Sci 26: 612-618.
23. Fleiszig SM, Zaidi TS, Fletcher EL, Preston MJ, Pier GB, (1994) Pseudomonas aeruginosa invades corneal epithelial cells during experimental infection. Infect Immun 62: 3485-3493.
24. Garcia-Medina R, Dunne WM, Singh PK, Brody SL, (2005) Pseudomonas aeruginosa acquires biofilm-like properties within airway epithelial cells. Infect Immun 73: 8298-8305.
25. Huang J, Brumell JH, (2009) Autophagy in immunity against intracellular bacteria. Curr Top Microbiol Immunol 335: 189-215.
26. Fleiszig SM, Zaidi TS, Preston MJ, Grout M, Evans DJ, et al. (1996) Relationship between cytotoxicity and corneal epithelial cell invasion by clinical isolates of Pseudomonas aeruginosa. Infect Immun 64: 2288-2294.
27. Plotkowski MC, de Bentzmann S, Pereira SH, Zahm JM, Bajolet-Laudinat O, et al. (1999) Pseudomonas aeruginosa internalization by human epithelial respiratory cells depends on cell differentiation, polarity, and junctional complex integrity. Am J Respir Cell Mol Biol 20: 880-890.
28. Schroeder TH, Reiniger N, Meluleni G, Grout M, Coleman FT, et al. (2001) Transgenic cystic fibrosis mice exhibit reduced early clearance of Pseudomonas aeruginosa from the respiratory tract. J Immunol 166: 7410-7418.
29. Zaas DW, Duncan MJ, Li G, Wright JR, Abraham SN, (2005) Pseudomonas invasion of type I pneumocytes is dependent on the expression and phosphorylation of caveolin-2. J Biol Chem 280: 4864-4872.
30. Lin TJ, Gao Z, Arock M, Abraham SN, (1999) Internalization of FimH+ Escherichia coli by the human mast cell line (HMC-1 5C6) involves protein kinase C. J Leukoc Biol. 66: 1031-1038.
31. Kamath S, Kapatral V, Chakrabarty AM, (1998) Cellular function of elastase in Pseudomonas aeruginosa: role in the cleavage of nucleoside diphosphate kinase and in alginate synthesis. Mol Microbiol 30: 933-941.
32. Power MR, Li B, Yamamoto M, Akira S, Lin TJ, (2007) A role of Toll-IL-1 receptor domain-containing adaptor-inducing IFN-beta in the host response to Pseudomonas aeruginosa lung infection in mice. J Immunol 178: 3170-3176.
33. Li B, Berman J, Tang JT, Lin TJ, (2007) The early growth response factor-1 is involved in stem cell factor (SCF)-induced interleukin 13 production by mast cells, but is dispensable for SCF-dependent mast cell growth. J Biol Chem 282: 22573-22581.
34. Weber S, Babina M, Kruger-Krasagakes S, Grutzkau A, Henz BM, (1996) A subclone (5C6) of the human mast cell line HMC-1 represents a more differentiated phenotype than the original cell line. Arch Dermatol Res 288: 778-782.
35. Cozens AL, Yezzi MJ, Kunzelmann K, Ohrui T, Chin L, et al. (1994) CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am J Respir Cell Mol Biol 10: 38-47.
36. Bruscia E, Sangiuolo F, Sinibaldi P, Goncz KK, Novelli G, et al. (2002) Isolation of CF cell lines corrected at DeltaF508-CFTR locus by SFHR-mediated targeting. Gene Ther 9: 683-685.
37. Yang YJ, Chen W, Edgar A, Li B, Molkentin JD, et al. (2009) Rcan1 negatively regulates Fc epsilonRI-mediated signaling and mast cell function. J Exp Med 206: 195-207.
38. Schneider T, Issekutz AC, (1996) Quantitation of eosinophil and neutrophil infiltration into rat lung by specific assays for eosinophil peroxidase and myeloperoxidase. Application in a Brown Norway rat model of allergic pulmonary inflammation. J Immunol Methods 198: 1-14.
39. Rouschop KM, van den Beucken T, Dubois L, Niessen H, Bussink J, et al. (2010) The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5. J Clin Invest 120: 127-141.
40. Abdulrahman BA, Khweek AA, Akhter A, Caution K, Kotrange S, et al. (2011) Autophagy stimulation by rapamycin suppresses lung inflammation and infection by Burkholderia cenocepacia in a model of cystic fibrosis. Autophagy 7: 1359-1370.
41. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, et al. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728.
42. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, et al. (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282: 24131-24145.
43. Leidal AM, Cyr DP, Hill RJ, Lee PW, McCormick C, (2012) Subversion of autophagy by Kaposi's sarcoma-associated herpesvirus impairs oncogene-induced senescence. Cell Host Microbe 11: 167-180.
44. Faulkner G, Garduno RA, (2002) Ultrastructural analysis of differentiation in Legionella pneumophila. J Bacteriol 184: 7025-7041.
45. Eskelinen EL, Reggiori F, Baba M, Kovacs AL, Seglen PO, (2011) Seeing is believing: the impact of electron microscopy on autophagy research. Autophagy 7: 935-956.
46. Tanida I, Ueno T, Kominami E, (2004) LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol 36: 2503-2518.
47. Ushio H, Ueno T, Kojima Y, Komatsu M, Tanaka S, et al. (2011) Crucial role for autophagy in degranulation of mast cells. J Allergy Clin Immunol 127: 1267-1276 e1266.
48. Mizushima N, Yoshimori T, Levine B, (2010) Methods in mammalian autophagy research. Cell 140: 313-326.
49. Gao W, Ding WX, Stolz DB, Yin XM, (2008) Induction of macroautophagy by exogenously introduced calcium. Autophagy 4: 754-761.
50. Hosokawa N, Hara Y, Mizushima N, (2006) Generation of cell lines with tetracycline-regulated autophagy and a role for autophagy in controlling cell size. FEBS Lett 580: 2623-2629.
51. Kneen M, Farinas J, Li Y, Verkman AS, (1998) Green fluorescent protein as a noninvasive intracellular pH indicator. Biophys J 74: 1591-1599.
52. Shaner NC, Steinbach PA, Tsien RY, (2005) A guide to choosing fluorescent proteins. Nat Methods 2: 905-909.
53. Samoszuk M, Kanakubo E, Chan JK, (2005) Degranulating mast cells in fibrotic regions of human tumors and evidence that mast cell heparin interferes with the growth of tumor cells through a mechanism involving fibroblasts. BMC Cancer 5: 121.
54. Plantinga TS, Joosten LA, van der Meer JW, Netea MG, (2012) Modulation of inflammation by autophagy: consequences for Crohn's disease. Curr Opin Pharmacol 12: 497-502.
55. Blommaart EF, Luiken JJ, Blommaart PJ, van Woerkom GM, Meijer AJ, (1995) Phosphorylation of ribosomal protein S6 is inhibitory for autophagy in isolated rat hepatocytes. J Biol Chem 270: 2320-2326.
56. Cutler NS, Heitman J, Cardenas ME, (1999) TOR kinase homologs function in a signal transduction pathway that is conserved from yeast to mammals. Mol Cell Endocrinol 155: 135-142.
57. Saemann MD, Haidinger M, Hecking M, Horl WH, Weichhart T, (2009) The multifunctional role of mTOR in innate immunity: implications for transplant immunity. Am J Transplant 9: 2655-2661.
58. Villella VR, Esposito S, Bruscia EM, Maiuri MC, Raia V, et al. (2013) Targeting the Intracellular Environment in Cystic Fibrosis: Restoring Autophagy as a Novel Strategy to Circumvent the CFTR Defect. Front Pharmacol 4: 1.
59. Mayer ML, Blohmke CJ, Falsafi R, Fjell CD, Madera L, et al. (2013) Rescue of dysfunctional autophagy attenuates hyperinflammatory responses from cystic fibrosis cells. J Immunol 190: 1227-1238.
60. Machen TE, (2006) Innate immune response in CF airway epithelia: hyperinflammatory? Am J Physiol Cell Physiol 291: C218-230.
61. Nichols DP, Konstan MW, Chmiel JF, (2008) Anti-inflammatory therapies for cystic fibrosis-related lung disease. Clin Rev Allergy Immunol 35: 135-153.
62. Shoji-Kawata S, Sumpter R, Leveno M, Campbell GR, Zou Z, et al. (2013) Identification of a candidate therapeutic autophagy-inducing peptide. Nature 494: 201-206.
63. Kirkegaard K, (2009) Subversion of the cellular autophagy pathway by viruses. Curr Top Microbiol Immunol 335: 323-333.
64. Campoy E, Colombo MI, (2009) Autophagy subversion by bacteria. Curr Top Microbiol Immunol 335: 227-250.
65. Skindersoe ME, Zeuthen LH, Brix S, Fink LN, Lazenby J, et al. (2009) Pseudomonas aeruginosa quorum-sensing signal molecules interfere with dendritic cell-induced T-cell proliferation. FEMS Immunol Med Microbiol 55: 335-345.
66. Wu L, Estrada O, Zaborina O, Bains M, Shen L, et al. (2005) Recognition of host immune activation by Pseudomonas aeruginosa. Science 309: 774-777.
67. Moser C, Jensen PO, Pressler T, Frederiksen B, Lanng S, et al. (2005) Serum concentrations of GM-CSF and G-CSF correlate with the Th1/Th2 cytokine response in cystic fibrosis patients with chronic Pseudomonas aeruginosa lung infection. APMIS 113: 400-409.
68. Moser C, Johansen HK, Song Z, Hougen HP, Rygaard J, et al. (1997) Chronic Pseudomonas aeruginosa lung infection is more severe in Th2 responding BALB/c mice compared to Th1 responding C3H/HeN mice. APMIS 105: 838-842.
69. Moser C, Kjaergaard S, Pressler T, Kharazmi A, Koch C, et al. (2000) The immune response to chronic Pseudomonas aeruginosa lung infection in cystic fibrosis patients is predominantly of the Th2 type. APMIS 108: 329-335.
70. Wolf P, Elsasser-Beile U, (2009) Pseudomonas exotoxin A: from virulence factor to anti-cancer agent. Int J Med Microbiol 299: 161-176.
71. Boyce M, Py BF, Ryazanov AG, Minden JS, Long K, et al. (2008) A pharmacoproteomic approach implicates eukaryotic elongation factor 2 kinase in ER stress-induced cell death. Cell Death Differ 15: 589-599.