Glyburide Reduces Bacterial Dissemination in a Mouse Model of Melioidosis

PLoS Neglected Tropical Diseases

Volumn 7, Issue 10, 2013, Pages

  Koh, Gavin C K W ^a,b,c,d,e   Weehuizen, Tassili A ^a   Breitbach, Katrin ^f   Krause, Kathrin ^f   de Jong, Hanna K ^a   Kager, Liesbeth M ^a   Hoogendijk, Arjan J ^a   Bast, Antje ^f   Peacock, Sharon J ^d,e   van der Poll, Tom ^a   Steinmetz, Ivo ^f   Wiersinga, W Joost ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c BIRMINGHAM HEARTLANDS HOSPITAL   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e MAHIDOL UNIVERSITY   (Thailand)

^f UNIVERSITY MEDICINE GREIFSWALD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CEFTAZIDIME; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; GLIBENCLAMIDE; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL LOAD; BACTERIAL TRANSMISSION; BURKHOLDERIA PSEUDOMALLEI; CONTROLLED STUDY; DIABETES MELLITUS; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; LUNG LAVAGE; LUNG PARENCHYMA; MACROPHAGE; MELIOIDOSIS; MINIMUM INHIBITORY CONCENTRATION; MOUSE; NONHUMAN;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTI-INFLAMMATORY AGENTS; BURKHOLDERIA PSEUDOMALLEI; CEFTAZIDIME; DIABETES COMPLICATIONS; DISEASE MODELS, ANIMAL; GLYBURIDE; INTERLEUKIN-1BETA; MELIOIDOSIS; MICE; MICE, INBRED C57BL; MICROBIAL SENSITIVITY TESTS; SEPSIS; TREATMENT OUTCOME;

EID: 84887306849     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002500     Document Type: Article

References (61)

1. Wiersinga WJ, Currie BJ, Peacock SJ, (2012) Melioidosis. N Engl J Med 367: 1035-1044.
2. Koh GCKW, Maude RR, Schreiber MF, Limmathurotsakul D, Wiersinga WJ, et al. (2011) Glyburide is anti-inflammatory and associated with reduced mortality in melioidosis. Clin Infect Dis 52: 717-725 doi:10.1093/cid/ciq192.
3. Department of Health and Human Services (2012) Possession, use, and transfer of select agents and toxins: biennial review. Federal Register 77: 61085-61115.
4. Simpson AJ, (2001) Melioidosis: a clinical model for Gram-negative sepsis. J Med Microbiol 50: 657-658.
5. Koh GCKW, Peacock SJ, van der Poll T, Wiersinga WJ, (2011) The impact of diabetes on the pathogenesis of sepsis. Eur J Clin Microbiol Infect Dis 31: 379-388 doi:10.1007/s10096-011-1337-4.
6. Pongcharoen S, Ritvirool PN, Sanguansermsri D, Chanchan P, Jienmongkol P, et al. (2008) Reduced interleukin-17 expression of Burkholderia pseudomallei-infected peripheral blood mononuclear cells of diabetic patients. Asian Pac J Allergy Immunol 26: 63-69.
7. Tan KS, Lee KO, Low KC, Gamage AM, Liu Y, et al. (2012) Glutathione deficiency in type 2 diabetes impairs cytokine responses and control of intracellular bacteria. J Clin Invest 122: 2289-2300.
8. Chin CY, Monack DM, Nathan S, (2012) Delayed activation of host innate immune pathways in streptozotocin-induced diabetic hosts leads to more severe disease during infection with Burkholderia pseudomallei. Immunology 135: 312-332.
9. Hodgson KA, Morris JL, Feterl ML, Govan BL, Ketheesan N, (2011) Altered macrophage function is associated with severe Burkholderia pseudomallei infection in a murine model of type 2 diabetes. Microbes Infect 13: 1177-1184 doi:10.1016/j.micinf.2011.07.008.
10. WHO Model List of Essential Medicines: 17th list (2011). Geneva, Switzerland: World Health Organization. 41 p.
11. Hamon Y, Luciani MF, Becq F, Verrier B, Rubartelli A, et al. (1997) Interleukin-1beta secretion is impaired by inhibitors of the Atp binding cassette transporter, ABC1. Blood 90: 2911-2915.
12. Lamkanfi M, Mueller JL, Vitari AC, Misaghi S, Fedorova A, et al. (2009) Glyburide inhibits the Cryopyrin/Nalp3 inflammasome. J Cell Biol 187: 61-70 doi:10.1083/jcb.200903124.
13. Toye AA, Lippiat JD, Proks P, Shimomura K, Bentley L, et al. (2005) A genetic and physiological study of impaired glucose homeostasis control in C57BL/6J mice. Diabetologia 48: 675-686 doi:10.1007/s00125-005-1680-z.
14. Freeman HC, Hugill A, Dear NT, Ashcroft FM, Cox RD, (2006) Deletion of nicotinamide nucleotide transhydrogenase: a new quantitive trait locus accounting for glucose intolerance in C57BL/6J mice. Diabetes 55: 2153-2156 doi:10.2337/db06-0358.
15. Huang T-T, Naeemuddin M, Elchuri S, Yamaguchi M, Kozy HM, et al. (2006) Genetic modifiers of the phenotype of mice deficient in mitochondrial superoxide dismutase. Human Molecular Genetics 15: 1187-1194 doi:10.1093/hmg/ddl034.
16. Leakey AK, Ulett GC, Hirst RG, (1998) BALB/c and C57Bl/6 mice infected with virulent Burkholderia pseudomallei provide contrasting animal models for the acute and chronic forms of human melioidosis. Microb Pathog 24: 269-275 doi:10.1006/mpat.1997.0179.
17. Hoppe I, Brenneke B, Rohde M, Kreft A, Häussler S, et al. (1999) Characterization of a murine model of melioidosis: comparison of different strains of mice. Infect Immun 67: 2891-2900.
18. Atkins T, Prior R, Mack K, Russell P, Nelson M, et al. (2002) Characterisation of an acapsular mutant of Burkholderia pseudomallei identified by signature tagged mutagenesis. J Med Microbiol 51: 539-547.
19. Wiersinga WJ, de Vos AF, de Beer R, Wieland CW, Roelofs JJTH, et al. (2008) Inflammation patterns induced by different Burkholderia species in mice. Cell Microbiol 10: 81-87 doi:10.1111/j.1462-5822.2007.01016.x.
20. Ulett GC, Ketheesan N, Hirst RG, (1998) Macrophage-lymphocyte interactions mediate anti-Burkholderia pseudomallei activity. FEMS Immunol Med Microbiol 21: 283-286.
21. Koo GC, Gan Y-H, (2006) The innate interferon gamma response of BALB/c and C57BL/6 mice to in vitro Burkholderia pseudomallei infection. BMC Immunol 7: 19 doi:10.1186/1471-2172-7-19.
22. Breitbach K, Klocke S, Tschernig T, van Rooijen N, Baumann U, et al. (2006) Role of inducible nitric oxide synthase and NADPH oxidase in early control of Burkholderia pseudomallei infection in mice. Infect Immun 74: 6300-6309 doi:10.1128/IAI.00966-06.
23. Eske K, Breitbach K, Köhler J, Wongprompitak P, Steinmetz I, (2009) Generation of murine bone marow derived macrophages in a standardised serum-free cell culture system. J Immunol Methods 342: 13-19.
24. Watanabe H, Numata K, Ito T, Takagi K, Matsukawa A, (2004) Innate immune response in Th1- and Th2-dominant mouse strains. Shock 22: 460-466.
25. Mathews CE, Leiter EH (2005) Chapter 18: Rodent models for the study of diabetes. In: Kahn CR, Weir GC, King GL, Moses AC, Smith RJ, et al., editors. Joslin's Diabetes Mellitus. Philadelphia, Pennsylvania: Lippincott Williams & Wilkins.
26. Isermann B, Vinnikov IA, Madhusudhan T, Herzog S, Kashif M, et al. (2007) Activated protein C protects against diabetic nephropathy by inhibiting endothelial and podocyte apoptosis. Nat Med 13: 1349-1358 doi:10.1038/nm1667.
27. Rakieten N, Rakieten ML, Nadkarni MV, (1963) Studies on the diabetogenic action of streptozotocin (NSC-37917). Cancer Chemother Rep 29: 91-98.
28. Golde WT, Gollobin P, Rodriguez LL, (2005) A rapid, simple, and humane method for submandibular bleeding of mice using a lancet. Lab Anim (NY) 34: 40-43.
29. DeShazer D, Brett PJ, Carlyon R, Woods DE, (1997) Mutagenesis of Burkholderia pseudomallei with Tn5-OT182: isolation of motility mutants and molecular characterization of the flagellin structural gene. J Bacteriol 179: 2116-2125.
30. Wiersinga WJ, de Vos AF, Wieland C, Leendertse M, Roelofs JJTH, et al. (2008) CD14 impairs host defense against Gram-negative sepsis caused by Burkholderia pseudomallei in mice. Clin Infect Dis 198: 1388-1397 doi:10.1086/592220.
31. Wiersinga WJ, Wieland CW, Dessing MC, Chantratita N, Cheng AC, et al. (2007) Toll-like receptor 2 impairs host defense in Gram-negative sepsis caused by Burkholderia pseudomallei (melioidosis). PLoS Med 4: e248 doi:10.1371/journal.pmed.0040248.
32. Ulett GC, Hirst R, Bowden B, Powell K, Norton R, (2003) A comparison of antibiotic regimens in the treatment of acute melioidosis in a mouse model. J Antimicrob Chemother 51: 77-81.
33. Clinical and Laboratory Standards Institute (2009) Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard (M07-A8). 8th ed. Wayne, Pennsylvania: Clinical and Laboratory Standards Institute.
34. Coppack SW, Lant AF, McIntosh CS, Rodgers AV (1990) Pharmacokinetic and pharmacodynamic studies of glibenclamide in non-insulin dependent diabetes mellitus. Available: http://ukpmc.ac.uk/articlerender.cgi?artid=1230045. Accessed 17 May 2009.
35. Easton A, Haque A, Chu K, Lukaszewski R, Bancroft GJ, (2007) A critical role for neutrophils in resistance to experimental infection with Burkholderia pseudomallei. J Infect Dis 195: 99-107 doi:10.1086/509810.
36. Ware LB, Matthay MA, (2000) The acute respiratory distress syndrome. N Engl J Med 342: 1334-1349.
37. Leff JA, Baer JW, Bodman ME, Kirkman JM, Shanley PF, et al. (1994) Interleukin-1-induced lung neutrophil accumulation and oxygen metabolite-mediated lung leak in rats. Am J Physiol 266: L2-8.
38. Koh Y, Hybertson BM, Jepson EK, Cho OJ, Repine JE, (1995) Cytokine-induced neutrophil chemoattractant is necessary for interleukin-1-induced lung leak in rats. J Appl Physiol 79: 472-478.
39. Franchi L, Eigenbrod T, Muñoz-Planillo R, Nuñez G, (2009) The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol 10: 241-247 doi:10.1038/ni.1703.
40. Dinarello CA, (1999) IL-18: A TH1-inducing, proinflammatory cytokine and new member of the IL-1 family. J Allergy Clin Immunol 103: 11-24.
41. Hodgson KA, Govan BL, Walduck AK, Ketheesan N, Morris JL, (2012) Impaired early cytokine responses at the site of infection in a murine model of type 2 diabetes and melioidosis comorbidity. Infect Immun 81: 470-477 doi:10.1128/IAI.00930-12.
42. Deakin AM, Payne AN, Blackwell GJ, (1994) Role of potassium channels in the regulation of cytokine release from THP-1 cells. Inflammation Research 41: C188-C190 doi:10.1007/BF01987632.
43. Laliberte RE, Eggler J, Gabel CA, (1999) ATP treatment of human monocytes promotes caspase-1 maturation and externalization. J Biol Chem 274: 36944-36951.
44. Lauw FN, Simpson AJ, Prins JM, Smith MD, Kurimoto M, et al. (1999) Elevated plasma concentrations of interferon (IFN)-gamma and the IFN-gamma-inducing cytokines interleukin (IL)-18, IL-12, and IL-15 in severe melioidosis. J Infect Dis 180: 1878-1885 doi:10.1086/315155.
45. Van der Poll T, Opal SM, (2008) Host-pathogen interactions in sepsis. Lancet Infect Dis 8: 32-43 doi:10.1016/S1473-3099(07)70265-7.
46. Wiersinga WJ, van der Poll T, White NJ, Day NP, Peacock SJ, (2006) Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat Rev Microbiol 4: 272-282 doi:10.1038/nrmicro1385.
47. Santanirand P, Harley VS, Dance DA, Drasar BS, Bancroft GJ, (1999) Obligatory role of gamma interferon for host survival in a murine model of infection with Burkholderia pseudomallei. Infect Immun 67: 3593-3600.
48. Lertmemongkolchai G, Cai G, Hunter CA, Bancroft GJ, (2001) Bystander activation of CD8+ T cells contributes to the rapid production of IFN-gamma in response to bacterial pathogens. J Immunol 166: 1097-1105.
49. Haque A, Easton A, Smith D, O'Garra A, Van Rooijen N, et al. (2006) Role of T cells in innate and adaptive immunity against murine Burkholderia pseudomallei infection. J Infect Dis 193: 370-379 doi:10.1086/498983.
50. Breitbach K, Sun GW, Koehler J, Eske K, Wongprompitak P, et al. (2009) Caspase-1 mediates resistance in murine melioidosis. Infect Immun 77: 1589-1595 doi:10.1128/IAI.01257-08.
51. Pugin J, Ricou B, Steinberg KP, Suter PM, Martin TR, (1996) Proinflammatory activity in bronchoalveolar lavage fluids from patients with ARDS, a prominent role for interleukin-1. Am J Respir Crit Care Med 153: 1850-1856.
52. Jones AL, Beveridge TJ, Woods DE, (1996) Intracellular survival of Burkholderia pseudomallei. Infect Immun 64: 782-790.
53. Pruksachartvuthi S, Aswapokee N, Thankerngpol K, (1990) Survival of Pseudomonas pseudomallei in human phagocytes. J Med Microbiol 31: 109-114.
54. French CT, Toesca IJ, Wu T-H, Teslaa T, Beaty SM, et al. (2011) Dissection of the Burkholderia intracellular life cycle using a photothermal nanoblade. Proc Natl Acad Sci USA 108: 12095-12100 doi:10.1073/pnas.1107183108.
55. Egan AM, Gordon DL, (1996) Burkholderia pseudomallei activates complement and is ingested but not killed by polymorphonuclear leukocytes. Infect Immun 64: 4952-4959.
56. Wiersinga WJ, Wieland CW, van der Windt GJW, de Boer A, Florquin S, et al. (2007) Endogenous interleukin-18 improves the early antimicrobial host response in severe melioidosis. Infect Immun 75: 3739-3746 doi:10.1128/IAI.00080-07.
57. Ceballos-Olvera I, Sahoo M, Miller MA, Del Barrio L, Re F, (2011) Inflammasome-dependent pyroptosis and IL-18 protect against Burkholderia pseudomallei lung infection while IL-1β is deleterious. PLoS Pathog 7: e1002452.
58. Pompermayer K, Souza DG, Lara GG, Silveira KD, Cassali GD, et al. (2005) The ATP-sensitive potassium channel blocker glibenclamide prevents renal ischemia/reperfusion injury in rats. Kidney Int 67: 1785-1796 doi:10.1111/j.1523-1755.2005.00276.x.
59. Pompermayer K, Amaral FA, Fagundes CT, Vieira AT, Cunha FQ, et al. (2007) Effects of the treatment with glibenclamide, an ATP-sensitive potassium channel blocker, on intestinal ischemia and reperfusion injury. Eur J Pharmacol 556: 215-222 doi:10.1016/j.ejphar.2006.10.065.
60. Ponte-Sucre A, Campos Y, Vázquez J, Moll H, Mendoza-León A, (1997) Sensitivity of Leishmania spp. to glibenclamide and 4-aminopyridine: a tool for the study of drug resistance development. Mem Inst Oswaldo Cruz 92: 601-606.
61. Koh GCKW, Maude RR, Schreiber MF, Limmathurotsakul D, Wiersinga WJ, et al. (2011) Glyburide is anti-inflammatory and associated with reduced mortality in melioidosis. Clin Infect Dis 52: 717-725 doi:10.1093/cid/ciq192.