Modelling staphylococcal pneumonia in a human 3D lung tissue model system delineates toxin-mediated pathology

DMM Disease Models and Mechanisms

Volumn 8, Issue 11, 2015, Pages 1413-1425

  Shambat, Srikanth Mairpady ^a   Chen, Puran ^a   Hoang, Anh Thu Nguyen ^a   Bergsten, Helena ^a   Vandenesch, Francois ^b,c   Siemens, Nikolai ^a   Lina, Gerard ^b,c   Monk, Ian R ^d   Foster, Timothy J ^d   Arakere, Gayathri ^e   Svensson, Mattias ^a   Norrby Teglund, Anna ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^c HOSPICES CIVILS DE LYON   (France)

^d TRINITY COLLEGE DUBLIN   (Ireland)

^e INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

3D lung tissue model; Pneumonia; Staphylococcus aureus

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN G; INTERLEUKIN 8; PANTON VALENTINE LEUKOCIDIN; STAPHYLOCOCCUS ALPHA TOXIN; UVOMORULIN; AUTACOID; BACTERIAL TOXIN; EXOTOXIN; HEMOLYSIN; IMMUNOGLOBULIN; IMMUNOLOGIC FACTOR; LEUKOCIDIN; PANTON-VALENTINE LEUKOCIDIN; STAPHYLOCOCCAL ALPHA-TOXIN;

ARTICLE; BACTERIAL STRAIN; CELL MIGRATION; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; DISEASE ASSOCIATION; DISEASE SEVERITY; EPITHELIUM CELL; FATALITY; HUMAN; HUMAN TISSUE; INFLAMMATION; LUNG ALVEOLUS EPITHELIUM; LUNG FIBROBLAST; LUNG PARENCHYMA; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN SUSCEPTIBLE STAPHYLOCOCCUS AUREUS; NEUTROPHIL; PLEURA EMPYEMA; PRIORITY JOURNAL; STAPHYLOCOCCAL PNEUMONIA; THREE DIMENSIONAL IMAGING; TISSUE INJURY; TISSUE NECROSIS; CHEMOTAXIS; CLASSIFICATION; COCULTURE; COMPARATIVE STUDY; DRUG EFFECTS; FIBROBLAST; IMMUNOLOGY; LUNG; METABOLISM; MICROBIOLOGY; NECROSIS; NEUTROPHIL CHEMOTAXIS; PATHOGENICITY; PATHOLOGY; PNEUMONIA, STAPHYLOCOCCAL; STAPHYLOCOCCUS AUREUS; TIME FACTOR; TUMOR CELL LINE;

BACTERIAL TOXINS; CELL LINE, TUMOR; CHEMOTAXIS; COCULTURE TECHNIQUES; EMPYEMA, PLEURAL; EPITHELIAL CELLS; EXOTOXINS; FIBROBLASTS; HEMOLYSIN PROTEINS; HUMANS; IMMUNOGLOBULINS, INTRAVENOUS; IMMUNOLOGIC FACTORS; INFLAMMATION MEDIATORS; LEUKOCIDINS; LUNG; NECROSIS; NEUTROPHIL INFILTRATION; PNEUMONIA, STAPHYLOCOCCAL; STAPHYLOCOCCUS AUREUS; TIME FACTORS;

EID: 84946737959     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.021923     Document Type: Article

References (47)

1. Alonzo, F., III and Torres, V. J. (2013). Bacterial survival amidst an immune onslaught: the contribution of the Staphylococcus aureus leukotoxins. PLoS Pathog. 9, e1003143.
2. Alonzo, F., III, Kozhaya, L., Rawlings, S. A., Reyes-Robles, T., DuMont, A. L., Myszka, D. G., Landau, N. R., Unutmaz, D. and Torres, V. J. (2013). CCR5 is a receptor for Staphylococcus aureus leukotoxin ED. Nature 493, 51-55.
3. Badiou, C., Dumitrescu, O., George, N., Forbes, A. R. N., Drougka, E., Chan, K. S., Ramdani-Bouguessa, N., Meugnier, H., Bes, M., Vandenesch, F. Et al. (2010). Rapid detection of Staphylococcus aureus Panton-Valentine leukocidin in clinical specimens by enzyme-linked immunosorbent assay and immunochromatographic tests. J. Clin. Microbiol. 48, 1384-1390.
4. Bartlett, A. H., Foster, T. J., Hayashida, A. and Park, P. W. (2008). Alpha-toxin facilitates the generation of CXC chemokine gradients and stimulates neutrophil homing in Staphylococcus aureus pneumonia. J. Infect. Dis. 198, 1529-1535.
5. Bhakdi, S. and Tranum-Jensen, J. (1991). Alpha-toxin of Staphylococcus aureus. Microbiol. Rev.55, 733-751.
6. Blanco, R., Tristan, A., Ezpeleta, G., Larsen, A. R., Bes, M., Etienne, J., Cisterna, R. and Laurent, F. (2011). Molecular epidemiology of Panton-Valentine leukocidin-positive Staphylococcus aureus in Spain: emergence of the USA300 clone in an autochthonous population. J. Clin. Microbiol. 49, 433-436.
7. Bubeck Wardenburg, J., Bae, T., Otto, M., Deleo, F. R. and Schneewind, O. (2007a). Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat. Med. 13, 1405-1406.
8. Bubeck Wardenburg, J., Patel, R. J. and Schneewind, O. (2007b). Surface proteins and exotoxins are required for the pathogenesis of Staphylococcus aureus pneumonia. Infect. Immun. 75, 1040-1044.
9. Bubeck Wardenburg, J., Palazzolo-Ballance, A. M., Otto, M., Schneewind, O. and DeLeo, F. R. (2008). Panton-Valentine leukocidin is not a virulence determinant in murine models of community-associated methicillin-resistant Staphylococcus aureus disease. J. Infect. Dis. 198, 1166-1170.
10. Diep, B. A., Chan, L., Tattevin, P., Kajikawa, O., Martin, T. R., Basuino, L., Mai, T. T., Marbach, H., Braughton, K. R., Whitney, A. R. Et al. (2010). Polymorphonuclear leukocytes mediate Staphylococcus aureus Panton-Valentine leukocidin-induced lung inflammation and injury. Proc. Natl. Acad. Sci. USA 107, 5587-5592.
11. Diep, B. A., Afasizheva, A., Le, H. N., Kajikawa, O., Matute-Bello, G., Tkaczyk, C., Sellman, B., Badiou, C., Lina, G. and Chambers, H. F. (2013). Effects of linezolid on suppressing in vivo production of staphylococcal toxins and improving survival outcomes in a rabbit model of methicillin-resistant Staphylococcus aureus necrotizing pneumonia. J. Infect. Dis. 208, 75-82.
12. DuMont, A. L. and Torres, V. J. (2014). Cell targeting by the Staphylococcus aureus pore-forming toxins: it's not just about lipids. Trends Microbiol. 22, 21-27.
13. DuMont,A.L.,Yoong,P.,Surewaard,B.G. J.,Benson,M.A., Nijland, R., vanStrijp, J. A. G.andTorres,V. J. (2013).Staphylococcus aureus elaborates leukocidinABto mediate escape from within human neutrophils. Infect. Immun. 81, 1830-1841.
14. Escotte, S., Al Alam, D., Le Naour, R., Puchelle, E., Guenounou, M. and Gangloff, S. C. (2006). T cell chemotaxis and chemokine release after Staphylococcus aureus interaction with polarized airway epithelium. Am. J. Respir. Cell Mol. Biol. 34, 348-354.
15. Farag, N., Mahran, L., Abou-Aisha, K. and El-Azizi, M. (2013). Assessment of the efficacy of polyclonal intravenous immunoglobulin G (IVIG) against the infectivity of clinical isolates of methicillin-resistant Staphylococcus aureus (MRSA) in vitro and in vivo. Eur. J. Clin. Microbiol. Infect. Dis. 32, 1149-1160.
16. Francis, J. S., Doherty, M. C., Lopatin, U., Johnston, C. P., Sinha, G., Ross, T., Cai, M., Hansel, N. N., Perl, T., Ticehurst, J. R. Et al. (2005). Severe communityonset pneumonia in healthy adults caused by methicillin-resistant Staphylococcus aureus carrying the Panton-Valentine leukocidin genes. Clin. Infect. Dis. 40, 100-107.
17. Gauduchon, V., Cozon, G., Vandenesch, F., Genestier, A.-L., Eyssade, N., Peyrol, S., Etienne, J. and Lina, G. (2004). Neutralization of Staphylococcus aureus Panton Valentine leukocidin by intravenous immunoglobulin in vitro. J. Infect. Dis. 189, 346-353.
18. Gillet, Y., Issartel, B., Vanhems, P., Fournet, J.-C., Lina, G., Bes, M., Vandenesch, F., Piemont, Y., Brousse, N., Floret, D. 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.
19. Gillet, Y., Vanhems, P., Lina, G., Bes, M., Vandenesch, F., Floret, D. and Etienne, J. (2007). Factors predicting mortality in necrotizing community-acquired pneumonia caused by Staphylococcus aureus containing Panton-Valentine leukocidin. Clin. Infect. Dis. 45, 315-321.
20. Heijink, I. H., Brandenburg, S. M., Noordhoek, J. A., Postma, D. S., Slebos, D.-J. and van Oosterhout, A. J. M. (2010). Characterisation of cell adhesion in airway epithelial cell types using electric cell-substrate impedance sensing. Eur. Respir. J .35, 894-903.
21. Heilbronner, S., Monk, I. R. and Foster, T. J. (2013). The phage integrase vector pIPI03 allows RecA-independent, site-specific labelling of Staphylococcus lugdunensis strains. Plasmid 70, 377-384.
22. Hermann, I., Ráth, S., Ziesemer, S., Volksdorf, T., Dress, R. J., Gutjahr, M., Müller, C., Beule, A. G. and Hildebrandt, J.-P. (2015). Staphylococcus aureus hemolysin A disrupts cell-matrix adhesions in human airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 52, 14-24.
23. Inoshima, I., Inoshima, N., Wilke, G. A., Powers, M. E., Frank, K. M., Wang, Y. and BubeckWardenburg, J. (2011). A Staphylococcus aureus pore-forming toxin subverts the activity of ADAM10 to cause lethal infection in mice. Nat. Med. 17, 1310-1314.
24. Johansson, L., Snáll, J., Sendi, P., Linnér, A., Thulin, P., Linder, A., Treutiger, C.-J.andNorrby-Teglund, A. (2014). HMGB1 in severe soft tissue infections caused by Streptococcus pyogenes. Front. Cell. Infect. Microbiol. 4, 4.
25. Labandeira-Rey, M., Couzon, F., Boisset, S., Brown, E. L., Bes, M., Benito, Y., Barbu, E. M., Vazquez, V., Hook, M., Etienne, J. Et al. (2007). Staphylococcus aureus Panton-Valentine leukocidin causes necrotizing pneumonia. Science 315, 1130-1133.
26. Li, M., Cheung, G. Y. C., Hu, J., Wang, D., Joo, H.-S., DeLeo, F. R. and Otto, M. (2010). Comparative analysis of virulence and toxin expression of global community-associated methicillin-resistant Staphylococcus aureus strains. J. Infect. Dis. 202, 1866-1876.
27. Löffler, B., Hussain, M., Grundmeier, M., Brück, M., Holzinger, D., Varga, G., Roth, J., Kahl, B. C., Proctor, R. A. and Peters, G. (2010). Staphylococcus aureus panton-valentine leukocidin is a very potent cytotoxic factor for human neutrophils. PLoS Pathog. 6, e1000715.
28. Mairpady Shambat, S., Haggar, A., Vandenesch, F., Lina, G., van Wamel, W. J., Arakere, G., Svensson, M. and Norrby-Teglund, A. (2014). Levels of alphatoxin correlate with distinct phenotypic response profiles of blood mononuclear cells and with agr background of community-associated Staphylococcus aureus isolates. PLoS ONE 9, e106107.
29. Monk, I. R., Shah, I. M., Xu, M., Tan, M.-W.andFoster, T. J. (2012). Transforming the untransformable: application of direct transformation to manipulate genetically Staphylococcus aureus and Staphylococcus epidermidis. mBio 3, e00277-11.
30. Nguyen Hoang, A. T., Chen, P., Juarez, J., Sachamitr, P., Billing, B., Bosnjak, L., Dahlen, B., Coles, M. and Svensson, M. (2012). Dendritic cell functional properties in a three-dimensional tissue model of human lung mucosa. Am. J. Physiol. Lung Cell.Mol. Physiol. 302, L226-L237.
31. Nguyen Hoang, A. T., Chen, P., Bjornfot, S., Hogstrand, K., Lock, J. G., Grandien, A., Coles, M. and Svensson, M. (2014). Technical advance: liveimaging analysis of human dendritic cell migrating behavior under the influence of immune-stimulating reagents in an organotypic model of lung. J. Leukoc. Biol. 96, 481-489.
32. Niemann, S., Ehrhardt, C., Medina, E.,Warnking, K., Tuchscherr, L., Heitmann, V., Ludwig, S., Peters, G. and 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.
33. Olsen, R. J., Kobayashi, S. D., Ayeras, A. A., Ashraf, M., Graves, S. F., Ragasa, W., Humbird, T., Greaver, J. L., Cantu, C., Swain, J. L. Et al. (2010). Lack of a major role of Staphylococcus aureus Panton-Valentine leukocidin in lower respiratory tract infection in nonhuman primates. Am. J. Pathol. 176, 1346-1354.
34. Parasa, V. R., Rahman, M. J., Ngyuen Hoang, A. T., Svensson, M., Brighenti, S. and Lerm, M. (2014). Modeling Mycobacterium tuberculosis early granuloma formation in experimental human lung tissue. Dis. Model. Mech. 7, 281-288.
35. Perret, M., Badiou, C., Lina, G., Burbaud, S., Benito, Y., Bes, M., Cottin, V., Couzon, F., Juruj, C., Dauwalder, O. Et al. (2012). Cross-talk between Staphylococcus aureus leukocidins-intoxicated macrophages and lung epithelial cells triggers chemokine secretion in an inflammasome-dependent manner. Cell. Microbiol. 14, 1019-1036.
36. Räth, S., Ziesemer, S., Witte, A., Konkel, A., Müller, C., Hildebrandt, P., Völker, U. and Hildebrandt, J.-P. (2013). S. aureus haemolysin A-induced IL-8 and IL-6 release from human airway epithelial cells is mediated by activation of p38-and Erk-MAP kinases and additional, cell type-specific signalling mechanisms. Cell. Microbiol. 15, 1253-1265.
37. Rose, H. R., Holzman, R. S., Altman, D. R., Smyth, D. S., Wasserman, G. A., Kafer, J. M., Wible, M., Mendes, R. E., Torres, V. J. and Shopsin, B. (2015). Cytotoxic virulence predicts mortality in nosocomial pneumonia due to methicillinresistant Staphylococcus aureus. J. Infect. Dis. 211, 1862-1874.
38. Rouzic, N., Janvier, F., Libert, N., Javouhey, E., Lina, G., Nizou, J. Y., Pasquier, P., Stamm, D., Brinquin, L., Pelletier, C. Et al. (2010). Prompt and successful toxin-targeting treatment of three patients with necrotizing pneumonia due to Staphylococcus aureus strains carrying the Panton-Valentine leukocidin genes. J. Clin. Microbiol. 48, 1952-1955.
39. Shambat, S., Nadig, S., Prabhakara, S., Bes, M., Etienne, J. and Arakere, G. (2012). Clonal complexes and virulence factors of Staphylococcus aureus from several cities in India. BMC Microbiol. 12, 64.
40. Spaan, A. N., Henry, T., van Rooijen,W. J. M., Perret, M., Badiou, C., Aerts, P. C., Kemmink, J., de Haas, C. J. C., van Kessel, K. P. M., Vandenesch, F. Et al. (2013). The staphylococcal toxin Panton-Valentine Leukocidin targets human C5a receptors. Cell Host Microbe 13, 584-594.
41. Surewaard, B. G. J., Nijland, R., Spaan, A. N., Kruijtzer, J. A.W., de Haas, C. J. C. and van Strijp, J. A. G. (2012). Inactivation of staphylococcal phenol soluble modulins by serum lipoprotein particles. PLoS Pathog. 8, e1002606.
42. Valeva, A., Walev, I., Pinkernell, M., Walker, B., Bayley, H., Palmer, M. and Bhakdi, S. (1997). Transmembrane beta-barrel of staphylococcal alpha-toxin forms in sensitive but not in resistant cells. Proc. Natl. Acad. Sci. USA 94, 11607-11611.
43. VanWetering, S., Mannesse-Lazeroms, S. P., Dijkman, J. H. and Hiemstra, P. S. (1997). Effect of neutrophil serine proteinases and defensins on lung epithelial cells: modulation of cytotoxicity and IL-8 production. J. Leukoc. Biol. 62, 217-226.
44. Vandenesch, F., Lina, G. and Henry, T. (2012). Staphylococcus aureus hemolysins, bi-component leukocidins, and cytolytic peptides: a redundant arsenal of membrane-damaging virulence factors? Front. Cell. Infect. Microbiol. 2, 12.
45. Voyich, J. M., Braughton, K. R., Sturdevant, D. E., Whitney, A. R., Said-Salim, B., Porcella, S. F., Long, R. D., Dorward, D. W., Gardner, D. J., Kreiswirth, B. N. Et al. (2005). Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J. Immunol. 175, 3907-3919.
46. Voyich, J. M., Otto, M., Mathema, B., Braughton, K. R., Whitney, A. R.,Welty, D., Long, R. D., Dorward, D. W., Gardner, D. J., Lina, G. Et al. (2006). Is Panton-Valentine leukocidin the major virulence determinant in community-associated methicillin-resistant Staphylococcus aureus disease? J. Infect. Dis. 194, 1761-1770.
47. Wilke, G. A. and BubeckWardenburg, J. (2010). Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus alpha-hemolysin-mediated cellular injury. Proc. Natl. Acad. Sci. USA 107, 13473-13478.