Actin polymerization as a key innate immune effector mechanism to control Salmonella infection

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 49, 2014, Pages 17588-17593

  Man, Si Ming ^a   Ekpenyong, Andrew ^a,b   Tourlomousis, Panagiotis ^a   Achouri, Sarra ^a   Cammarota, Eugenia ^a   Hughes, Katherine ^a   Rizzo, Alessandro ^a   Ng, Gilbert ^a,b   Wright, John A ^a   Cicuta, Pietro ^a   Guck, Jochen R ^a,b   Bryant, Clare E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

ASC; Caspase 1; Cytoskeleton; Innate immunity; ROS

Indexed keywords

CASPASE 11; F ACTIN; HYDROGEN PEROXIDE; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PROTEIN NLRC4; UNCLASSIFIED DRUG; ACTIN; APOPTOSIS REGULATORY PROTEIN; CALCIUM BINDING PROTEIN; IPAF PROTEIN, MOUSE; REACTIVE OXYGEN METABOLITE;

ACTIN POLYMERIZATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL LOAD; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; BONE MARROW DERIVED MACROPHAGE; CELL MIGRATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOSKELETON; DISEASE CONTROL; EPITHELIUM CELL; INNATE IMMUNITY; MACROPHAGE MIGRATION; MICROTUBULE ASSEMBLY; MOLECULE; MOUSE; NONHUMAN; REGULATORY MECHANISM; RIGIDITY; SALMONELLOSIS; SINGLE CELL ANALYSIS; ACTIN FILAMENT; ANIMAL; BONE MARROW CELL; CHEMISTRY; CYTOLOGY; IMMUNOLOGY; INFLAMMATION; MACROPHAGE; METABOLISM; MICROBIOLOGY; NEUTROPHIL; POLYMERIZATION; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; TRANSGENIC MOUSE;

SALMONELLA;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; APOPTOSIS REGULATORY PROTEINS; BONE MARROW CELLS; CALCIUM-BINDING PROTEINS; CASPASE 1; CYTOSKELETON; HYDROGEN PEROXIDE; IMMUNITY, INNATE; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-1BETA; MACROPHAGES; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; NEUTROPHILS; POLYMERIZATION; REACTIVE OXYGEN SPECIES; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM;

EID: 84916215920     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1419925111     Document Type: Article

References (39)

1. Crump JA, Luby SP, Mintz ED (2004) The global burden of typhoid fever. Bull World Health Organ 82(5):346-353.
2. Aderem A, Underhill DM (1999) Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17:593-623.
3. Mastroeni P, Grant A, Restif O, Maskell D (2009) A dynamic view of the spread and intracellular distribution of Salmonella enterica. Nat Rev Microbiol 7(1):73-80.
4. Fields PI, Swanson RV, Haidaris CG, Heffron F (1986) Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA 83(14):5189-5193.
5. Haraga A, Ohlson MB, Miller SI (2008) Salmonellae interplay with host cells. Nat Rev Microbiol 6(1):53-66.
6. Janeway CA, Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197-216.
7. Tschopp J, Martinon F, Burns K (2003) NALPs: A novel protein family involved in inflammation. Nat Rev Mol Cell Biol 4(2):95-104.
8. Zhao Y, et al. (2011) The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 477(7366):596-600.
9. Kofoed EM, Vance RE (2011) Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 477(7366):592-595.
10. Yang J, Zhao Y, Shi J, Shao F (2013) Human NAIP and mouse NAIP1 recognize bacterial type III secretion needle protein for inflammasome activation. Proc Natl Acad Sci USA 110(35):14408-14413.
11. Rayamajhi M, Zak DE, Chavarria-Smith J, Vance RE, Miao EA (2013) Cutting edge: Mouse NAIP1 detects the type III secretion system needle protein. J Immunol 191(8): 3986-3989.
12. Mariathasan S, et al. (2004) Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430(6996):213-218.
13. Broz P, von Moltke J, Jones JW, Vance RE, Monack DM (2010) Differential requirement for Caspase-1 autoproteolysis in pathogen-induced cell death and cytokine processing. Cell Host Microbe 8(6):471-483.
14. Kayagaki N, et al. (2011) Non-canonical inflammasome activation targets caspase-11. Nature 479(7371):117-121.
15. Broz P, et al. (2012) Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 490(7419):288-291.
16. Gurung P, et al. (2012) Toll or interleukin-1 receptor (TIR) domain-containing adaptor inducing interferon-β (TRIF)-mediated caspase-11 protease production integrates Tolllike receptor 4 (TLR4) protein- and Nlrp3 inflammasome-mediated host defense against enteropathogens. J Biol Chem 287(41):34474-34483.
17. Man SM, et al. (2014) Inflammasome activation causes dual recruitment of NLRC4 and NLRP3 to the same macromolecular complex. Proc Natl Acad Sci USA 111(20): 7403-7408.
18. Miao EA, et al. (2010) Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 11(12):1136-1142.
19. Franchi L, et al. (2012) NLRC4-driven production of IL-1β discriminates between pathogenic and commensal bacteria and promotes host intestinal defense. Nat Immunol 13(5):449-456.
20. Sellin ME, et al. (2014) Epithelium-intrinsic NAIP/NLRC4 inflammasome drives infected enterocyte expulsion to restrict Salmonella replication in the intestinal mucosa. Cell Host Microbe 16(2):237-248.
21. Gog JR, et al. (2012) Dynamics of Salmonella infection of macrophages at the single cell level. J R Soc Interface 9(75):2696-2707.
22. West AP, et al. (2011) TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472(7344):476-480.
23. Hicks SW, Galán JE (2013) Exploitation of eukaryotic subcellular targeting mechanisms by bacterial effectors. Nat Rev Microbiol 11(5):316-326.
24. Brenner SL, Korn ED (1980) The effects of cytochalasins on actin polymerization and actin ATPase provide insights into the mechanism of polymerization. J Biol Chem 255(3):841-844.
25. Brenner SL, Korn ED (1979) Substoichiometric concentrations of cytochalasin D inhibit actin polymerization. Additional evidence for an F-actin treadmill. J Biol Chem 254(20):9982-9985.
26. Poyet JL, et al. (2001) Identification of Ipaf, a human caspase-1-activating protein related to Apaf-1. J Biol Chem 276(30):28309-28313.
27. Proell M, Gerlic M, Mace PD, Reed JC, Riedl SJ (2013) The CARD plays a critical role in ASC foci formation and inflammasome signalling. Biochem J 449(3):613-621.
28. Man SM, et al. (2013) Salmonella infection induces recruitment of Caspase-8 to the inflammasome to modulate IL-1β production. J Immunol 191(10):5239-5246.
29. Guck J, et al. (2001) The optical stretcher: A novel laser tool to micromanipulate cells. Biophys J 81(2):767-784.
30. Lautenschläger F, et al. (2009) The regulatory role of cell mechanics for migration of differentiating myeloid cells. Proc Natl Acad Sci USA 106(37):15696-15701.
31. Guck J, Lautenschläger F, Paschke S, Beil M (2010) Critical review: Cellular mechanobiology and amoeboid migration. Integr Biol (Camb) 2(11-12):575-583.
32. Chen KW, et al. (2014) The neutrophil NLRC4 inflammasome selectively promotes IL-1β maturation without pyroptosis during acute Salmonella challenge. Cell Reports 8(2):570-582.
33. Lamkanfi M, et al. (2008) Targeted peptidecentric proteomics reveals caspase-7 as a substrate of the caspase-1 inflammasomes. Mol Cell Proteomics 7(12):2350-2363.
34. Konradt C, et al. (2011) The Shigella flexneri type three secretion system effector IpgD inhibits T cell migration by manipulating host phosphoinositide metabolism. Cell Host Microbe 9(4):263-272.
35. Salgado-Pabón W, et al. (2013) Shigella impairs T lymphocyte dynamics in vivo. Proc Natl Acad Sci USA 110(12):4458-4463.
36. Willingham SB, et al. (2007) Microbial pathogen-induced necrotic cell death mediated by the inflammasome components CIAS1/cryopyrin/NLRP3 and ASC. Cell Host Microbe 2(3):147-159.
37. Suzuki T, et al. (2007) Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog 3(8):e111.
38. Hautefort I, Proenc¸a MJ, Hinton JC (2003) Single-copy green fluorescent protein gene fusions allow accurate measurement of Salmonella gene expression in vitro and during infection of mammalian cells. Appl Environ Microbiol 69(12):7480-7491.
39. Guck J, et al. (2005) Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys J 88(5):3689-3698.