Inability to sustain intraphagolysosomal killing of Staphylococcus aureus predisposes to bacterial persistence in macrophages

Cellular Microbiology

Volumn 18, Issue 1, 2016, Pages 80-96

  Jubrail, Jamil ^a,b   Morris, Paul ^a,b   Bewley, Martin A ^a,b   Stoneham, Simon ^a,b   Johnston, Simon A ^a,b   Foster, Simon J ^a,b   Peden, Andrew A ^a   Read, Robert C ^c   Marriott, Helen M ^a,b   Dockrell, David H ^a,b,d  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^d SHEFFIELD TEACHING HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Antimicrobial; Immunology; Microbial cell interaction; Staphylococci

Indexed keywords

CASPASE 3; CATHEPSIN D; CYTOCHALASIN D; GAMMA INTERFERON; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ACIDIFICATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; BACTERIAL VIABILITY; CELL MATURATION; CELL MEMBRANE PERMEABILITY; CELL PH; CELL PHAGOCYTOSIS; CELL VIABILITY; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENZYME ACTIVATION; FEMALE; HOST RESISTANCE; INTERNALIZATION; INTRACELLULAR KILLING; LUNG ALVEOLUS MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; PHAGOLYSOSOME; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; ANIMAL; CELL SURVIVAL; DISEASE MODEL; IMMUNOLOGY; MACROPHAGE; MICROBIAL VIABILITY; MICROBIOLOGY; PATHOLOGY; PHAGOCYTOSIS; PHYSIOLOGY; STAPHYLOCOCCAL PNEUMONIA;

ANIMALS; CELL SURVIVAL; DISEASE MODELS, ANIMAL; MACROPHAGES; MICE; MICROBIAL VIABILITY; PHAGOCYTOSIS; PNEUMONIA, STAPHYLOCOCCAL; STAPHYLOCOCCUS AUREUS;

EID: 84940920011     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12485     Document Type: Article

References (73)

1. Aberdein, J.D., Cole, J., Bewley, M.A., Marriott, H.M., and Dockrell, D.H. (2013) Alveolar macrophages in pulmonary host defence the unrecognized role of apoptosis as a mechanism of intracellular bacterial killing. Clin Exp Immunol 174: 193-202.
2. Berger, S.B., Romero, X., Ma, C., Wang, G., Faubion, W.A., Liao, G., et al. (2010) SLAM is a microbial sensor that regulates bacterial phagosome functions in macrophages. Nat Immunol 11: 920-927.
3. Bewley, M.A., Marriott, H.M., Tulone, C., Francis, S.E., Mitchell, T.J., Read, R.C., et al. (2011a) A cardinal role for cathepsin D in co-ordinating the host-mediated apoptosis of macrophages and killing of pneumococci. PLoS Pathog 7: e1001262.
4. Bewley, M.A., Pham, T.K., Marriott, H.M., Noirel, J., Chu, H.P., Ow, S.Y., et al. (2011b) Proteomic evaluation and validation of cathepsin D regulated proteins in macrophages exposed to Streptococcus pneumoniae. Mol Cell Proteomics 10: M111 008193.
5. Bewley, M.A., Naughton, M., Preston, J., Mitchell, A., Holmes, A., Marriott, H.M., et al. (2014) Pneumolysin activates macrophage lysosomal membrane permeabilization and executes apoptosis by distinct mechanisms without membrane pore formation. mBio 5: e01710-01714.
6. Birjandi, S.Z., Ippolito, J.A., Ramadorai, A.K. and Witte, P.L. (2011) Alterations in marginal zone macrophages and marginal zone B cells in old mice. J Immunol 186: 3441-3451.
7. Brown, S.S., and Spudich, J.A. (1979) Cytochalasin inhibits the rate of elongation of actin filament fragments. J Cell Biol 83: 657-662.
8. Bucci, C., Parton, R.G., Mather, I.H., Stunnenberg, H., Simons, K., Hoflack, B., and Zerial, M. (1992) The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70: 715-728.
9. Capony, F., Morisset, M., Barrett, A.J., Capony, J.P., Broquet, P., Vignon, F., et al. (1987) Phosphorylation, glycosylation, and proteolytic activity of the 52-kD estrogen-induced protein secreted by MCF7 cells. J Cell Biol 104: 253-262.
10. Cassatella, M.A., Della Bianca, V., Berton, G., and Rossi, F. (1985) Activation by gamma interferon of human macrophage capability to produce toxic oxygen molecules is accompanied by decreased Km of the superoxide-generating NADPH oxidase. Biochem Biophys Res Commun 132: 908-914.
11. Clement, S., Vaudaux, P., Francois, P., Schrenzel, J., Huggler, E., Kampf, S., et al. (2005) Evidence of an intracellular reservoir in the nasal mucosa of patients with recurrent Staphylococcus aureus rhinosinusitis. J Infect Dis 192: 1023-1028.
12. Daigneault, M., Preston, J.A., Marriott, H.M., Whyte, M.K., and Dockrell, D.H. (2010) The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS One 5: e8668.
13. Das, D., and Bishayi, B. (2010) Contribution of catalase and superoxide dismutase to the intracellular survival of clinical isolates of Staphylococcus aureus in murine macrophages. Indian J Microbiol 50: 375-384.
14. Degnan, B.A., Palmer, J.M., Robson, T., Jones, C.E., Fischer, M., Glanville, M., et al. (1998) Inhibition of human peripheral blood mononuclear cell proliferation by Streptococcus pyogenes cell extract is associated with arginine deiminase activity. Infect Immun 66: 3050-3058.
15. DeLeo, F.R., Allen, L.A., Apicella, M., and Nauseef, W.M. (1999) NADPH oxidase activation and assembly during phagocytosis. J Immunol 163: 6732-6740.
16. DeLoid, G.M., Sulahian, T.H., Imrich, A., and Kobzik, L. (2009) Heterogeneity in macrophage phagocytosis of Staphylococcus aureus strains: high-throughput scanning cytometry-based analysis. PLoS One 4: e6209.
17. Diep, B.A., Gill, S.R., Chang, R.F., Phan, T.H., Chen, J.H., Davidson, M.G., et al. (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367: 731-739.
18. Dockrell, D.H., Lee, M., Lynch, D.H., and Read, R.C. (2001) Immune-mediated phagocytosis and killing of Streptococcus pneumoniae are associated with direct and bystander macrophage apoptosis. J Infect Dis 184: 713-722.
19. Dockrell, D.H., Marriott, H.M., Prince, L.R., Ridger, V.C., Ince, P.G., Hellewell, P.G., and Whyte, M.K. (2003) Alveolar macrophage apoptosis contributes to pneumococcal clearance in a resolving model of pulmonary infection. J Immunol 171: 5380-5388.
20. Flannagan, R.S., Cosio, G., and Grinstein, S. (2009) Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7: 355-366.
21. Fluit, A.C., Jones, M.E., Schmitz, F.J., Acar, J., Gupta, R., and Verhoef, J. (2000) Antimicrobial susceptibility and frequency of occurrence of clinical blood isolates in Europe from the SENTRY antimicrobial surveillance program, 1997 and 1998. Clin Infectious Dis: Off Publ Infectious Dis Soc Am 30: 454-460.
22. Fowler, V.G., Jr., Olsen, M.K., Corey, G.R., Woods, C.W., Cabell, C.H., Reller, L.B., et al. (2003) Clinical identifiers of complicated Staphylococcus aureus bacteremia. Arch Intern Med 163: 2066-2072.
23. Godbold, G.D., Ahn, K., Yeyeodu, S., Lee, L.F., Ting, J.P., and Erickson, A.H. (1998) Biosynthesis and intracellular targeting of the lysosomal aspartic proteinase cathepsin D. Adv Exp Med Biol 436: 153-162.
24. Goldstein, E., Lippert, W., and Warshauer, D. (1974) Pulmonary alveolar macrophage. Defender against bacterial infection of the lung. J Clin Invest 54: 519-528.
25. Gordon, A.H., Hart, P.D., and Young, M.R. (1980) Ammonia inhibits phagosome-lysosome fusion in macrophages. Nature 286: 79-80.
26. Gordon, S.B., Irving, G.R., Lawson, R.A., Lee, M.E., and Read, R.C. (2000) Intracellular trafficking and killing of Streptococcus pneumoniae by human alveolar macrophages are influenced by opsonins. Infect Immun 68: 2286-2293.
27. Green, G.M., and Kass, E.H. (1964) The role of the alveolar macrophage in the clearance of bacteria from the lung. J Exp Med 119: 167-176.
28. Grosz, M., Kolter, J., Paprotka, K., Winkler, A.-C., Schäfer, D., Chatterjee, S.S., et al. (2014) Cytoplasmic replication of Staphylococcus aureus upon phagosomal escape triggered by phenol-soluble modulin α. Cell Microbiol 16: 451-465.
29. Hackam, D.J., Rotstein, O.D., Zhang, W.J., Demaurex, N., Woodside, M., Tsai, O., and Grinstein, S. (1997) Regulation of phagosomal acidification. Differential targeting of Na+/H+ exchangers, Na+/K+-ATPases, and vacuolar-type H+-atpases. J Biol Chem 272: 29810-29820.
30. Hampton, M.B., Kettle, A.J., and Winterbourn, C.C. (1996) Involvement of superoxide and myeloperoxidase in oxygen-dependent killing of Staphylococcus aureus by neutrophils. Infect Immun 64: 3512-3517.
31. Hampton, M.B., Kettle, A.J. and Winterbourn, C.C. (1998) Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92: 3007-3017.
32. Harrison, R.E., Bucci, C., Vieira, O.V., Schroer, T.A. and Grinstein, S. (2003) Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol Cell Biol 23: 6494-6506.
33. Herold, B.C., Immergluck, L.C., Maranan, M.C., Lauderdale, D.S., Gaskin, R.E., Boyle-Vavra, S., et al. (1998) Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. Jama 279: 593-598.
34. Houghton, A.M., Hartzell, W.O., Robbins, C.S., Gomis-Ruth, F.X., and Shapiro, S.D. (2009) Macrophage elastase kills bacteria within murine macrophages. Nature 460: 637-641.
35. Huynh, K.K., Eskelinen, E.L., Scott, C.C., Malevanets, A., Saftig, P., and Grinstein, S. (2007) LAMP proteins are required for fusion of lysosomes with phagosomes. EMBO J 26: 313-324.
36. Jackson, S.H., Gallin, J.I., and Holland, S.M. (1995) The p47phox mouse knock-out model of chronic granulomatous disease. J Exp Med 182: 751-758.
37. Jamur, M.C., and Oliver, C. (2010) Permeabilization of cell membranes. Methods Mol Biol (Clifton, NJ) 588: 63-66.
38. Jonsson, S., Musher, D.M., Chapman, A., Goree, A., and Lawrence, E.C. (1985) Phagocytosis and killing of common bacterial pathogens of the lung by human alveolar macrophages. J Infect Dis 152: 4-13.
39. Koziel, J., Kmiecik, K., Chmiest, D., Maresz, K., Mizgalska, D., Maciag-Gudowska, A., et al. (2013) The role of Mcl-1 in S.aureus-induced cytoprotection of infected macrophages. Mediators Inflamm 2013: 427021.
40. Kubica, M., Guzik, K., Koziel, J., Zarebski, M., Richter, W., Gajkowska, B., et al. (2008) A potential new pathway for Staphylococcus aureus dissemination: the silent survival of S.aureus phagocytosed by human monocyte-derived macrophages. PLoS One 3: e1409.
41. Kubota, K. (2010) Innate IFN-gamma production by subsets of natural killer cells, natural killer T cells and gammadelta T cells in response to dying bacterial-infected macrophages. Scand J Immunol 71: 199-209.
42. Kuronita, T., Eskelinen, E.L., Fujita, H., Saftig, P., Himeno, M., and Tanaka, Y. (2002) A role for the lysosomal membrane protein LGP85 in the biogenesis and maintenance of endosomal and lysosomal morphology. J Cell Sci 115: 4117-4131.
43. 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 Infectious Dis 202: 1866-1876.
44. Liu, G.Y. (2009) Molecular pathogenesis of Staphylococcus aureus infection. Pediatr Res 65: 71R-77R.
45. Marriott, H.M., Ali, F., Read, R.C., Mitchell, T.J., Whyte, M.K., and Dockrell, D.H. (2004) Nitric oxide levels regulate macrophage commitment to apoptosis or necrosis during pneumococcal infection. FASEB J 18: 1126-1128.
46. Marriott, H.M., Bingle, C.D., Read, R.C., Braley, K.E., Kroemer, G., Hellewell, P.G., et al. (2005) Dynamic changes in Mcl-1 expression regulate macrophage viability or commitment to apoptosis during bacterial clearance. J Clin Invest 115: 359-368.
47. Miles, A.A., Misra, S.S. and Irwin, J.O. (1938) The estimation of the bactericidal power of the blood. J Hyg 38: 732-749.
48. Palecanda, A., Paulauskis, J., Al-Mutairi, E., Imrich, A., Qin, G., Suzuki, H., et al. (1999) Role of the scavenger receptor MARCO in alveolar macrophage binding of unopsonized environmental particles. J Exp Med 189: 1497-1506.
49. Pizzolla, A., Hultqvist, M., Nilson, B., Grimm, M.J., Eneljung, T., Jonsson, I.M., et al. (2012) Reactive oxygen species produced by the NADPH oxidase 2 complex in monocytes protect mice from bacterial infections. J Immunol 188: 5003-5011.
50. Reeves, E.P., Lu, H., Jacobs, H.L., Messina, C.G., Bolsover, S., Gabella, G., et al. (2002) Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416: 291-297.
51. Regoli, F., and Winston, G.W. (1999) Quantification of total oxidant scavenging capacity of antioxidants for peroxynitrite, peroxyl radicals, and hydroxyl radicals. Toxicol Appl Pharmacol 156: 96-105.
52. Rehm, S.R., Gross, G.N. and Pierce, A.K. (1980) Early bacterial clearance from murine lungs. Species-dependent phagocyte response. J Clin Invest 66: 194-199.
53. Sasaki, S., Miura, T., Nishikawa, S., Yamada, K., Hirasue, M., and Nakane, A. (1998) Protective role of nitric oxide in Staphylococcus aureus infection in mice. Infect Immun 66: 1017-1022.
54. Schindler, C.A., and Schuhardt, V.T. (1964) Lysostaphin: a new bacteriolytic agent for the Staphylococcus. Proc Natl Acad Sci U S A 51: 414-421.
55. Segal, A.W., Geisow, M., Garcia, R., Harper, A., and Miller, R. (1981) The respiratory burst of phagocytic cells is associated with a rise in vacuolar pH. Nature 290: 406-409.
56. Shay, A.H., Choi, R., Whittaker, K., Salehi, K., Kitchen, C.M., Tashkin, D.P., et al. (2003) Impairment of antimicrobial activity and nitric oxide production in alveolar macrophages from smokers of marijuana and cocaine. J Infect Dis 187: 700-704.
57. Sokolovska, A., Becker, C.E., Ip, W.K., Rathinam, V.A., Brudner, M., Paquette, N., et al. (2013) Activation of caspase-1 by the NLRP3 inflammasome regulates the NADPH oxidase NOX2 to control phagosome function. Nat Immunol 14: 543-553.
58. Stapels, D.A.C., Ramyar, K.X., Ricklin, D., Milder, F.J.J., Bischoff, M., Hermann, M., et al. (2012) Extracellular adherence protein (Eap) of Staphylococcus aureus evades innate immunity by inhibiting complement activation and neutrophil elastase. Immunobiology 217: 1170.
59. Stuart, L.M., Deng, J., Silver, J.M., Takahashi, K., Tseng, A.A., Hennessy, E.J., et al. (2005) Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J Cell Biol 170: 477-485.
60. Thwaites, G.E., Edgeworth, J.D., Gkrania-Klotsas, E., Kirby, A., Tilley, R., Torok, M.E., et al. (2011) Clinical management of Staphylococcus aureus bacteraemia. Lancet Infect Dis 11: 208-222.
61. Tobler, A., Miller, C.W., Johnson, K.R., Selsted, M.E., Rovera, G., and Koeffler, H.P. (1988) Regulation of gene expression of myeloperoxidase during myeloid differentiation. J Cell Physiol 136: 215-225.
62. Totemeyer, S., Sheppard, M., Lloyd, A., Roper, D., Dowson, C., Underhill, D., et al. (2006) IFN-gamma enhances production of nitric oxide from macrophages via a mechanism that depends on nucleotide oligomerization domain-2. J Immunol 176: 4804-4810.
63. Tuchscherr, L., Heitmann, V., Hussain, M., Viemann, D., Roth, J., von Eiff, C., et al. (2010) Staphylococcus aureus small-colony variants are adapted phenotypes for intracellular persistence. J Infect Dis 202: 1031-1040.
64. van Deurs, B., Holm, P.K., and Sandvig, K. (1996) Inhibition of the vacuolar H(+)-ATPase with bafilomycin reduces delivery of internalized molecules from mature multivesicular endosomes to lysosomes in HEp-2 cells. Eur J Cell Biol 69: 343-350.
65. Vesga, O., Groeschel, M.C., Otten, M.F., Brar, D.W., Vann, J.M., and Proctor, R.A. (1996) Staphylococcus aureus small colony variants are induced by the endothelial cell intracellular milieu. J Infect Dis 173: 739-742.
66. von Eiff, C., Becker, K., Metze, D., Lubritz, G., Hockmann, J., Schwarz, T., and Peters, G. (2001) Intracellular persistence of Staphylococcus aureus small-colony variants within keratinocytes: a cause for antibiotic treatment failure in a patient with Darier's disease. Clin Infectious Dis: Off Publ Infectious Dis Soc Am 32: 1643-1647.
67. Wang, J.H., Zhou, Y.J., and He, P. (2010) Staphylococcus aureus induces apoptosis of human monocytic U937 cells via NF-kappaB signaling pathways. Microb Pathog 49: 252-259.
68. Wardman, P. (2007) Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospects. Free Radic Biol Med 43: 995-1022.
69. Webster, S.J., Daigneault, M., Bewley, M.A., Preston, J.A., Marriott, H.M., Walmsley, S.R., et al. (2010) Distinct cell death programs in monocytes regulate innate responses following challenge with common causes of invasive bacterial disease. J Immunol 185: 2968-2979.
70. Wisplinghoff, H., Bischoff, T., Tallent, S.M., Seifert, H., Wenzel, R.P., and Edmond, M.B. (2004) Nosocomial bloodstream infections in US hospitals: analysis of 24179 cases from a prospective nationwide surveillance study. Clin Infectious Dis: Off Publ Infectious Dis Soc Am 39: 309-317.
71. Wolf, A.J., Arruda, A., Reyes, C.N., Kaplan, A.T., Shimada, T., Shimada, K., et al. (2011) Phagosomal degradation increases TLR access to bacterial ligands and enhances macrophage sensitivity to bacteria. J Immunol 187: 6002-6010.
72. Wong, D., Bach, H., Sun, J., Hmama, Z., and Av-Gay, Y. (2011) Mycobacterium tuberculosis protein tyrosine phosphatase (PtpA) excludes host vacuolar-H+-ATPase to inhibit phagosome acidification. Proc Natl Acad Sci U S A 108: 19371-19376.
73. Zarember, K.A., Marshall-Batty, K.R., Cruz, A.R., Chu, J., Fenster, M.E., Shoffner, A.R., et al. (2012) Innate immunity against Granulibacter bethesdensis, an emerging gram-negative bacterial pathogen. Infect Immun 80: 975-981.