Priming innate immune responses to infection by cyclooxygenase inhibition kills antibiotic-susceptible and -resistant bacteria

Blood

Volumn 116, Issue 16, 2010, Pages 2950-2959

  Stables, Melanie J ^a   Newson, Justine ^a   Ayoub, Samir S ^b   Brown, Jeremy ^c   Hyams, Catherine J ^c   Gilroy, Derek W ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

5 (4 CHLOROPHENYL) 1 (4 METHOXYPHENYL) 3 TRIFLUOROMETHYL 1H PYRAZOLE; ACETYLSALICYLIC ACID; BETA LACTAM; CYCLIC AMP; CYCLOOXYGENASE 1; INDOMETACIN; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; NAPROXEN; NONSTEROID ANTIINFLAMMATORY AGENT; PENICILLIN G; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; INFECTION; INNATE IMMUNITY; LEUKOCYTE; MINIMUM INHIBITORY CONCENTRATION; MOUSE; NONHUMAN; PERITONITIS; PHAGOCYTOSIS; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; STREPTOCOCCUS PNEUMONIAE;

EID: 77958191161     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-05-284844     Document Type: Article

References (50)

1. Livermore DM. Minimising antibiotic resistance. Lancet Infect Dis. 2005;5(7):450-459.
2. Moncada S, Vane JR. Pharmacology and endogenous roles of prostaglandin endoperoxides, thromboxane A2, and prostacyclin. Pharmacol Rev. 1978;30(3):293-331. (Pubitemid 10198932)
3. Simmons DL, Botting RM, Hla T. Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol Rev. 2004;56(3):387-437. (Pubitemid 39096597)
4. Matsuoka T, Narumiya S. Prostaglandin receptor signaling in disease. ScientificWorldJournal. 2007;7:1329-1347.
5. Aronoff DM, Canetti C, Serezani CH, Luo M, Peters-Golden M. Cutting edge: macrophage inhibition by cyclic AMP (cAMP): differential roles of protein kinase A and exchange protein directly activated by cAMP-1. J Immunol. 2005;174(2):595-599.
6. Crawford MA, Aylott CV, Bourdeau RW, Bokoch GM. Bacillus anthracis toxins inhibit human neutrophil NADPH oxidase activity. J Immunol. 2006;176(12):7557-7565.
7. Mitsuyama T, Takeshige K, Minakami S. Cyclic AMP inhibits the respiratory burst of electropermeabilized human neutrophils at a downstream site of protein kinase C. Biochim Biophys Acta. 1993;1177(2):167-173. (Pubitemid 23169571)
8. Hwang TL, Yeh SH, Leu YL, Chern CY, Hsu HC. Inhibition of superoxide anion and elastase release in human neutrophils by 3′-isopropoxychalcone via a cAMP-dependent pathway. Br J Pharmacol. 2006;148(1):78-87.
9. Aronoff DM, Canetti C, Peters-Golden M. Prostaglandin E2 inhibits alveolar macrophage phagocytosis through an E-prostanoid 2 receptor-mediated increase in intracellular cyclic AMP. J Immunol. 2004;173(1):559-565. (Pubitemid 38797384)
10. Vane JR. Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat New Biol. 1971;231(25):232-235.
11. Aronoff DM, Lewis C, Serezani CH, et al. E-Prostanoid 3 Receptor Deletion Improves Pulmonary Host Defense and Protects Mice from Death in Severe Streptococcus pneumoniae Infection. J Immunol. 2009.
12. Fong CH, Bebien M, Didierlaurent A, et al. An antiinflammatory role for IKKbeta through the inhibition of "classical" macrophage activation. J Exp Med. 2008;205(6):1269-1276.
13. Gilroy DW, Colville-Nash PR, Willis D, Chivers J, Paul-Clark MJ, Willoughby DA. Inducible cyclooxygenase may have anti-inflammatory properties. Nat Med. 1999;5(6):698-701.
14. Brown JS, Hussell T, Gilliland SM, et al. The classical pathway is the dominant complement pathway required for innate immunity to Streptococcus pneumoniae infection in mice. Proc Natl Acad Sci U S A. 2002;99(26):16969-16974.
15. Yuste J, Sen A, Truedsson L, et al. Impaired opsonization with C3b and phagocytosis of Streptococcus pneumoniae in sera from subjects with defects in the classical complement pathway. Infect Immun. 2008;76(8):3761-3770.
16. Jomaa M, Yuste J, Paton JC, Jones C, Dougan G, Brown JS. Antibodies to the iron uptake ABC transporter lipoproteins PiaA and PiuA promote opsonophagocytosis of Streptococcus pneumoniae. Infect Immun. 2005;73(10):6852-6859.
17. Warner TD, Giuliano F, Vojnovic I, Bukasa A, Mitchell JA, Vane JR. Nonsteroid drug selectivities for cyclo-oxygenase-1 rather than cyclo-oxygenase-2 are associated with human gastrointestinal toxicity: a full in vitro analysis. Proc Natl Acad Sci U S A. 1999;96(13):7563-7568.
18. van den Ouweland FA, Franssen MJ, van de Putte LB, Tan Y, van Ginneken CA, Gribnau FW. Naproxen pharmacokinetics in patients with rheumatoid arthritis during active polyarticular inflammation. Br J Clin Pharmacol. 1987;23(2):189-193. (Pubitemid 17113495)
19. Gilroy DW, Tomlinson A, Willoughby DA. Differential effects of inhibitors of cyclooxygenase (cyclooxygenase 1 and cyclooxygenase 2) in acute inflammation. Eur J Pharmacol. 1998;355(2-3):211-217,. (Pubitemid 28404704)
20. Wallace JL. Selective COX-2 inhibitors: is the water becoming muddy? Trends Pharmacol Sci. 1999;20(1):4-6. (Pubitemid 29304515)
21. Morham SG, Langenbach R, Loftin CD, et al. Prostaglandin synthase 2 gene disruption causes severe renal pathology in the mouse. Cell. 1995;83(3):473-482.
22. Serezani CH, Ballinger MN, Aronoff DM, Peters-Golden M. Cyclic AMP: master regulator of innate immune cell function. Am J Respir Cell Mol Biol. 2008;39(2):127-132.
23. Bystrom J, Evans I, Newson J, et al. Resolution-phase macrophages possess a unique inflammatory and bactericidal phenotype that is controlled by cAMP. Blood. 2008;112(10).
24. Soares AC, Souza DG, Pinho V, et al. Impaired host defense to Klebsiella pneumoniae infection in mice treated with the PDE4 inhibitor rolipram. Br J Pharmacol. 2003;140(5):855-862.
25. Spite M, Norling LV, Summers L, et al. Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis. Nature. 2009;461(7268):1287-1291.
26. Mancuso P, Nana-Sinkam P, Peters-Golden M. Leukotriene B4 augments neutrophil phagocytosis of Klebsiella pneumoniae. Infect Immun. 2001;69(4):2011-2016. (Pubitemid 32239663)
27. Mancuso P, Standiford TJ, Marshall T, Peters-Golden M. 5-Lipoxygenase reaction products modulate alveolar macrophage phagocytosis of Klebsiella pneumoniae. Infect Immun. 1998;66(11):5140-5146.
28. Spinas GA, Bloesch D, Keller U, Zimmerli W, Cammisuli S. Pretreatment with ibuprofen augments circulating tumor necrosis factor-alpha, interleukin-6, and elastase during acute endotoxinemia. J Infect Dis. 1991;163(1):89-95.
29. Martich GD, Danner RL, Ceska M, Suffredini AF. Detection of interleukin 8 and tumor necrosis factor in normal humans after intravenous endotoxin: the effect of antiinflammatory agents. J Exp Med. 1991;173(4):1021-1024.
30. Michie HR, Manogue KR, Spriggs DR, et al. Detection of circulating tumor necrosis factor after endotoxin administration. N Engl J Med. 1988;318(23):1481-1486.
31. Fisher CJ, Jr, Agosti JM, Opal SM, et al. Treatment of septic shock with the tumor necrosis factor receptor:Fc fusion protein. The Soluble TNF Receptor Sepsis Study Group. N Engl J Med. 1996;334(26):1697-1702.
32. Brun-Buisson CJ, Saada M, Trunet P, Rapin M, Roujeau JC, Revuz J. Haemolytic streptococcal gangrene and nonsteroidal anti-inflammatory drugs. Br Med J (Clin Res Ed). 1985;290(6484):1786. (Pubitemid 15059214)
33. Veenstra RP, Manson WE, van der Werf TS, et al. Fulminant necrotizing fasciitis and nonsteroidal anti-inflammatory drugs. Intensive Care Med. 2001;27(11):1831.
34. Rimailho A, Riou B, Richard C, Auzepy P. Fulminant necrotizing fasciitis and nonsteroidal antiinflammatory drugs. J Infect Dis. 1987;155(1):143-146. (Pubitemid 17225098)
35. Aronoff DM, Bloch KC. Assessing the relationship between the use of nonsteroidal antiinflammatory drugs and necrotizing fasciitis caused by group A streptococcus. Medicine (Baltimore). 2003;82(4):225-235.
36. Legras A, Giraudeau B, Jonville-Bera AP, et al. A multicentre case-control study of nonsteroidal anti-inflammatory drugs as a risk factor for severe sepsis and septic shock. Crit Care. 2009;13(2):R43.
37. Abdeltawab NF, Aziz RK, Kansal R, et al. An unbiased systems genetics approach to mapping genetic loci modulating susceptibility to severe streptococcal sepsis. PLoS Pathog. 2008;4(4):e1000042.
38. Levy SB, Marshall B. Antibacterial resistance worldwide: causes, challenges and responses. Nat Med. 2004;10(12 Suppl):S122-129.
39. Marquez B. Bacterial efflux systems and efflux pumps inhibitors. Biochimie. 2005;87(12):1137-1147. (Pubitemid 41572643)
40. Bassetti M, Righi E, Viscoli C. Novel beta-lactam antibiotics and inhibitor combinations. Expert Opin Investig Drugs. 2008;17(3):285-296.
41. Housby JN, Mann NH. Phage therapy. Drug Discov Today. 2009;14(11-12):536-540.
42. Gillor O, Etzion A, Riley MA. The dual role of bacteriocins as anti- and probiotics. Appl Microbiol Biotechnol. 2008;81(4):591-606.
43. Wallace JL, McKnight W, Reuter BK, Vergnolle N. NSAID-induced gastric damage in rats: requirement for inhibition of both cyclooxygenase 1 and 2. Gastroenterology. 2000;119(3):706-714.
44. Sadikot RT, Zeng H, Azim AC, et al. Bacterial clearance of Pseudomonas aeruginosa is enhanced by the inhibition of COX-2. Eur J Immunol. 2007;37(4):1001-1009.
45. Gilroy DW, Newson J, Sawmynaden P, Willoughby DA, Croxtall JD. A novel role for phospholipase A2 isoforms in the checkpoint control of acute inflammation. FASEB J. 2004;18(3):489-498. (Pubitemid 38326305)
46. Gilroy DW, Colville-Nash PR, McMaster S, Sawatzky DA, Willoughby DA, Lawrence T. Inducible cyclooxygenase-derived 15-deoxy(Delta)12-14PGJ2 brings about acute inflammatory resolution in rat pleurisy by inducing neutrophil and macrophage apoptosis. FASEB J. 2003;17(15):2269-2271.
47. Rajakariar R, Hilliard M, Lawrence T, et al. Hematopoietic prostaglandin D2 synthase controls the onset and resolution of acute inflammation through PGD2 and 15-deoxyDelta12 14 PGJ2. Proc Natl Acad Sci U S A. 2007;104(52):20979- 20984.
48. Serhan CN, Hong S, Gronert K, et al. Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med. 2002;196(8):1025- 1037.
49. Claria J, Serhan CN. Aspirin triggers previously undescribed bioactive eicosanoids by human endothelial cell-leukocyte interactions. Proc Natl Acad Sci U S A. 1995;92(21):9475-9479.
50. Godson C, Mitchell S, Harvey K, Petasis NA, Hogg N, Brady HR. Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J Immunol. 2000;164(4):1663-1667.