Fatty acids regulate stress resistance and virulence factor production for Listeria monocytogenes

Journal of Bacteriology

Volumn 194, Issue 19, 2012, Pages 5274-5284

  Sun, Yvonne ^a   Wilkinson, Brian J ^b   Standiford, Theodore J ^a   Akinbi, Henry T ^c   O'Riordan, Mary X D ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b ILLINOIS STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRANCHED CHAIN AMINO ACID; FATTY ACID; LISTERIOLYSIN O; PEPTIDOGLYCAN; POLYPEPTIDE ANTIBIOTIC AGENT; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL SURVIVAL; CONTROLLED STUDY; FATTY ACID METABOLISM; GENE MUTATION; LISTERIA MONOCYTOGENES; LOW TEMPERATURE; MACROPHAGE; NONHUMAN; PH; PHAGOSOME; PRIORITY JOURNAL; STRESS;

ANIMALS; CELL LINE; FATTY ACIDS; LISTERIA MONOCYTOGENES; MACROPHAGES; MICE; MOLECULAR STRUCTURE; MUTATION; STRESS, PHYSIOLOGICAL; VIRULENCE; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES;

EID: 84868335539     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00045-12     Document Type: Article

References (63)

1. Abachin E, et al. 2002. Formation of D-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Mol. Microbiol. 43: 1-14.
2. Reference deleted
3. Bader MW, et al. 2005. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122:461-472.
4. Balemans W, et al. 2010. Essentiality of FASII pathway for Staphylococcus aureus. Nature 463:E3.
5. Bayer AS, et al. 2000. In vitro resistance of Staphylococcus aureus to thrombin-induced platelet microbicidal protein is associated with alterations in cytoplasmic membrane fluidity. Infect. Immun. 68:3548-3553.
6. Bennett HJ, et al. 2007. Characterization of relA and codY mutants of Listeria monocytogenes: identification of the CodY regulon and its role in virulence. Mol. Microbiol. 63:1453-1467.
7. Bonazzi M, Lecuit M, Cossart P. 2009. Listeria monocytogenes internalin and E-cadherin: from structure to pathogenesis. Cell. Microbiol. 11:693-702.
8. Boneca IG, et al. 2007. A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc. Natl. Acad. Sci. U. S. A. 104:997-1002.
9. Brinster S, et al. 2009. Type II fatty acid synthesis is not a suitable antibiotic target for Gram-positive pathogens. Nature 458:83-86.
10. Camberg JL, et al. 2007. Synergistic stimulation of EpsE ATP hydrolysis by EpsL and acidic phospholipids. EMBO J. 26:19-27.
11. Camejo A, et al. 2009. In vivo transcriptional profiling of Listeria monocytogenes and mutagenesis identify new virulence factors involved in infection. PLoS Pathog. 5:e1000449. doi:10.1371/journal.ppat.1000449.
12. Cardenal-Muñoz E, Ramos-Morales F. 2011. Analysis of the expression, secretion, and translocation of the Salmonella enterica type III secretion system effector SteA. PLoS One 6:e26930. doi:10.1371/journal.pone.0026930.
13. de las Heras A, Cain RJ, Bielecka MK, Vázquez-Boland JA. 2011. Regulation of Listeria virulence: PrfA master and commander. Curr. Opin. Microbiol. 14:118-127.
14. Diogo A, Veríssimo A, Nobre MF, da Costa MS. 1999. Usefulness of fatty acid composition for differentiation of Legionella species. J. Clin. Microbiol. 37:2248-2254.
15. Edgcomb MR, Sirimanne S, Wilkinson BJ, Drouin P, Morse RD. 2000. Electron paramagnetic resonance studies of the membrane fluidity of the food-borne pathogenic psychrotroph Listeria monocytogenes. Biochim. Biophys. Acta Biomembr. 1463:31-42.
16. Edwards RL, Dalebroux ZD, Swanson MS. 2009. Legionella pneumophila couples fatty acid flux to microbial differentiation and virulence. Mol. Microbiol. 71:1190-1204.
17. Evans M, Feola D, Rapp R. 1999. Polymyxin B sulfate and colistin: old antibiotics for emerging multiresistant Gram-negative bacteria. Ann. Pharmacother. 33:960-967.
18. Flannagan RS, Cosio G, Grinstein S. 2009. Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat. Rev. Microbiol. 7:355-366.
19. Fliss I, Emond E, Simard RE, Pandian S. 1991. A rapid and efficient method of lysis of Listeria and other Gram-positive bacteria using mutanolysin. Biotechniques 453:456-457.
20. Gallo R, et al. 1997. Identification of CRAMP, a cathelin-related antimicrobial peptide expressed in the embryonic and adult mouse RID A-8931-2009. J. Biol. Chem. 272:13088-13093.
21. Gantois I, et al. 2006. Butyrate specifically downregulates Salmonella pathogenicity island 1 gene expression. Appl. Environ. Microbiol. 72:946-949.
22. Giles DK, Hankins JV, Guan Z, Trent MS. 2011. Remodeling of the Vibrio cholerae membrane by incorporation of exogenous fatty acids from host and aquatic environments. Mol. Microbiol. 79:716-728.
23. Giotis ES, McDowell DA, Blair IS, Wilkinson BJ. 2007. Role of branched-chain fatty acids in pH stress tolerance in Listeria monocytogenes. Appl. Environ. Microbiol. 73:997-1001.
24. Heath R, White S, Rock C. 2002. Inhibitors of fatty acid synthesis as antimicrobial chemotherapeutics. Appl. Microbiol. Biotechnol. 58:695-703.
25. Herold S, Paton JC, Srimanote P, Paton AW. 2009. Differential effects of short-chain fatty acids and iron on expression of iha in Shiga-toxigenic Escherichia coli. Microbiology 155:3554-3563.
26. Johansen C, Gill T, Gram L. 1995. Antibacterial effect of protamine assayed by impedimetry. J. Appl. Microbiol. 78:297-303.
27. Johansson J, et al. 2002. An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110:551-561.
28. Jones S, Drouin P, Wilkinson B, Morse P. 2002. Correlation of longrange membrane order with temperature-dependent growth characteristics of parent and a cold-sensitive, branched-chain-fatty-acid-deficient mutant of Listeria monocytogenes. Arch. Microbiol. 177:217-222.
29. oC. Appl. Environ. Microbiol. 76:1423-1432.
30. Kaneda T. 1991. Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol. Rev. 55:288-302.
31. Keeney K, Colosi L, Weber W, O'Riordan M. 2009. Generation of branched-chain fatty acids through lipoate-dependent metabolism facilitates intracellular growth of Listeria monocytogenes. J. Bacteriol. 191:2187-2196.
32. Koprivnjak T, Peschel A. 2011. Bacterial resistance mechanisms against host defense peptides. Cell. Mol. Life Sci. 68:2243-2254.
33. Lawhon S, Maurer R, Suyemoto M, Altier C. 2002. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Mol. Microbiol. 46:1451-1464.
34. Lee PP, Weppner WA, Neuhaus FC. 1980. Initial membrane reaction in peptidoglycan synthesis: perturbation of lipid-phospho-Nacetylmuramyl-pentapeptide translocase interactions by n-Butanol. Biochim. Biophys. Acta Biomembr. 597:603-613.
35. Martínez B, Rodríguez A. 2005. Antimicrobial susceptibility of nisin resistant Listeria monocytogenes of dairy origin. FEMS Microbiol. Lett. 252:67-72.
36. Mendez-Samperio P. 2010. The human cathelicidin hCAP18/LL-37: amultifunctional peptide involved in mycobacterial infections. Peptides 31:1791-1798.
37. Mendoza F, Maqueda M, Galvez A, Martinez-Bueno M, Valdivia E. 1999. Antilisterial activity of peptide AS-48 and study of changes induced in the cell envelope properties of an AS-48-adapted strain of Listeria monocytogenes. Appl. Environ. Microbiol. 65:618-625.
38. Milenbachs AA, Brown DP, Moors M, Youngman P. 1997. Carbon source regulation of virulence gene expression in Listeria monocytogenes. Mol. Microbiol. 23:1075-1085.
39. Ming X, Daeschel M. 1993. Nisin resistance of foodborne bacteria and the specific resistance responses of Listeria monocytogenes Scott-A. J. Food Prot. 56:944-948.
40. Mishra NN, et al. 2011. In vitro cross-resistance to daptomycin and host defense cationic antimicrobial peptides in clinical methicillin-resistant Staphylococcus aureus isolates. Antimicrob. Agents Chemother. 55:4012-4018.
41. Mishra NN, et al. 2011. Carotenoid-related alteration of cell membrane fluidity impacts Staphylococcus aureus susceptibility to host defense peptides. Antimicrob. Agents Chemother. 55:526-531.
42. Naghmouchi K, Drider D, Hammami R, Fliss I. 2008. Effect of antimicrobial peptides divergicin M35 and nisin A on Listeria monocytogenes LSD530 potassium channels. Curr. Microbiol. 56:609-612.
43. Nakanishi N, et al. 2009. Regulation of virulence by butyrate sensing in enterohaemorrhagic Escherichia coli. Microbiology 155:521-530.
44. Parsons JB, Frank MW, Subramanian C, Saenkham P, Rock CO. 2011. Metabolic basis for the differential susceptibility of Gram-positive pathogens to fatty acid synthesis inhibitors. Proc. Natl. Acad. Sci. U. S. A. 108: 15373-15383.
45. Potter R, Truelstrup Hansen L, Gill TA. 2005. Inhibition of foodborne bacteria by native and modified protamine: importance of electrostatic interactions. Int. J. Food Microbiol. 103:23-34.
46. Rae CS, Geissler A, Adamson PC, Portnoy DA. 2011. Mutations of the Listeria monocytogenes peptidoglycan N-deacetylase and O-acetylase result in enhanced lysozyme sensitivity, bacteriolysis, and hyperinduction of innate immune pathways. Infect. Immun. 79:3596-3606.
47. Shinoda W, Mikami M, Baba T, Hato M. 2004. Molecular dynamics study on the effects of chain branching on the physical properties of lipid bilayers. 2. Permeability. J. Phys. Chem. B 108:9346-9356.
48. Singh AK, et al. 2009. FabH selectivity for anteiso branched-chain fatty acid precursors in low-temperature adaptation in Listeria monocytogenes. FEMS Microbiol. Lett. 301:188-192.
49. Stenz L, et al. 2011. The CodY pleiotropic repressor controls virulence in Gram-positive pathogens. FEMS Immunol. Med. Microbiol. 62:123-139.
50. Storm DR, Rosenthal KS, Swanson PE. 1977. Polymyxin and related peptide antibiotics. Annu. Rev. Biochem. 46:723-763.
51. Sun Y, O'Riordan MXD. 2010. Branched-chain fatty acids promote Listeria monocytogenes intracellular infection and virulence. Infect. Immun. 78:4667-4673.
52. Thedieck K, et al. 2006. The MprF protein is required for lysinylation of phospholipids in listerial membranes and confers resistance to cationic antimicrobial peptides (CAMPs) on Listeria monocytogenes. Mol. Microbiol. 62:1325-1339.
53. Tobe T, Nakanishi N, Sugimoto N. 2011. Activation of motility by sensing short-chain fatty acids via two steps in a flagellar gene regulatory cascade in enterohemorrhagic Escherichia coli. Infect. Immun. 79:1016-1024.
54. Tristram-Nagle S, et al. 2010. Structure and water permeability of fully hydrated diphytanoyl PC. Chem. Phys. Lipids 163:630-637.
55. Turner J, Cho Y, Dinh N-N, Waring AJ, Lehrer RI. 1998. Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils. Antimicrob. Agents Chemother. 42:2206-2214.
56. Vadyvaloo V, et al. 2004. Cell-surface alterations in class IIa bacteriocinresistant Listeria monocytogenes strains. Microbiology 150:3025-3033.
57. Vadyvaloo V, Hastings JW, van der Merwe MJ, Rautenbach M. 2002. Membranes of class IIa bacteriocin-resistant Listeria monocytogenes cells contain increased levels of desaturated and short-acyl-chain phosphatidylglycerols. Appl. Environ. Microbiol. 68:5223-5230.
58. Verdon J, et al. 2011. Fatty acid composition modulates sensitivity of Legionella pneumophila to warnericin RK, an antimicrobial peptide. Biochim. Biophys. Acta Biomembr. 1808:1146-1153.
59. Whittaker P, et al. 2005. Use of fatty acid profiles to identify food-borne bacterial pathogens and aerobic endospore-forming bacilli. J. Agric. Food Chem. 53:3735-3742.
60. Willecke K, Pardee AB. 1971. Fatty acid-requiring mutant of Bacillus subtilis defective in branched chain α-keto acid dehydrogenase. J. Biol. Chem. 246:5264-5272.
61. Yeaman MR, Yount NY. 2003. Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 55:27-55.
62. Zhang Y-M, Rock CO. 2008. Membrane lipid homeostasis in bacteria. Nat. Rev. Microbiol. 6:222-233.
63. Zhu K, Ding X, Julotok M, Wilkinson BJ. 2005. Exogenous isoleucine and fatty acid shortening ensure the high content of anteiso-C15:0 fatty acid required for low-temperature growth of Listeria monocytogenes. Appl. Environ. Microbiol. 71:8002-8007.