Autophagy mediates tolerance to staphylococcus aureus alpha-toxin

Cell Host and Microbe

Volumn 17, Issue 4, 2015, Pages 429-440

  Maurer, Katie ^a   Reyes Robles, Tamara ^a   Alonzo, Francis ^b   Durbin, Joan ^c   Torres, Victor J ^a   Cadwell, Ken ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOYOLA UNIVERSITY CHICAGO   (United States)

^c RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOST FACTOR; STAPHYLOCOCCUS ALPHA TOXIN; VIRULENCE FACTOR; ATG16L1 PROTEIN, MOUSE; BACTERIAL TOXIN; CARRIER PROTEIN; HEMOLYSIN; STAPHYLOCOCCAL ALPHA-TOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGY; BACTERIAL LOAD; BACTERIAL STRAIN; CONTROLLED STUDY; DENDRITIC CELL; ENDOTHELIUM CELL; INFECTION SENSITIVITY; LIMIT OF DETECTION; LUNG INFECTION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PNEUMONIA; PRIORITY JOURNAL; SEPSIS; SURVIVAL; ANIMAL; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; KNOCKOUT MOUSE; MICROBIOLOGY; STAPHYLOCOCCAL PNEUMONIA; SURVIVAL ANALYSIS;

METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MUS; STAPHYLOCOCCUS AUREUS;

ANIMALS; AUTOPHAGY; BACTERIAL TOXINS; CARRIER PROTEINS; HEMOLYSIN PROTEINS; IMMUNE TOLERANCE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICE, KNOCKOUT; PNEUMONIA, STAPHYLOCOCCAL; SEPSIS; SURVIVAL ANALYSIS;

EID: 84926656919     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2015.03.001     Document Type: Article

References (50)

1. F. Alonzo 3rd, and V.J. Torres The bicomponent pore-forming leucocidins of Staphylococcus aureus Microbiol. Mol. Biol. Rev. 78 2014 199 230
2. J.S. Ayres, N.J. Trinidad, and R.E. Vance Lethal inflammasome activation by a multidrug-resistant pathobiont upon antibiotic disruption of the microbiota Nat. Med. 18 2012 799 806
3. R.E. Becker, B.J. Berube, G.R. Sampedro, A.C. DeDent, and J. Bubeck Wardenburg Tissue-specific patterning of host innate immune responses by Staphylococcus aureus α-toxin J. Innate Immun. 6 2014 619 631
4. B.J. Berube, and J. Bubeck Wardenburg Staphylococcus aureus α-toxin: nearly a century of intrigue Toxins (Basel) 5 2013 1140 1166
5. A. Bessede, M. Gargaro, M.T. Pallotta, D. Matino, G. Servillo, C. Brunacci, S. Bicciato, E.M. Mazza, A. Macchiarulo, and C. Vacca Aryl hydrocarbon receptor control of a disease tolerance defence pathway Nature 511 2014 184 190
6. J. Bubeck Wardenburg, T. Bae, M. Otto, F.R. Deleo, and O. Schneewind Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia Nat. Med. 13 2007 1405 1406
7. J. Bubeck Wardenburg, R.J. Patel, and O. Schneewind Surface proteins and exotoxins are required for the pathogenesis of Staphylococcus aureus pneumonia Infect. Immun. 75 2007 1040 1044
8. K. Cadwell, J.Y. Liu, S.L. Brown, H. Miyoshi, J. Loh, J.K. Lennerz, C. Kishi, W. Kc, J.A. Carrero, and S. Hunt A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells Nature 456 2008 259 263
9. G.M. Cann, C. Guignabert, L. Ying, N. Deshpande, J.M. Bekker, L. Wang, B. Zhou, and M. Rabinovitch Developmental expression of LC3alpha and beta: absence of fibronectin or autophagy phenotype in LC3beta knockout mice Dev. Dyn. 237 2008 187 195
10. A. Ferreira, I. Marguti, I. Bechmann, V. Jeney, A. Chora, N.R. Palha, S. Rebelo, A. Henri, Y. Beuzard, and M.P. Soares Sickle hemoglobin confers tolerance to Plasmodium infection Cell 145 2011 398 409
11. N. Figueiredo, A. Chora, H. Raquel, N. Pejanovic, P. Pereira, B. Hartleben, A. Neves-Costa, C. Moita, D. Pedroso, and A. Pinto Anthracyclines induce DNA damage response-mediated protection against severe sepsis Immunity 39 2013 874 884
12. L.C. Gomes, and I. Dikic Autophagy in antimicrobial immunity Mol. Cell 54 2014 224 233
13. B.E. Gonzalez, A.M. Rueda, S.A. Shelburne 3rd, D.M. Musher, R.J. Hamill, and K.G. Hulten Community-associated strains of methicillin-resistant Staphylococccus aureus as the cause of healthcare-associated infection Infect. Control Hosp. Epidemiol. 27 2006 1051 1056
14. J.C. Hageman, T.M. Uyeki, J.S. Francis, D.B. Jernigan, J.G. Wheeler, C.B. Bridges, S.J. Barenkamp, D.M. Sievert, A. Srinivasan, and M.C. Doherty Severe community-acquired pneumonia due to Staphylococcus aureus, 2003-04 influenza season Emerg. Infect. Dis. 12 2006 894 899
15. C. He, Y. Wei, K. Sun, B. Li, X. Dong, Z. Zou, Y. Liu, L.N. Kinch, S. Khan, and S. Sinha Beclin 2 functions in autophagy, degradation of G protein-coupled receptors, and metabolism Cell 154 2013 1085 1099
16. V.M. Hubbard-Lucey, Y. Shono, K. Maurer, M.L. West, N.V. Singer, C.G. Ziegler, C. Lezcano, A.C. Motta, K. Schmid, and S.M. Levi Autophagy gene Atg16L1 prevents lethal T cell alloreactivity mediated by dendritic cells Immunity 41 2014 579 591
17. I. Inoshima, N. Inoshima, G.A. Wilke, M.E. Powers, K.M. Frank, Y. Wang, and J. Bubeck Wardenburg A Staphylococcus aureus pore-forming toxin subverts the activity of ADAM10 to cause lethal infection in mice Nat. Med. 17 2011 1310 1314
18. J.S. Ju, S.E. Miller, E. Jackson, K. Cadwell, D. Piwnica-Worms, and C.C. Weihl Quantitation of selective autophagic protein aggregate degradation in vitro and in vivo using luciferase reporters Autophagy 5 2009 511 519
19. A.D. Kennedy, J. Bubeck Wardenburg, D.J. Gardner, D. Long, A.R. Whitney, K.R. Braughton, O. Schneewind, and F.R. DeLeo Targeting of alpha-hemolysin by active or passive immunization decreases severity of USA300 skin infection in a mouse model J. Infect. Dis. 202 2010 1050 1058
20. R.M. Klevens, M.A. Morrison, J. Nadle, S. Petit, K. Gershman, S. Ray, L.H. Harrison, R. Lynfield, G. Dumyati, J.M. Townes Active Bacterial Core surveillance (ABCs) MRSA Investigators Invasive methicillin-resistant Staphylococcus aureus infections in the United States JAMA 298 2007 1763 1771
21. K.G. Lassen, P. Kuballa, K.L. Conway, K.K. Patel, C.E. Becker, J.M. Peloquin, E.J. Villablanca, J.M. Norman, T.C. Liu, and R.J. Heath Atg16L1 T300A variant decreases selective autophagy resulting in altered cytokine signaling and decreased antibacterial defense Proc. Natl. Acad. Sci. USA 111 2014 7741 7746
22. B. Levine, and G. Kroemer Autophagy in the pathogenesis of disease Cell 132 2008 27 42
23. A.M. Marchiando, D. Ramanan, Y. Ding, L.E. Gomez, V.M. Hubbard-Lucey, K. Maurer, C. Wang, J.W. Ziel, N. van Rooijen, and G. Nuñez A deficiency in the autophagy gene Atg16L1 enhances resistance to enteric bacterial infection Cell Host Microbe 14 2013 216 224
24. R. Mathew, S. Khor, S.R. Hackett, J.D. Rabinowitz, D.H. Perlman, and E. White Functional role of autophagy-mediated proteome remodeling in cell survival signaling and innate immunity Mol. Cell 55 2014 916 930
25. Q. McAfee, Z. Zhang, A. Samanta, S.M. Levi, X.H. Ma, S. Piao, J.P. Lynch, T. Uehara, A.R. Sepulveda, and L.E. Davis Autophagy inhibitor Lys05 has single-agent antitumor activity and reproduces the phenotype of a genetic autophagy deficiency Proc. Natl. Acad. Sci. USA 109 2012 8253 8258
26. R. Medzhitov, D.S. Schneider, and M.P. Soares Disease tolerance as a defense strategy Science 335 2012 936 941
27. M.B. Mestre, and M.I. Colombo cAMP and EPAC are key players in the regulation of the signal transduction pathway involved in the α-hemolysin autophagic response PLoS Pathog. 8 2012 e1002664
28. M.B. Mestre, C.M. Fader, C. Sola, and M.I. Colombo Alpha-hemolysin is required for the activation of the autophagic pathway in Staphylococcus aureus-infected cells Autophagy 6 2010 110 125
29. G.R. Nimmo USA300 abroad: global spread of a virulent strain of community-associated methicillin-resistant Staphylococcus aureus Clin. Microbiol. Infect. 18 2012 725 734
30. R.P. Novick, and E. Geisinger Quorum sensing in staphylococci Annu. Rev. Genet. 42 2008 541 564
31. M. O'Reilly, J.C. de Azavedo, S. Kennedy, and T.J. Foster Inactivation of the alpha-haemolysin gene of Staphylococcus aureus 8325-4 by site-directed mutagenesis and studies on the expression of its haemolysins Microb. Pathog. 1 1986 125 138
32. A. Orvedahl, S. MacPherson, R. Sumpter Jr., Z. Tallóczy, Z. Zou, and B. Levine Autophagy protects against Sindbis virus infection of the central nervous system Cell Host Microbe 7 2010 115 127
33. A. Pamplona, A. Ferreira, J. Balla, V. Jeney, G. Balla, S. Epiphanio, A. Chora, C.D. Rodrigues, I.P. Gregoire, and M. Cunha-Rodrigues Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria Nat. Med. 13 2007 703 710
34. T.R. Pasquale, B. Jabrocki, S.J. Salstrom, T.L. Wiemken, P. Peyrani, N.Z. Haque, E.G. Scerpella, K.D. Ford, M.J. Zervos, J.A. Ramirez, T.M. File Jr. IMPACT-HAP Study Group Emergence of methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of late-onset nosocomial pneumonia in intensive care patients in the USA Int. J. Infect. Dis. 17 2013 e398 e403
35. M.E. Powers, H.K. Kim, Y. Wang, and J. Bubeck Wardenburg ADAM10 mediates vascular injury induced by Staphylococcus aureus α-hemolysin J. Infect. Dis. 206 2012 352 356
36. L. Råberg, D. Sim, and A.F. Read Disentangling genetic variation for resistance and tolerance to infectious diseases in animals Science 318 2007 812 814
37. L. Råberg, A.L. Graham, and A.F. Read Decomposing health: tolerance and resistance to parasites in animals Philos. Trans. R. Soc. Lond. B Biol. Sci. 364 2009 37 49
38. D. Ramanan, M.S. Tang, R. Bowcutt, P. Loke, and K. Cadwell Bacterial sensor Nod2 prevents inflammation of the small intestine by restricting the expansion of the commensal Bacteroides vulgatus Immunity 41 2014 311 324
39. T. Reyes-Robles, F. Alonzo 3rd, L. Kozhaya, D.B. Lacy, D. Unutmaz, and V.J. Torres Staphylococcus aureus leukotoxin ED targets the chemokine receptors CXCR1 and CXCR2 to kill leukocytes and promote infection Cell Host Microbe 14 2013 453 459
40. C.E. Richardson, T. Kooistra, and D.H. Kim An essential role for XBP-1 in host protection against immune activation in C. elegans Nature 463 2010 1092 1095
41. K.A. Rodvold, and K.W. McConeghy Methicillin-resistant Staphylococcus aureus therapy: past, present, and future Clin. Infect. Dis. 58 1 2014 S20 S27
42. T. Saitoh, N. Fujita, M.H. Jang, S. Uematsu, B.G. Yang, T. Satoh, H. Omori, T. Noda, N. Yamamoto, and M. Komatsu Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production Nature 456 2008 264 268
43. G.R. Sampedro, A.C. DeDent, R.E. Becker, B.J. Berube, M.J. Gebhardt, H. Cao, and J. Bubeck Wardenburg Targeting Staphylococcus aureus α-toxin as a novel approach to reduce severity of recurrent skin and soft-tissue infections J. Infect. Dis. 210 2014 1012 1018
44. A. Schnaith, H. Kashkar, S.A. Leggio, K. Addicks, M. Krönke, and O. Krut Staphylococcus aureus subvert autophagy for induction of caspase-independent host cell death J. Biol. Chem. 282 2007 2695 2706
45. D.S. Schneider, and J.S. Ayres Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases Nat. Rev. Immunol. 8 2008 889 895
46. M.E. Stryjewski, and G.R. Corey Methicillin-resistant Staphylococcus aureus: an evolving pathogen Clin. Infect. Dis. 58 1 2014 S10 S19
47. E. Taillebourg, D.S. Schneider, and M.O. Fauvarque The Drosophila deubiquitinating enzyme dUSP36 acts in the hemocytes for tolerance to Listeria monocytogenes infections J. Innate Immun. 6 2014 632 638
48. F. Vandenesch, G. Lina, and T. Henry Staphylococcus aureus hemolysins, bi-component leukocidins, and cytolytic peptides: a redundant arsenal of membrane-damaging virulence factors? Front Cell Infect Microbiol 2 2012 12
49. O. Visvikis, N. Ihuegbu, S.A. Labed, L.G. Luhachack, A.M. Alves, A.C. Wollenberg, L.M. Stuart, G.D. Stormo, and J.E. Irazoqui Innate host defense requires TFEB-mediated transcription of cytoprotective and antimicrobial genes Immunity 40 2014 896 909
50. C. Wang, G.R. Mendonsa, J.W. Symington, Q. Zhang, K. Cadwell, H.W. Virgin, and I.U. Mysorekar Atg16L1 deficiency confers protection from uropathogenic Escherichia coli infection in vivo Proc. Natl. Acad. Sci. USA 109 2012 11008 11013