Linezolid has unique immunomodulatory effects in post-influenza community acquired MRSA pneumonia

PLoS ONE

Volumn 10, Issue 1, 2015, Pages

  Bhan, Urvashi ^a   Podsiad, Amy B ^a   Kovach, Melissa A ^a   Ballinger, Megan N ^b   Keshamouni, Venkateshwar ^a   Standiford, Theodore J ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; GAMMA INTERFERON; INTERLEUKIN 1BETA; LINEZOLID; TUMOR NECROSIS FACTOR ALPHA; VANCOMYCIN; ACETAMIDE DERIVATIVE; OXAZOLIDINONE DERIVATIVE;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL PNEUMONIA; CELL TRANSPORT; COLONY FORMING UNIT; COMMUNITY ACQUIRED PNEUMONIA; CONTROLLED STUDY; IMMUNOMODULATION; INFLAMMATORY CELL; INFLUENZA; INFLUENZA VIRUS A H1N1; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; ANIMAL; COMPLICATION; DRUG EFFECTS; HUMAN; INFLUENZA A VIRUS (H1N1); INFLUENZA, HUMAN; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIOLOGY; PATHOGENICITY; PNEUMONIA, BACTERIAL; STAPHYLOCOCCAL INFECTIONS;

ANIMALIA; BACTERIA (MICROORGANISMS); METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MURINAE; MUS; STAPHYLOCOCCUS AUREUS;

ACETAMIDES; ANIMALS; HUMANS; IMMUNOMODULATION; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; LINEZOLID; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICE; OXAZOLIDINONES; PNEUMONIA, BACTERIAL; STAPHYLOCOCCAL INFECTIONS;

EID: 84961289143     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114574     Document Type: Article

References (65)

1. Rubinstein E, Kollef MH, Nathwani D (2008) Pneumonia caused by methicillin-resistant Staphylococcus aureus. Clin Infect Dis 46 Suppl 5: S378-385. doi: 10.1086/533594PMID: 18462093
2. Finelli L, Fiore A, Dhara R, Brammer L, Shay DK, et al. (2008) Influenza-associated pediatric mortality in the United States: increase of Staphylococcus aureus coinfection. Pediatrics 122: 805-811. doi: 10. 1542/peds.2008-1336 PMID: 18829805
3. Murray RJ, Robinson JO, White JN, Hughes F, Coombs GW, et al. (2010) Community-acquired pneumonia due to pandemic A(H1N1)2009 influenzavirus and methicillin resistant Staphylococcus aureus co-infection. PLoS One 5: e8705. doi: 10.1371/journal.pone.0008705 PMID: 20090931
4. Melles DC, van Leeuwen WB, Boelens HA, Peeters JK, Verbrugh HA, et al. (2006) Panton-Valentine leukocidin genes in Staphylococcus aureus. Emerg Infect Dis 12: 1174-1175. doi: 10.3201/eid1207.n 050865 PMID: 16848048
5. Niemann S, Ehrhardt C, Medina E, Warnking K, Tuchscherr L, et al. (2012) Combined action of influenza virus and Staphylococcus aureus panton-valentine leukocidin provokes severe lung epithelium damage. J Infect Dis 206: 1138-1148. doi: 10.1093/infdis/jis468 PMID: 22837490
6. Colin DA, Mazurier I, Sire S, Finck-Barbancon V (1994) Interaction of the two components of leukocidin from Staphylococcus aureus with human polymorphonuclear leukocyte membranes: sequential binding and subsequent activation. Infect Immun 62: 3184-3188. PMID: 8039887
7. Hensler T, Konig B, Prevost G, Piemont Y, Koller M, et al. (1994) Leukotriene B4 generation and DNA fragmentation induced by leukocidin from Staphylococcus aureus: protective role of granulocytemacrophage colony-stimulating factor (GM-CSF) and G-CSF for human neutrophils. Infect Immun 62: 2529-2535. PMID: 7514577
8. Konig B, Prevost G, Piemont Y, KonigW(1995) Effects of Staphylococcus aureus leukocidins on inflammatory mediator release from human granulocytes. J Infect Dis 171: 607-613. doi: 10.1093/infdis/ 171.3.607 PMID: 7533198
9. Szmigielski S, Prevost G, Monteil H, Colin DA, Jeljaszewicz J (1999) Leukocidal toxins of staphylococci. Zentralbl Bakteriol 289: 185-201. doi: 10.1016/S0934-8840(99)80105-4 PMID: 10360319
10. Meunier O, Falkenrodt A, Monteil H, Colin DA (1995) Application of flow cytometry in toxinology: pathophysiology of human polymorphonuclear leukocytes damaged by a pore-forming toxin from Staphylococcus aureus. Cytometry 21: 241-247. doi: 10.1002/cyto.990210304 PMID: 8582246
11. Wunderink RG (2013) How important is methicillin-resistant Staphylococcus aureus as a cause of community-acquired pneumonia and what is best antimicrobial therapy? Infect Dis Clin North Am 27: 177-188. doi: 10.1016/j.idc.2012.11.006 PMID: 23398873
12. Wunderink RG, Niederman MS, Kollef MH, Shorr AF, Kunkel MJ, et al. (2012) Linezolid in methicillin-resistant Staphylococcus aureus nosocomial pneumonia: a randomized, controlled study. Clin Infect Dis 54: 621-629. doi: 10.1093/cid/cir895 PMID: 22247123
13. Dumitrescu O, Boisset S, Badiou C, Bes M, Benito Y, et al. (2007) Effect of antibiotics on Staphylococcus aureus producing Panton-Valentine leukocidin. Antimicrob Agents Chemother 51: 1515-1519. doi: 10.1128/AAC.01201-06 PMID: 17242137
14. Yoshizawa S, Tateda K, Saga T, Ishii Y, Yamaguchi K (2012) Virulence-suppressing effects of linezolid on methicillin-resistant Staphylococcus aureus: possible contribution to early defervescence. Antimicrob Agents Chemother 56: 1744-1748. doi: 10.1128/AAC.05430-11 PMID: 22290944
15. Schwarzmann SW, Adler JL, Sullivan RJ Jr., MarineWM(1971) Bacterial pneumonia during the Hong Kong influenza epidemic of 1968-1969. Arch Intern Med 127: 1037-1041. doi: 10.1001/archinte.127. 6.1037 PMID: 5578560
16. Martin CM, KuninCM, Gottlieb LS, Finland M (1959) Asian influenza A in Boston, 1957-1958. II. Severe staphylococcal pneumonia complicating influenza. AMA Arch Intern Med 103: 532-542.PMID: 13636471
17. Mandell LA, Wunderink R (2012) Methicillin-resistant staphylococcus aureus and community-acquired pneumonia: an evolving relationship. Clin Infect Dis 54: 1134-1136. doi: 10.1093/cid/cis045 PMID: 22438344
18. Tashiro M, Klenk HD, Rott R (1987) Inhibitory effect of a protease inhibitor, leupeptin, on the development of influenza pneumonia, mediated by concomitant bacteria. J Gen Virol 68 (Pt 7): 2039-2041.doi: 10.1099/0022-1317-68-7-2039PMID: 3298542
19. Tashiro M, Ciborowski P, Klenk HD, Pulverer G, Rott R (1987) Role of Staphylococcus protease in the development of influenza pneumonia. Nature 325: 536-537. doi: 10.1038/325536a0 PMID: 3543690
20. Nickerson CL, Jakab GJ (1990) Pulmonary antibacterial defenses during mild and severe influenza virus infection. Infect Immun 58: 2809-2814. PMID: 2143751
21. Davison VE, Sanford BA (1981) Adherence of staphylococcus aureus to influenza A virus-infected Madin-Darby canine kidney cell cultures. Infect Immun 32: 118-126. PMID: 7216481
22. Abramson JS, Lewis JC, Lyles DS, Heller KA, Mills EL, et al. (1982) Inhibition of neutrophil lysosomephagosome fusion associated with influenza virus infection in vitro. Role in depressed bactericidal activity. J Clin Invest 69: 1393-1397. doi: 10.1172/JCI110580PMID: 7085879
23. Abramson JS, Giebink GS, Quie PG (1982) Influenza A virus-induced polymorphonuclear leukocyte dysfunction in the pathogenesis of experimental pneumococcal otitis media. Infect Immun 36: 289-296. PMID: 7076299
24. Sun K, MetzgerDW (2014) Influenza infection suppresses NADPH oxidase-dependent phagocytic bacterial clearance and enhances susceptibility to secondary methicillin-resistant Staphylococcus aureus infection. J Immunol 192: 3301-3307. doi: 10.4049/jimmunol.1303049 PMID: 24563256
25. Iverson AR, Boyd KL, McAuley JL, Plano LR, Hart ME, et al. (2011) Influenza virus primes mice for pneumonia from Staphylococcus aureus. J Infect Dis 203: 880-888. doi: 10.1093/infdis/jiq113 PMID: 21278211
26. Lodise TP, McKinnon PS, Swiderski L, Rybak MJ (2003) Outcomes analysis of delayed antibiotic treatment for hospital-acquired Staphylococcus aureus bacteremia. Clin Infect Dis 36: 1418-1423. doi: 10. 1086/375057 PMID: 12766837
27. Wunderink RG, Rello J, Cammarata SK, Croos-Dabrera RV, Kollef MH (2003) Linezolid vs vancomycin: analysis of two double-blind studies of patients with methicillin-resistant Staphylococcus aureus nosocomial pneumonia. Chest 124: 1789-1797. doi: 10.1378/chest.124.5.1789 PMID: 14605050
28. Kollef MH, Rello J, Cammarata SK, Croos-Dabrera RV, Wunderink RG (2004) Clinical cure and survival in Gram-positive ventilator-associated pneumonia: retrospective analysis of two double-blind studies comparing linezolid with vancomycin. Intensive Care Med 30: 388-394. doi: 10.1007/s00134-003-2088-1 PMID: 14714107
29. Conte JE Jr., Golden JA, Kipps J, Zurlinden E (2002) Intrapulmonary pharmacokinetics of linezolid. Antimicrob Agents Chemother 46: 1475-1480. doi: 10.1128/AAC.46.5.1475-1480.2002 PMID: 11959585
30. Honeybourne D, Tobin C, Jevons G, Andrews J, Wise R (2003) Intrapulmonary penetration of linezolid. J Antimicrob Chemother 51: 1431-1434. doi: 10.1093/jac/dkg262 PMID: 12746375
31. Klein B, Brailly H (1995) Cytokine-binding proteins: stimulating antagonists. Immunol Today 16: 216-220. doi: 10.1016/0167-5699(95)80161-8 PMID: 7779250
32. Morikawa K, Watabe H, Araake M, Morikawa S (1996) Modulatory effect of antibiotics on cytokine production by human monocytes in vitro. Antimicrob Agents Chemother 40: 1366-1370. PMID: 8726002
33. Araujo FG, Slifer TL, Remington JS (2002) Inhibition of secretion of interleukin-1alpha and tumor necrosis factor alpha by the ketolide antibiotic telithromycin. Antimicrob Agents Chemother 46: 3327-3330. doi: 10.1128/AAC.46.10.3327-3330.2002 PMID: 12234873
34. Khan AA, Slifer TR, Araujo FG, Remington JS (1999) Effect of clarithromycin and azithromycin on production of cytokines by human monocytes. Int J Antimicrob Agents 11: 121-132. doi: 10.1016/S0924-8579(98)00091-0 PMID: 10221415
35. Garcia-Roca P, Mancilla-Ramirez J, Santos-Segura A, Fernandez-Aviles M, Calderon-Jaimes E (2006) Linezolid diminishes inflammatory cytokine production from human peripheral blood mononuclear cells. Arch Med Res 37: 31-35. doi: 10.1016/j.arcmed.2005.05.022 PMID: 16314183
36. McNamee LA, Harmsen AG (2006) Both influenza-induced neutrophil dysfunction and neutrophil-independent mechanisms contribute to increased susceptibility to a secondary Streptococcus pneumoniae infection. Infect Immun 74: 6707-6721. doi: 10.1128/IAI.00789-06 PMID: 16982840
37. Keel RA, Crandon JL, Nicolau DP (2012) Pharmacokinetics and pulmonary disposition of tedizolid and linezolid in a murine pneumonia model under variable conditions. Antimicrob Agents Chemother 56: 3420-3422. doi: 10.1128/AAC.06121-11 PMID: 22430966
38. Estes KS, Derendorf H (2010) Comparison of the pharmacokinetic properties of vancomycin, linezolid, tigecyclin, and daptomycin. Eur J Med Res 15: 533-543. doi: 10.1186/2047-783X-15-12-533 PMID: 21163728
39. Bhan U, Lukacs NW, Osterholzer JJ, Newstead MW, Zeng X, et al. (2007) TLR9 is required for protective innate immunity in Gram-negative bacterial pneumonia: role of dendritic cells. J Immunol 179: 3937-3946. doi: 10.4049/jimmunol.179.6.3937 PMID: 17785831
40. Bhan U, Trujillo G, Lyn-Kew K, Newstead MW, Zeng X, et al. (2008) Toll-like receptor 9 regulates the lung macrophage phenotype and host immunity in murine pneumonia caused by Legionella pneumophila. Infect Immun 76: 2895-2904. doi: 10.1128/IAI.01489-07 PMID: 18426877
41. Bosmann M, Grailer JJ, Ruemmler R, Russkamp NF, Zetoune FS, et al. (2013) Extracellular histones are essential effectors of C5aR- and C5L2-mediated tissue damage and inflammation in acute lung injury. FASEB J 27: 5010-5021. doi: 10.1096/fj.13-236380 PMID: 23982144
42. Suter PM, Suter S, Girardin E, Roux-Lombard P, Grau GE, et al. (1992) High bronchoalveolar levels of tumor necrosis factor and its inhibitors, interleukin-1, interferon, and elastase, in patients with adult respiratory distress syndrome after trauma, shock, or sepsis. Am Rev Respir Dis 145: 1016-1022. doi: 10.1164/ajrccm/145.5.1016 PMID: 1586041
43. Patel BV, Wilson MR, O'Dea KP, Takata M (2013) TNF-induced death signaling triggers alveolar epithelial dysfunction in acute lung injury. J Immunol 190: 4274-4282. doi: 10.4049/jimmunol.1202437 PMID: 23487422
44. Chavanet P (2013) The ZEPHyR study: a randomized comparison of linezolid and vancomycin for MRSA pneumonia. Med Mal Infect 43: 451-455. doi: 10.1016/j.medmal.2013.09.011 PMID: 24238896
45. Liu X, He Y, Xiao K, White JR, Fusco DN, et al. (2013) Effect of linezolid on clinical severity and pulmonary cytokines in a murine model of influenza A and Staphylococcus aureus coinfection. PLoS One 8: e57483. doi: 10.1371/journal.pone.0057483 PMID: 23478252
46. Ware LB (2006) Pathophysiology of acute lung injury and the acute respiratory distress syndrome. Semin Respir Crit Care Med 27: 337-349. doi: 10.1055/s-2006-948288 PMID: 16909368
47. Lucas R, Verin AD, Black SM, Catravas JD (2009) Regulators of endothelial and epithelial barrier integrity and function in acute lung injury. Biochem Pharmacol 77: 1763-1772. doi: 10.1016/j.bcp.2009.01. 014 PMID: 19428331
48. Mukhopadhyay S, Hoidal JR, Mukherjee TK (2006) Role of TNFalpha in pulmonary pathophysiology. Respir Res 7: 125. doi: 10.1186/1465-9921-7-125 PMID: 17034639
49. Perrone LA, Szretter KJ, Katz JM, Mizgerd JP, Tumpey TM (2010) Mice lacking both TNF and IL-1 receptors exhibit reduced lung inflammation and delay in onset of death following infection with a highly virulent H5N1 virus. J Infect Dis 202: 1161-1170. doi: 10.1086/656365 PMID: 20815704
50. Breslow-Deckman JM, Mattingly CM, Birket SE, Hoskins SN, Ho TN, et al. (2013) Linezolid decreases susceptibility to secondary bacterial pneumonia postinfluenza infection in mice through its effects on IFN-gamma. J Immunol 191: 1792-1799. doi: 10.4049/jimmunol.1300180 PMID: 23833238
51. Manzer R, Dinarello CA, McConville G, Mason RJ (2008) Ozone exposure of macrophages induces an alveolar epithelial chemokine response through IL-1alpha. Am J Respir Cell Mol Biol 38: 318-323. doi: 10.1165/rcmb.2007-0250OC PMID: 17901407
52. Thorley AJ, Ford PA, Giembycz MA, Goldstraw P, Young A, et al. (2007) Differential regulation of cytokine release and leukocyte migration by lipopolysaccharide-stimulated primary human lung alveolar type II epithelial cells and macrophages. J Immunol 178: 463-473. doi: 10.4049/jimmunol.178.1.463 PMID: 17182585
53. Chan MC, Cheung CY, Chui WH, Tsao SW, Nicholls JM, et al. (2005) Proinflammatory cytokine responses induced by influenza A (H5N1) viruses in primary human alveolar and bronchial epithelial cells. Respir Res 6: 135. doi: 10.1186/1465-9921-6-135 PMID: 16283933
54. Abraham E (2003) Neutrophils and acute lung injury. Crit Care Med 31: S195-199. doi: 10.1097/01. CCM.0000057843.47705.E8 PMID: 12682440
55. Matthay MA, Eschenbacher WL, Goetzl EJ (1984) Elevated concentrations of leukotriene D4 in pulmonary edema fluid of patients with the adult respiratory distress syndrome. J Clin Immunol 4: 479-483. doi: 10.1007/BF00916578 PMID: 6511865
56. Parsons PE, Fowler AA, Hyers TM, Henson PM (1985) Chemotactic activity in bronchoalveolar lavage fluid from patients with adult respiratory distress syndrome. Am Rev Respir Dis 132: 490-493. PMID: 4037522
57. Steinberg KP, Milberg JA, Martin TR, Maunder RJ, Cockrill BA, et al. (1994) Evolution of bronchoalveolar cell populations in the adult respiratory distress syndrome. Am J Respir Crit Care Med 150: 113-122. doi: 10.1164/ajrccm.150.1.8025736 PMID: 8025736
58. Abraham E, Carmody A, Shenkar R, Arcaroli J (2000) Neutrophils as early immunologic effectors in hemorrhage- or endotoxemia-induced acute lung injury. Am J Physiol Lung Cell Mol Physiol 279: L1137-1145. PMID: 11076804
59. Craven RR, Gao X, Allen IC, Gris D, Bubeck Wardenburg J, et al. (2009) Staphylococcus aureus alpha-hemolysin activates the NLRP3-inflammasome in human and mouse monocytic cells. PLoS One 4: e7446. doi: 10.1371/journal.pone.0007446 PMID: 19826485
60. Mariathasan S, Weiss DS, Newton K, McBride J, O'Rourke K, et al. (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440: 228-232. doi: 10.1038/nature04515 PMID: 16407890
61. Holzinger D, Gieldon L, Mysore V, Nippe N, Taxman DJ, et al. (2012) Staphylococcus aureus Panton-Valentine leukocidin induces an inflammatory response in human phagocytes via the NLRP3 inflammasome. J Leukoc Biol 92: 1069-1081. doi: 10.1189/jlb.0112014 PMID: 22892107
62. Gillet Y, Issartel B, Vanhems P, Fournet JC, Lina G, et al. (2002) Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet 359: 753-759. doi: 10.1016/S0140-6736(02)07877-7 PMID: 11888586
63. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, et al. (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298: 1763-1771. doi: 10.1001/jama. 298.15.1763 PMID: 17940231
64. Hensler T, Koller M, Prevost G, Piemont Y, KonigW(1994) GTP-binding proteins are involved in the modulated activity of human neutrophils treated with the Panton-Valentine leukocidin from Staphylococcus aureus. Infect Immun 62: 5281-5289. PMID: 7960106
65. Stevens DL, Ma Y, Salmi DB, McIndoo E, Wallace RJ, et al. (2007) Impact of antibiotics on expression of virulence-associated exotoxin genes in methicillin-sensitive and methicillin-resistant Staphylococcus aureus. J Infect Dis 195: 202-211. doi: 10.1086/510396 PMID: 17191165