PhoPQ regulates acidic glycerophospholipid content of the Salmonella Typhimurium outer membrane

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

Volumn 111, Issue 5, 2014, Pages 1963-1968

  Dalebroux, Zachary D ^a   Matamouros, Susana ^a   Whittington, Dale ^a   Bishop, Russell E ^b   Miller, Samuel I ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Acyltransferase; Lipid remodeling; Pathogenesis; Signal transduction

Indexed keywords

CARDIOLIPIN; GLYCEROPHOSPHOLIPID; LIPID A; LIPOPOLYSACCHARIDE; PHOP PROTEIN;

ACYLATION; ALLELE; ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; CELL SURVIVAL; INNATE IMMUNITY; LIPID ANALYSIS; MEMBRANE LEAFLET; MEMBRANE STRUCTURE; NONHUMAN; OUTER MEMBRANE; PH; PHAGOSOME; PRIORITY JOURNAL; REGULATORY MECHANISM; SALMONELLA TYPHIMURIUM;

ACYLTRANSFERASE; LIPID REMODELING; PATHOGENESIS; SIGNAL TRANSDUCTION;

ALLELES; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL PROTEINS; CARDIOLIPINS; CELL MEMBRANE; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GLYCEROPHOSPHOLIPIDS; PALMITATES; POLYMYXIN B; SALMONELLA TYPHIMURIUM; TRANSCRIPTION, GENETIC;

EID: 84893511071     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1316901111     Document Type: Article

References (40)

1. Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67(4):593-656.
2. Needham BD, Trent MS (2013) Fortifying the barrier: The impact of lipid A remodelling on bacterial pathogenesis. Nat Rev Microbiol 11(7):467-481.
3. Haraga A, Ohlson MB, Miller SI (2008) Salmonellae interplay with host cells. Nat Rev Microbiol 6(1):53-66.
4. Prost LR, Miller SI (2008) The Salmonellae PhoQ sensor: Mechanisms of detection of phagosome signals. Cell Microbiol 10(3):576-582.
5. Murata T, Tseng W, Guina T, Miller SI, Nikaido H (2007) PhoPQ-mediated regulation produces a more robust permeability barrier in the outer membrane of Salmonella enterica serovar typhimurium. J Bacteriol 189(20):7213-7222.
6. Gunn JS, Belden WJ, Miller SI (1998) Identification of PhoP-PhoQ activated genes within a duplicated region of the Salmonella typhimurium chromosome. Microb Pathog 25(2):77-90.
7. Bishop RE, et al. (2000) Transfer of palmitate from phospholipids to lipid A in outer membranes of gram-negative bacteria. EMBO J 19(19):5071-5080.
8. Hwang PM, et al. (2002) Solution structure and dynamics of the outer membrane enzyme PagP by NMR. Proc Natl Acad Sci USA 99(21):13560-13565.
9. Guo L, et al. (1998) Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95(2):189-198.
10. Jia W, et al. (2004) Lipid trafficking controls endotoxin acylation in outer membranes of Escherichia coli. J Biol Chem 279(43):44966-44975.
11. Dekker N (2000) Outer-membrane phospholipase A: Known structure, unknown biological function. Mol Microbiol 35(4):711-717.
12. Malinverni JC, Silhavy TJ (2009) An ABC transport system that maintains lipid asymmetry in the gram-negative outer membrane. Proc Natl Acad Sci USA 106(19): 8009-8014.
13. Hsu L, Jackowski S, Rock CO (1991) Isolation and characterization of Escherichia coli K-12 mutants lacking both 2-acyl-glycerophosphoethanolamine acyltransferase and acyl-acyl carrier protein synthetase activity. J Biol Chem 266(21):13783-13788.
14. Ames GF (1968) Lipids of Salmonella typhimurium and Escherichia coli: Structure and metabolism. J Bacteriol 95(3):833-843.
15. Garrett TA, Kordestani R, Raetz CR (2007) Quantification of cardiolipin by liquid chromatography-electrospray ionization mass spectrometry. Methods Enzymol 433: 213-230.
16. Parsons JB, Rock CO (2013) Bacterial lipids: Metabolism and membrane homeostasis. Prog Lipid Res 52(3):249-276.
17. Zhou Z, White KA, Polissi A, Georgopoulos C, Raetz CR (1998) Function of Escherichia coli MsbA, an essential ABC family transporter, in lipid A and phospholipid biosynthesis. J Biol Chem 273(20):12466-12475.
18. Gunn JS, Miller SI (1996) PhoP-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance. J Bacteriol 178(23):6857-6864.
19. Olsen RW, Ballou CE (1971) Acyl phosphatidylglycerol: A new phospholipid from Salmonella typhimurium. J Biol Chem 246(10):3305-3313.
20. Hsu FF, Turk J (2006) Characterization of cardiolipin from Escherichia coli by electrospray ionization with multiple stage quadrupole ion-trap mass spectrometric analysis of [M-2H + Na]-ions. J Am Soc Mass Spectrom 17(3):420-429.
21. Hsu FF, Turk J, Shi Y, Groisman EA (2004) Characterization of acylphosphatidylglycerols from Salmonella typhimurium by tandem mass spectrometry with electrospray ionization. J Am Soc Mass Spectrom 15(1):1-11.
22. Bader MW, et al. (2003) Regulation of Salmonella typhimurium virulence gene expression by cationic antimicrobial peptides. Mol Microbiol 50(1):219-230.
23. Ahn VE, et al. (2004) A hydrocarbon ruler measures palmitate in the enzymatic acylation of endotoxin. EMBO J 23(15):2931-2941.
24. Guo L, et al. (1997) Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science 276(5310):250-253.
25. Cuesta-Seijo JA, et al. (2010) PagP crystallized from SDS/cosolvent reveals the route for phospholipid access to the hydrocarbon ruler. Structure 18(9):1210-1219.
26. Khan MA, Bishop RE (2009) Molecular mechanism for lateral lipid diffusion between the outer membrane external leaflet and a beta-barrel hydrocarbon ruler. Biochemistry 48(41):9745-9756.
27. Osborn MJ, Gander JE, Parisi E, Carson J (1972) Mechanism of assembly of the outer membrane of Salmonella typhimurium: Isolation and characterization of cytoplasmic and outer membrane. J Biol Chem 247(12):3962-3972.
28. Koppelman CM, Den Blaauwen T, Duursma MC, Heeren RM, Nanninga N (2001) Escherichia coli minicell membranes are enriched in cardiolipin. J Bacteriol 183(20):6144-6147.
29. Renner LD, Weibel DB (2011) Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes. Proc Natl Acad Sci USA 108(15):6264-6269.
30. Renner LD, Weibel DB (2012) MinD and MinE interact with anionic phospholipids and regulate division plane formation in Escherichia coli. J Biol Chem 287(46): 38835-38844.
31. Doan T, et al. (2013) FisB mediates membrane fission during sporulation in Bacillus subtilis. Genes Dev 27(3):322-334.
32. Schlame M (2008) Cardiolipin synthesis for the assembly of bacterial and mitochondrial membranes. J Lipid Res 49(8):1607-1620.
33. Tran TT, et al. (2013) Daptomycin-resistant Enterococcus faecalis diverts the antibiotic molecule from the division septum and remodels cell membrane phospholipids. MBio 4(4).
34. Hartmann M, et al. (2010) Damage of the bacterial cell envelope by antimicrobial peptides gramicidin S and PGLa as revealed by transmission and scanning electron microscopy. Antimicrob Agents Chemother 54(8):3132-3142.
35. Bishop RE (2005) The lipid A palmitoyltransferase PagP: Molecular mechanisms and role in bacterial pathogenesis. Mol Microbiol 57(4):900-912.
36. Guzman LM, Belin D, Carson MJ, Beckwith J (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177(14):4121-4130.
37. Castanié-Cornet MP, Cam K, Jacq A (2006) RcsF is an outer membrane lipoprotein involved in the RcsCDB phosphorelay signaling pathway in Escherichia coli. J Bacteriol 188(12):4264-4270.
38. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(8):911-917.
39. Khan MA, et al. (2007) Gauging a hydrocarbon ruler by an intrinsic exciton probe. Biochemistry 46(15):4565-4579.
40. Homma H, Kudo I, Inoue K, Nojima S (1987) Characteristics of phospholipid transacylase of Escherichia coli. J Biochem 101(4):1033-1039.