Activation of IFN-γ/STAT/IRF-1 in hepatic responses to Klebsiella pneumoniae infection

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Lin, Yi Chun ^a   Lu, Min Chi ^b,c   Lin, Chingju ^d   Chiang, Ming Ko ^e   Jan, Ming Shiou ^c   Tang, Hui Ling ^a,f   Liu, Hsu Chung ^b,c   Lin, Wea Lung ^b,c   Huang, Chih Yang ^g,h   Chen, Chuan Mu ^a   Lai, Yi Chyi ^b,c  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^d CHINA MEDICAL UNIVERSITY   (Taiwan)

^e NATIONAL CHUNG CHENG UNIVERSITY   (Taiwan)

^f CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^g CHINA MEDICAL UNIVERSITY   (Taiwan)

^h ASIA UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; GAMMA INTERFERON; INITIATION FACTOR 2ALPHA; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 2; STAT1 PROTEIN; STAT2 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DIABETES MELLITUS; DISEASE ASSOCIATION; DISEASE SEVERITY; ENZYME ACTIVATION; HEPATITIS; IN VIVO STUDY; INFECTION SENSITIVITY; INFLAMMATION; KLEBSIELLA PNEUMONIAE INFECTION; LIVER; LIVER CELL; MORBIDITY; MOUSE; MOUSE MODEL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; TRANSCRIPTION INITIATION; UPREGULATION;

ANIMALS; CASPASE 3; CHEMOKINE CXCL2; INTERFERON REGULATORY FACTOR-1; INTERFERON-GAMMA; INTERLEUKIN-1BETA; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; LIVER; MALE; MICE; MICE, INBRED BALB C;

EID: 84892404428     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079961     Document Type: Article

References (54)

1. Podschun R, Ullmann U (1998) Klebsiella spp. as Nosocomial Pathogens: Epidemiology, Taxonomy, Typing Methods, and Pathogenicity Factors. Clin Microbiol Rev 11: 589-603. PubMed: 9767057.
2. Wang JH, Liu YC, Lee SS, Yen MY, Chen YS et al. (1998) Primary liver abscess due to Klebsiella pneumoniae in Taiwan. Clin Infect Dis 26: 1434-1438. doi:10.1086/516369. PubMed: 9636876.
3. Chung DR, Lee SS, Lee HR, Kim HB, Choi HJ et al. (2007) Emerging invasive liver abscess caused by K1 serotype Klebsiella pneumoniae in Korea. J Infect 54: 578-583. doi:10.1016/j.jinf.2006.11.008. PubMed: 17175028.
4. Karama EM, Willermain F, Janssens X, Claus M, Van den Wijngaert S et al. (2008) Endogenous endophthalmitis complicating Klebsiella pneumoniae liver abscess in Europe: case report. Int Ophthalmol 28: 111-113. doi:10.1007/s10792- 007-9111-4. PubMed: 17668150.
5. Nadasy KA, Domiati-Saad R, Tribble MA (2007) Invasive Klebsiella pneumoniae syndrome in North America. Clin Infect Dis 45: e25-e28. doi:10.1086/519424. PubMed: 17599300.
6. Yeh CC, Sung FC, Tang R, Chang-Chieh CR, Hsieh LL (2007) Association between polymorphisms of biotransformation and DNArepair genes and risk of colorectal cancer in Taiwan. J Biomed Sci 14: 183-193. doi:10.1007/s11373-006- 9139-x. PubMed: 17191090.
7. Fang CT, Lai SY, Yi WC, Hsueh PR, Liu KL et al. (2007) Klebsiella pneumoniae genotype K1: an emerging pathogen that causes septic ocular or central nervous system complications from pyogenic liver abscess. Clin Infect Dis 45: 284-293. doi:10.1086/519262. PubMed: 17599305.
8. Korrapati MC, Shaner BE, Neely BA, Alge JL, Arthur JM et al. (2012) Diabetes-induced renal injury in rats is attenuated by suramin. J Pharmacol Exp Ther 343: 34-43. doi:10.1124/jpet.112.196964. PubMed: 22736507.
9. Yang CS, Tsai HY, Sung CS, Lin KH, Lee FL et al. (2007) Endogenous Klebsiella endophthalmitis associated with pyogenic liver abscess. Ophthalmology 114: 876-880. doi:10.1016/j.ophtha.2006.12.035. PubMed: 17467526.
10. Wang J-H, Liu Y-C, Lee SS-J, Yen M-Y, Chen Y-S et al. (1998) Primary Liver Abscess Due to Klebsiella pneumoniae in Taiwan. Clin Infect Dis 26: 1434-1438. doi:10.1086/516369. PubMed: 9636876.
11. Dellacasagrande J, Ghigo E, Raoult D, Capo C, Mege J-L (2002) IFN- {gamma}-Induced Apoptosis and Microbicidal Activity in Monocytes Harboring the Intracellular Bacterium Coxiella burnetii Require Membrane TNF and Homotypic Cell Adherence. J Immunol 169: 6309-6315. PubMed: 12444137.
12. Spörri R, Joller N, Albers U, Hilbi H, Oxenius A (2006) MyD88- Dependent IFN-{gamma} Production by NK Cells Is Key for Control of Legionella pneumophila Infection. J Immunol 176: 6162-6171. PubMed: 16670325.
13. Rowe JH, Ertelt JM, Way SS (2012) Innate IFN-{gamma} Is Essential for Programmed Death Ligand-1-Mediated T Cell Stimulation following Listeria monocytogenes Infection. J Immunol 189: 876-884. doi: 10.4049/jimmunol.1103227. PubMed: 22711893.
14. McLoughlin RM, Lee JC, Kasper DL, Tzianabos AO (2008) IFN- {gamma} Regulated Chemokine Production Determines the Outcome of Staphylococcus aureus Infection. J Immunol 181: 1323-1332. PubMed: 18606687.
15. Rothfuchs AG, Trumstedt C, Mattei F, Schiavoni G, Hidmark A et al. (2006) STAT1 Regulates IFN-{alpha}beta- and IFN-{gamma}- Dependent Control of Infection with Chlamydia pneumoniae by Nonhemopoietic Cells. J Immunol 176: 6982-6990. PubMed: 16709859.
16. Jaruga B, Hong F, Kim WH, Gao B (2004) IFN-gamma/STAT1 acts as a proinflammatory signal in T cell-mediated hepatitis via induction of multiple chemokines and adhesion molecules: a critical role of IRF-1. Am J Physiol Gastrointest Liver Physiol 287: G1044-G1052. doi: 10.1152/ajpgi.00184.2004. PubMed: 15246962.
17. Kano A, Haruyama T, Akaike T, Watanabe Y (1999) IRF-1 is an essential mediator in IFN-gamma-induced cell cycle arrest and apoptosis of primary cultured hepatocytes. Biochem Biophys Res Commun 257: 672-677. doi:10.1006/bbrc.1999.0276. PubMed: 10208842.
18. Shen K, Zheng S-S, Park O, Wang H, Sun Z et al. (2008) Activation of innate immunity (NK/IFN-{gamma}) in rat allogeneic liver transplantation: contribution to liver injury and suppression of hepatocyte proliferation. Am J Physiol Gastrointest Liver Physiol 294: G1070-G1077. doi:10.1152/ajpgi.00554. 2007. PubMed: 18292182.
19. Rawlings JS, Rosler KM, Harrison DA (2004) The JAK/STAT signaling pathway. J Cell Sci 117: 1281-1283. doi:10.1242/jcs.00963. PubMed: 15020666.
20. Hu X, Ivashkiv LB (2009) Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immunity 31: 539-550. doi:10.1016/j.immuni.2009.09.002. PubMed: 19833085.
21. Qing Y, Stark GR (2004) Alternative Activation of STAT1 and STAT3 in Response to Interferon-{gamma}. J Biol Chem 279: 41679-41685. doi: 10.1074/jbc.M406413200. PubMed: 15284232.
22. Jaruga B, Hong F, Kim W-H, Gao B (2004) IFN-{gamma}/STAT1 acts as a proinflammatory signal in T cell-mediated hepatitis via induction of multiple chemokines and adhesion molecules: a critical role of IRF-1. Am J Physiol Gastrointest Liver Physiol 287: G1044-G1052. doi: 10.1152/ajpgi.00184.2004. PubMed: 15246962.
23. Horras CJ, Lamb CL, Mitchell KA (2011) Regulation of hepatocyte fate by interferon-? Cytokine Growth Factor Rev 22: 35-43. doi:10.1016/j.cytogfr.2011. 01.001. PubMed: 21334249.
24. Watanabe Y, Suzuki O, Haruyama T, Akaike T (2003) Interferongamma induces reactive oxygen species and endoplasmic reticulum stress at the hepatic apoptosis. J Cell Biochem 89: 244-253. doi: 10.1002/jcb.10501. PubMed: 12704788.
25. Fung CP, Chang FY, Lee SC, Hu BS, Kuo BI et al. (2002) A global emerging disease of Klebsiella pneumoniae liver abscess: is serotype K1 an important factor for complicated endophthalmitis? Gut 50: 420-424. doi:10.1136/gut.50.3. 420. PubMed: 11839725.
26. Rahimian J, Wilson T, Oram V, Holzman RS (2004) Pyogenic liver abscess: recent trends in etiology and mortality. Clin Infect Dis 39: 1654-1659. doi:10.1086/425616. PubMed: 15578367.
27. Pozzilli P, Leslie RD (1994) Infections and diabetes: mechanisms and prospects for prevention. Diabet Med 11: 935-941. doi:10.1111/j.1464-5491.1994. tb00250.x. PubMed: 7895457.
28. Moore TA, Perry ML, Getsoian AG, Newstead MW, Standiford TJ (2002) Divergent Role of Gamma Interferon in a Murine Model of Pulmonary versus Systemic Klebsiella pneumoniae Infection. Infect Immun 70: 6310-6318. doi:10.1128/IAI.70.11.6310-6318.2002. PubMed: 12379710.
29. Winson MK, Swift S, Hill PJ, Sims CM, Griesmayr G et al. (1998) Engineering the luxCDABE genes from Photorhabdus luminescens to provide a bioluminescent reporter for constitutive and promoter probe plasmids and mini-Tn5 constructs. FEMS Microbiol Lett 163: 193-202. doi:10.1111/j.1574-6968. 1998.tb13045.x. PubMed: 9673022.
30. Wetzstein M, Schumann W (1990) Promoters of major Escherichia coli heat shock genes seem non-functional in Bacillus subtilis. FEMS Microbiol Lett 60: 55-58. PubMed: 2126519.
31. Eastgate JA, Taylor N, Coleman MJ, Healy B, Thompson L et al. (1995) Cloning, expression, and characterization of the lon gene of Erwinia amylovora: evidence for a heat shock response. J Bacteriol 177: 932-937. PubMed: 7860603.
32. De Champs C, Sauvant MP, Chanal C, Sirot D, Gazuy N et al. (1989) Prospective survey of colonization and infection caused by expanded-spectrum- beta-lactamase-producing members of the family Enterobacteriaceae in an intensive care unit. J Clin Microbiol 27: 2887-2890. PubMed: 2592552.
33. Fung CP, Lin YT, Lin JC, Chen TL, Yeh KM et al. (2012) Klebsiella pneumoniae in gastrointestinal tract and pyogenic liver abscess. Emerg Infect Dis 18: 1322-1325. PubMed: 22840473.
34. Knodell RG, Ishak KG, Black WC, Chen TS, Craig R et al. (1981) Formulation and application of a numerical scoring system for assessing histological activity in asymptomatic chronic active hepatitis. Hepatology 1: 431-435. doi:10.1002/hep.1840010511. PubMed: 7308988.
35. Toyonaga T, Hino O, Sugai S, Wakasugi S, Abe K et al. (1994) Chronic active hepatitis in transgenic mice expressing interferon-gamma in the liver. Proc Natl Acad Sci U S A 91: 614-618. doi:10.1073/pnas. 91.2.614. PubMed: 8290572.
36. Kanki K, Kawamura T, Watanabe Y (2009) Control of ER stress by a chemical chaperone counteracts apoptotic signals in IFN-gammatreated murine hepatocytes. Apoptosis 14: 309-319. doi:10.1007/s10495-009-0318-x. PubMed: 19184438.
37. Watts T, Berti I, Sapone A, Gerarduzzi T, Not T et al. (2005) Role of the intestinal tight junction modulator zonulin in the pathogenesis of type I diabetes in BB diabetic-prone rats. Proc Natl Acad Sci U S A 102: 2916-2921. doi:10.1073/pnas.0500178102. PubMed: 15710870.
38. Secondulfo M, Iafusco D, Carratù R, deMagistris L, Sapone A, et al. (2004) Ultrastructural mucosal alterations and increased intestinal permeability in non-celiac, type I diabetic patients. Dig Liver Dis 36: 35-45. doi:10.1016/j.dld.2003.09.016. PubMed: 14971814. doi:10.1016/j.dld.2003.09.016 PubMed: 14971814
39. Damci T, Nuhoglu I, Devranoglu G, Osar Z, Demir M et al. (2003) Increased intestinal permeability as a cause of fluctuating postprandial blood glucose levels in Type 1 diabetic patients. Eur J Clin Invest 33: 397-401. doi:10.1046/j.1365-2362.2003.01161.x. PubMed: 12713453.
40. Bebien M, Hensler ME, Davanture S, Hsu LC, Karin M et al. The poreforming toxin beta hemolysin/cytolysin triggers p38 MAPK-dependent IL-10 production in macrophages and inhibits innate immunity. PLOS Pathog 8: e1002812.
41. Sunahara KKS, Martins JO (2012) Alveolar macrophages in diabetes: friends or foes? J Leukoc Biol 91: 871-876. doi:10.1189/jlb.0911488. PubMed: 22422924.
42. Hewett JA, Schultze AE, VanCise S, Roth RA (1992) Neutrophil depletion protects against liver injury from bacterial endotoxin. Lab Invest 66: 347-361. PubMed: 1538588.
43. Lee A, Whyte MK, Haslett C (1993) Inhibition of apoptosis and prolongation of neutrophil functional longevity by inflammatory mediators. J Leukoc Biol 54: 283-288. PubMed: 8409750.
44. Streetz K, Fregien B, Plümpe J, Körber K, Kubicka S et al. (2001) Dissection of the intracellular pathways in hepatocytes suggests a role for Jun kinase and IFN regulatory factor-1 in Con A-induced liver failure. J Immunol 167: 514-523. PubMed: 11418690.
45. Vadrot N, Legrand A, Nello E, Bringuier AF, Guillot R et al. (2006) Inducible nitric oxide synthase (iNOS) activity could be responsible for resistance or sensitivity to IFN-gamma-induced apoptosis in several human hepatoma cell lines. J Interferon Cytokine Res 26: 901-913. doi: 10.1089/jir.2006.26.901. PubMed: 17238833.
46. Sironi JJ, Ouchi T (2004) STAT1-induced Apoptosis Is Mediated by Caspases 2: 3, and 7. J Biol Chem 279: 4066-4074
47. Tagawa Y, Sekikawa K, Iwakura Y (1997) Suppression of concanavalin A-induced hepatitis in IFN-gamma(-/-) mice, but not in TNF-alpha(-/-) mice: role for IFN-gamma in activating apoptosis of hepatocytes. J Immunol 159: 1418-1428. PubMed: 9233639.
48. Liu CY, Kaufman RJ (2003) The unfolded protein response. J Cell Sci 116: 1861-1862. doi:10.1242/jcs.00408. PubMed: 12692187.
49. Cnop M, Foufelle F, Velloso LAM, Foufelle F, Velloso LA (2011) Endoplasmic reticulum stress, obesity and diabetes. Trends Mol Med 18: 59-68. PubMed: 21889406. .
50. Chang HY, Lee JH, Deng WL, Fu TF, Peng HL (1996) Virulence and outer membrane properties of a galU mutant of Klebsiella pneumoniae CG43. Microb Pathog 20: 255-261. doi:10.1006/mpat.1996.0024. PubMed: 8861391.
51. Tu Y-C, Lu M-C, Chiang M-K, Huang S-P, Peng H-L et al. (2009) Genetic Requirements for Klebsiella pneumoniae-Induced Liver Abscess in an Oral Infection Model. Infect Immun 77: 2657-2671. doi: 10.1128/IAI.01523-08. PubMed: 19433545.
52. Lin YC, Lu MC, Tang HL, Liu HC, Chen CH et al. (2011) Assessment of hypermucoviscosity as a virulence factor for experimental Klebsiella pneumoniae infections: comparative virulence analysis with hypermucoviscosity-negative strain. BMC Microbiol 11: 50. doi: 10.1186/1471-2180-11-50. PubMed: 21385400.
53. Rossini AA, Like AA, Chick WL, Appel MC, Cahill GF Jr. (1977) Studies of streptozotocin-induced insulitis and diabetes. Proc Natl Acad Sci U S A 74: 2485-2489. doi:10.1073/pnas.74.6.2485. PubMed: 142253.
54. Contag PR, Olomu IN, Stevenson DK, Contag CH (1998) Bioluminescent indicators in living mammals. Nat Med 4: 245-247. doi: 10.1038/nm0298-245. PubMed: 9461201.