Phenol-soluble modulin peptides contribute to influenza A virusassociated Staphylococcus aureus pneumonia

Infection and Immunity

Volumn 85, Issue 12, 2017, Pages

  Bloes, Dominik Alexander ^a   Haasbach, Emanuel ^b   Hartmayer, Carmen ^b   Hertlein, Tobias ^c   Klingel, Karin ^b   Kretschmer, Dorothee ^a   Planz, Oliver ^b   Peschel, Andreas ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Influenza; Pneumonia; Staphylococcus aureus; Toxins

Indexed keywords

BACTERIAL PROTEIN; CYTOTOXIN; INTERLEUKIN 8; PHENOL SOLUBLE MODULIN PEPTIDE; STAPHYLOCOCCUS TOXIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL TOXIN; STAPHYLOCOCCAL DELTA TOXIN;

2009 H1N1 INFLUENZA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; HUMAN; HUMAN CELL; INFLUENZA A; LUNG ALVEOLUS EPITHELIUM CELL; MORTALITY RATE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; STAPHYLOCOCCAL PNEUMONIA; ANIMAL; CELL LINE; COMPLICATION; DISEASE MODEL; EPITHELIUM CELL; GROWTH, DEVELOPMENT AND AGING; INFLUENZA; INFLUENZA A VIRUS (H1N1); METABOLISM; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; PIG; SURVIVAL ANALYSIS; VIROLOGY;

ANIMALS; BACTERIAL TOXINS; CELL LINE; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICE; PNEUMONIA, STAPHYLOCOCCAL; SURVIVAL ANALYSIS; SWINE; VIRULENCE FACTORS;

EID: 85034063195     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00620-17     Document Type: Article

References (41)

1. Ruuskanen O, Lahti E, Jennings LC, Murdoch DR. 2011. Viral pneumonia. Lancet 377:1264-1275. https://doi.org/10.1016/S0140-6736(10)61459-6
2. Pittet LA, Hall-Stoodley L, Rutkowski MR, Harmsen AG. 2010. Influenza virus infection decreases tracheal mucociliary velocity and clearance of Streptococcus pneumoniae. Am J Respir Cell Mol Biol 42:450-460. https://doi.org/10.1165/rcmb.2007-0417OC
3. Zeng H, Goldsmith CS, Maines TR, Belser JA, Gustin KM, Pekosz A, Zaki SR, Katz JM, Tumpey TM. 2013. Tropism and infectivity of influenza virus, including highly pathogenic avian H5N1 virus, in ferret tracheal differentiated primary epithelial cell cultures. J Virol 87:2597-2607. https:// doi.org/10.1128/JVI.02885-12
4. Gill JR, Sheng ZM, Ely SF, Guinee DG, Beasley MB, Suh J, Deshpande C, Mollura DJ, Morens DM, Bray M, Travis WD, Taubenberger JK. 2010. Pulmonary pathologic findings of fatal 2009 pandemic influenza A/H1N1 viral infections. Arch Pathol Lab Med 134:235-243
5. Mauad T, Hajjar LA, Callegari GD, da Silva LF, Schout D, Galas FR, Alves VA, Malheiros DM, Auler JO, Jr, Ferreira AF, Borsato MR, Bezerra SM, Gutierrez PS, Caldini ET, Pasqualucci CA, Dolhnikoff M, Saldiva PH. 2010. Lung pathology in fatal novel human influenza A (H1N1) infection. Am J Respir Crit Care Med 181:72-79. https://doi.org/10.1164/rccm.200909-1420OC
6. Centers for Disease Control and Prevention. 2009. Bacterial coinfections in lung tissue specimens from fatal cases of 2009 pandemic influenza A (H1N1)-United States, May-August 2009. MMWR Morb Mortal Wkly Rep 58:1071-1074
7. Nolte FS. 2008. Molecular diagnostics for detection of bacterial and viral pathogens in community-acquired pneumonia. Clin Infect Dis 47(Suppl 3):S123-S126. https://doi.org/10.1086/591392
8. Lynch JP, III. 2001. Hospital-acquired pneumonia: risk factors, microbiology, and treatment. Chest 119:373S-384S. https://doi.org/10.1378/chest.119.2_suppl.373S
9. Sohn KM, Chung DR, Baek JY, Kim SH, Joo EJ, Ha YE, Ko KS, Kang CI, Peck KR, Song JH. 2012. Post-influenza pneumonia caused by the USA300 community-associated methicillin-resistant Staphylococcus aureus in Korea. J Korean Med Sci 27:313-316. https://doi.org/10.3346/jkms.2012.27.3.313
10. Finelli L, Fiore A, Dhara R, Brammer L, Shay DK, Kamimoto L, Fry A, Hageman J, Gorwitz R, Bresee J, Uyeki T. 2008. Influenza-associated pediatric mortality in the United States: increase of Staphylococcus aureus coinfection. Pediatrics 122:805-811. https://doi.org/10.1542/peds.2008-1336
11. Bhat N, Wright JG, Broder KR, Murray EL, Greenberg ME, Glover MJ, Likos AM, Posey DL, Klimov A, Lindstrom SE, Balish A, Medina MJ, Wallis TR, Guarner J, Paddock CD, Shieh WJ, Zaki SR, Sejvar JJ, Shay DK, Harper SA, Cox NJ, Fukuda K, Uyeki TM. 2005. Influenza-associated deaths among children in the United States, 2003-2004. N Engl J Med 353:2559-2567. https://doi.org/10.1056/NEJMoa051721
12. Marrie TJ, Fine MJ, Obrosky DS, Coley C, Singer DE, Kapoor WN. 1998. Community-acquired pneumonia due to Escherichia coli. Clin Microbiol Infect 4:717-723. https://doi.org/10.1111/j.1469-0691.1998.tb00657.x
13. King P. 2012. Haemophilus influenzae and the lung (Haemophilus and the lung). Clin Transl Med 1:10. https://doi.org/10.1186/2001-1326-1-10
14. Prince SE, Dominger KA, Cunha BA, Klein NC. 1997. Klebsiella pneumoniae pneumonia. Heart Lung 26:413-417. https://doi.org/10.1016/ S0147-9563(97)90028-5
15. Fujitani S, Sun HY, Yu VL, Weingarten JA. 2011. Pneumonia due to Pseudomonas aeruginosa. Part I: epidemiology, clinical diagnosis, and source. Chest 139:909-919. https://doi.org/10.1378/chest.10-0166
16. Hageman JC, Uyeki TM, Francis JS, Jernigan DB, Wheeler JG, Bridges CB, Barenkamp SJ, Sievert DM, Srinivasan A, Doherty MC, McDougal LK, Killgore GE, Lopatin UA, Coffman R, MacDonald JK, McAllister SK, Fosheim GE, Patel JB, McDonald LC. 2006. Severe community-acquired pneumonia due to Staphylococcus aureus, 2003-04 influenza season. Emerg Infect Dis 12:894-899. https://doi.org/10.3201/eid1206.051141
17. Rubinstein E, Kollef MH, Nathwani D. 2008. Pneumonia caused by methicillin-resistant Staphylococcus aureus. Clin Infect Dis 46(Suppl 5): S378-S385. https://doi.org/10.1086/533594
18. Chambers HF, Deleo FR. 2009. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7:629-641. https://doi.org/10.1038/nrmicro2200
19. Bubeck Wardenburg J, Patel RJ, Schneewind O. 2007. Surface proteins and exotoxins are required for the pathogenesis of Staphylococcus aureus pneumonia. Infect Immun 75:1040-1044. https://doi.org/10.1128/IAI.01313-06
20. Iverson AR, Boyd KL, McAuley JL, Plano LR, Hart ME, McCullers JA. 2011. Influenza virus primes mice for pneumonia from Staphylococcus aureus. J Infect Dis 203:880-888. https://doi.org/10.1093/infdis/jiq113
21. Loffler B, Niemann S, Ehrhardt C, Horn D, Lanckohr C, Lina G, Ludwig S, Peters G. 2013. Pathogenesis of Staphylococcus aureus necrotizing pneumonia: the role of PVL and an influenza coinfection. Expert Rev Anti Infect Ther 11:1041-1051. https://doi.org/10.1586/14787210.2013.827891
22. Diep BA, Chan L, Tattevin P, Kajikawa O, Martin TR, Basuino L, Mai TT, Marbach H, Braughton KR, Whitney AR, Gardner DJ, Fan X, Tseng CW, Liu GY, Badiou C, Etienne J, Lina G, Matthay MA, DeLeo FR, Chambers HF. 2010. Polymorphonuclear leukocytes mediate Staphylococcus aureus Panton-Valentine leukocidin-induced lung inflammation and injury. Proc Natl Acad Sci U S A 107:5587-5592. https://doi.org/10.1073/pnas.0912403107
23. Peschel A, Otto M. 2013. Phenol-soluble modulins and staphylococcal infection. Nat Rev Microbiol 11:667-673. https://doi.org/10.1038/ nrmicro3110
24. Wang R, Braughton KR, Kretschmer D, Bach TH, Queck SY, Li M, Kennedy AD, Dorward DW, Klebanoff SJ, Peschel A, DeLeo FR, Otto M. 2007. Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat Med 13:1510-1514. https://doi.org/10.1038/nm1656
25. Rautenberg M, Joo HS, Otto M, Peschel A. 2011. Neutrophil responses to staphylococcal pathogens and commensals via the formyl peptide receptor 2 relates to phenol-soluble modulin release and virulence. FASEB J 25:1254-1263. https://doi.org/10.1096/fj.10-175208
26. Kretschmer D, Gleske AK, Rautenberg M, Wang R, Koberle M, Bohn E, Schoneberg T, Rabiet MJ, Boulay F, Klebanoff SJ, van Kessel KA, van Strijp JA, Otto M, Peschel A. 2010. Human formyl peptide receptor 2 senses highly pathogenic Staphylococcus aureus. Cell Host Microbe 7:463-473. https://doi.org/10.1016/j.chom.2010.05.012
27. Bloes DA, Kretschmer D, Peschel A. 2015. Enemy attraction: bacterial agonists for leukocyte chemotaxis receptors. Nat Rev Microbiol 13: 95-104. https://doi.org/10.1038/nrmicro3390
28. Berube BJ, Bubeck Wardenburg J. 2013. Staphylococcus aureus alphatoxin: nearly a century of intrigue. Toxins 5:1140-1166. https://doi.org/ 10.3390/toxins5061140
29. Hsiao HM, Thatcher TH, Levy EP, Fulton RA, Owens KM, Phipps RP, Sime PJ. 2014. Resolvin D1 attenuates polyinosinic-polycytidylic acid-induced inflammatory signaling in human airway epithelial cells via TAK1. J Immunol 193:4980-4987. https://doi.org/10.4049/jimmunol.1400313
30. Fu H, Karlsson J, Bylund J, Movitz C, Karlsson A, Dahlgren C. 2006. Ligand recognition and activation of formyl peptide receptors in neutrophils. J Leukoc Biol 79:247-256. https://doi.org/10.1189/jlb.0905498
31. Niemann S, Ehrhardt C, Medina E, Warnking K, Tuchscherr L, Heitmann V, Ludwig S, Peters G, Loffler B. 2012. Combined action of influenza virus and Staphylococcus aureus Panton-Valentine leukocidin provokes severe lung epithelium damage. J Infect Dis 206:1138-1148. https://doi.org/10.1093/infdis/jis468
32. Bubeck Wardenburg J, Bae T, Otto M, Deleo FR, Schneewind O. 2007. Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat Med 13:1405-1406. https://doi.org/10.1038/nm1207-1405
33. Gillet Y, Issartel B, Vanhems P, Fournet JC, Lina G, Bes M, Vandenesch F, Piemont Y, Brousse N, Floret D, Etienne J. 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. https://doi.org/10.1016/S0140-6736(02)07877-7
34. Genestier AL, Michallet MC, Prevost G, Bellot G, Chalabreysse L, Peyrol S, Thivolet F, Etienne J, Lina G, Vallette FM, Vandenesch F, Genestier L. 2005 Staphylococcus aureus Panton-Valentine leukocidin directly targets mitochondria and induces Bax-independent apoptosis of human neutrophils. J Clin Invest 115:3117-3127. https://doi.org/10.1172/ JCI22684
35. Spaan AN, Henry T, van Rooijen WJ, Perret M, Badiou C, Aerts PC, Kemmink J, de Haas CJ, van Kessel KP, Vandenesch F, Lina G, van Strijp JA. 2013. The staphylococcal toxin Panton-Valentine leukocidin targets human C5a receptors. Cell Host Microbe 13:584-594. https://doi.org/10.1016/j.chom.2013.04.006
36. Sharma-Kuinkel BK, Ahn SH, Rude TH, Zhang Y, Tong SY, Ruffin F, Genter FC, Braughton KR, Deleo FR, Barriere SL, Fowler VG, Jr. 2012. Presence of genes encoding Panton-Valentine leukocidin is not the primary determinant of outcome in patients with hospital-acquired pneumonia due to Staphylococcus aureus. J Clin Microbiol 50:848-856. https://doi.org/10.1128/JCM.06219-11
37. Kobayashi SD, Olsen RJ, LaCasse RA, Safronetz D, Ashraf M, Porter AR, Braughton KR, Feldmann F, Clifton DR, Kash JC, Bailey JR, Gardner DJ, Otto M, Brining DL, Kreiswirth BN, Taubenberger JK, Parnell MJ, Feldmann H, Musser JM, DeLeo FR. 2013. Seasonal H3N2 influenza A virus fails to enhance Staphylococcus aureus co-infection in a non-human primate respiratory tract infection model. Virulence 4:707-715. https:// doi.org/10.4161/viru.26572
38. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC, Qui PT, Cam BV, Ha DQ, Guan Y, Peiris JSM, Chinh NT, Hien TT, Farrar J. 2006. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12:1203-1207. https://doi.org/10.1038/nm1477
39. Sibille Y, Marchandise FX. 1993. Pulmonary immune cells in health and disease: polymorphonuclear neutrophils. Eur Respir J 6:1529-1543
40. Chatterjee SS, Joo HS, Duong AC, Dieringer TD, Tan VY, Song Y, Fischer ER, Cheung GY, Li M, Otto M. 2013. Essential Staphylococcus aureus toxin export system. Nat Med 19:364-367. https://doi.org/10.1038/nm.3047
41. Bloes DA, Otto M, Peschel A, Kretschmer D. 2012. Enterococcus faecium stimulates human neutrophils via the formyl-peptide receptor 2. PLoS One 7:e39910. https://doi.org/10.1371/journal.pone.0039910