Daptomycin inhibits cell envelope synthesis by interfering with fluid membrane microdomains

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

Volumn 113, Issue 45, 2016, Pages E7077-E7086

  Müller, Anna ^a,b   Wenzel, Michaela ^c   Strahl, Henrik ^d   Grein, Fabian ^a,b   Saaki, Terrens N V ^c   Kohl, Bastian ^e   Siersma, Tjalling ^c   Bandow, Julia E ^e   Sahl, Hans Georg ^a,b   Schneider, Tanja ^a,b   Hamoen, Leendert W ^c  

^a UNIVERSITY OF BONN   (Germany)

^b German Center for Infection Research (DZIF)   (Germany)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

^e RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Antibiotics; Bacillus subtilis; Cell wall biosynthesis; Daptomycin; Membrane potential

Indexed keywords

DAPTOMYCIN; LIPID 2 SYNTHASE MURG; PHOSPHOLIPID SYNTHASE PLSX; SYNTHETASE; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL WALL; CELL MEMBRANE; CONTROLLED STUDY; FLUORESCENT LIGHTING; HYDROPHOBICITY; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; SYNTHESIS;

EID: 84994508668     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1611173113     Document Type: Article

References (91)

1. Baltz RH, Miao V, Wrigley SK (2005) Natural products to drugs: Daptomycin and related lipopeptide antibiotics. Nat Prod Rep 22(6):717-741.
2. Debono M, et al. (1987) A21978C, a complex of new acidic peptide antibiotics: Isolation, chemistry, and mass spectral structure elucidation. J Antibiot (Tokyo) 40(6):761-777.
3. Baltz RH, McHenney MA, Hosted TJ (1997) Genetics of lipopeptide antibiotic biosynthesis in Streptomyces fradiae A54145 and Streptomyces roseosporus A21978C. Developments in Industrial Microbiology, eds Baltz RH, Hegeman GD, Skatrud PL (Society for Industrial Microbiology, Fairfax, VA), p 93.
4. Allen NE, Hobbs JN, Alborn WEJ, Jr (1987) Inhibition of peptidoglycan biosynthesis in gram-positive bacteria by LY146032. Antimicrob Agents Chemother 31(7):1093-1099.
5. Huber FM, Pieper RL, Tietz AJ (1988) The formation of daptomycin by supplying decanoic acid to Streptomyces roseosporus cultures producing the antibiotic complex A21978C. J Biotechnol 7(4):283-292.
6. Straus SK, Hancock REW (2006) Mode of action of the new antibiotic for Gram-positive pathogens daptomycin: Comparison with cationic antimicrobial peptides and lipopeptides. Biochim Biophys Acta 1758(9):1215-1223.
7. Jung D, Rozek A, Okon M, Hancock REW (2004) Structural transitions as determinants of the action of the calcium-dependent antibiotic daptomycin. Chem Biol 11(7):949-957.
8. Scott WRP, Baek S-B, Jung D, Hancock REW, Straus SK (2007) NMR structural studies of the antibiotic lipopeptide daptomycin in DHPC micelles. Biochim Biophys Acta 1768(12):3116-3126.
9. Rotondi KS, Gierasch LM (2005) A well-defined amphipathic conformation for the calciumfree cyclic lipopeptide antibiotic, daptomycin, in aqueous solution. Biopolymers 80(2-3):374-385.
10. Ball L-J, Goult CM, Donarski JA, Micklefield J, Ramesh V (2004) NMR structure determination and calcium binding effects of lipopeptide antibiotic daptomycin. Org Biomol Chem 2(13):1872-1878.
11. Hachmann AB, et al. (2011) Reduction in membrane phosphatidylglycerol content leads to daptomycin resistance in Bacillus subtilis. Antimicrob Agents Chemother 55(9):4326-4337.
12. Mengin-Lecreulx D, Allen NE, Hobbs JN, van Heijenoort J (1990) Inhibition of peptidoglycan biosynthesis in Bacillus megaterium by daptomycin. FEMS Microbiol Lett 57(3):245-248.
13. Schneider T, et al. (2009) The lipopeptide antibiotic Friulimicin B inhibits cell wall biosynthesis through complex formation with bactoprenol phosphate. Antimicrob Agents Chemother 53(4):1610-1618.
14. Canepari P, Boaretti M, Lleó MM, Satta G (1990) Lipoteichoic acid as a new target for activity of antibiotics: Mode of action of daptomycin (LY146032). Antimicrob Agents Chemother 34(6):1220-1226.
15. Laganas V, Alder J, Silverman JA (2003) In vitro bactericidal activities of daptomycin against Staphylococcus aureus and Enterococcus faecalis are not mediated by inhibition of lipoteichoic acid biosynthesis. Antimicrob Agents Chemother 47(8):2682-2684.
16. Silverman JA, Perlmutter NG, Shapiro HM (2003) Correlation of daptomycin bactericidal activity and membrane depolarization in Staphylococcus aureus. Antimicrob Agents Chemother 47(8):2538-2544.
17. Zhang T, Muraih JK, MacCormick B, Silverman J, Palmer M (2014) Daptomycin forms cationand size-selective pores in model membranes. Biochim Biophys Acta 1838(10):2425-2430.
18. Wecke T, et al. (2009) Daptomycin versus Friulimicin B: In-depth profiling of Bacillus subtilis cell envelope stress responses. Antimicrob Agents Chemother 53(4):1619-1623.
19. Hachmann A-B, Angert ER, Helmann JD (2009) Genetic analysis of factors affecting susceptibility of Bacillus subtilis to daptomycin. Antimicrob Agents Chemother 53(4):1598-1609.
20. Lenarcic R, et al. (2009) Localisation of DivIVA by targeting to negatively curved membranes. EMBO J 28(15):2272-2282.
21. Ramamurthi KS, Losick R (2009) Negative membrane curvature as a cue for subcellular localization of a bacterial protein. Proc Natl Acad Sci USA 106(32):13541-13545.
22. Pogliano J, Pogliano N, Silverman JA (2012) Daptomycin-mediated reorganization of membrane architecture causes mislocalization of essential cell division proteins. J Bacteriol 194(17):4494-4504.
23. Wenzel M, et al. (2012) Proteomic response of Bacillus subtilis to lantibiotics reflects differences in interaction with the cytoplasmic membrane. Antimicrob Agents Chemother 56(11):5749-5757.
24. Bandow JE, Brötz H, Leichert LI, Labischinski H, Hecker M (2003) Proteomic approach to understanding antibiotic action. Antimicrob Agents Chemother 47(3):948-955.
25. Kobayashi R, Suzuki T, Yoshida M (2007) Escherichia coli phage-shock protein A (PspA) binds to membrane phospholipids and repairs proton leakage of the damaged membranes. Mol Microbiol 66(1):100-109.
26. Mascher T, Margulis NG, Wang T, Ye RW, Helmann JD (2003) Cell wall stress responses in Bacillus subtilis: The regulatory network of the bacitracin stimulon. Mol Microbiol 50(5):1591-1604.
27. Sun G, et al. (1996) Regulators of aerobic and anaerobic respiration in Bacillus subtilis. J Bacteriol 178(5):1374-1385.
28. Julsing MK, Rijpkema M, Woerdenbag HJ, Quax WJ, Kayser O (2007) Functional analysis of genes involved in the biosynthesis of isoprene in Bacillus subtilis. Appl Microbiol Biotechnol 75(6):1377-1384.
29. Leatherbarrow AJ, Yazdi MA, Curson JP, Moir A (1998) The gerC locus of Bacillus subtilis, required for menaquinone biosynthesis, is concerned only indirectly with spore germination. Microbiology 144(Pt 8):2125-2130.
30. Alborn WEJ, Jr, Allen NE, Preston DA (1991) Daptomycin disrupts membrane potential in growing Staphylococcus aureus. Antimicrob Agents Chemother 35(11):2282-2287.
31. Wenzel M, et al. (2013) Analysis of the mechanism of action of potent antibacterial hetero-tri-organometallic compounds: A structurally new class of antibiotics. ACS Chem Biol 8(7):1442-1450.
32. Wenzel M, et al. (2015) Antimicrobial Peptides from the Aurein Family Form Ion-Selective Pores in Bacillus subtilis. ChemBioChem 16(7):1101-1108.
33. Te Winkel JD, Gray DA, Seistrup KH, Hamoen LW, Strahl H (2016) Analysis of antimicrobialtriggered membrane depolarisation using voltage sensitive dyes. Front Cell Dev Biol 4:29.
34. Strahl H, Hamoen LW (2010) Membrane potential is important for bacterial cell division. Proc Natl Acad Sci USA 107(27):12281-12286.
35. Lewis PJ, Thaker SD, Errington J (2000) Compartmentalization of transcription and translation in Bacillus subtilis. EMBO J 19(4):710-718.
36. Koller D, Lohner K (2014) The role of spontaneous lipid curvature in the interaction of interfacially active peptides with membranes. Biochim Biophys Acta 1838(9):2250-2259.
37. Zweytick D, Tumer S, Blondelle SE, Lohner K (2008) Membrane curvature stress and antibacterial activity of lactoferricin derivatives. Biochem Biophys Res Commun 369(2):395-400.
38. Strahl H, Burmann F, Hamoen LW (2014) The actin homologue MreB organizes the bacterial cell membrane. Nat Commun 5:3442.
39. Kucherak OA, et al. (2010) Switchable nile red-based probe for cholesterol and lipid order at the outer leaflet of biomembranes. J Am Chem Soc 132(13):4907-4916.
40. Parasassi T, Gratton E (1995) Membrane lipid domains and dynamics as detected by Laurdan fluorescence. J Fluoresc 5(1):59-69.
41. Andrich MP, Vanderkooi JM (1976) Temperature dependence of 1, 6-diphenyl-1, 3, 5-hexatriene fluorescence in phophoslipid artificial membranes. Biochemistry 15(6):1257-1261.
42. Vanderkooi JM, Landesberg R, Selick H, 2nd, McDonald GG (1977) Interaction of general anesthetics with phospholipid vesicles and biological membranes. Biochim Biophys Acta 464(1):1-18.
43. Cornell RB, Taneva SG (2006) Amphipathic helices as mediators of the membrane interaction of amphitropic proteins, and as modulators of bilayer physical properties. Curr Protein Pept Sci 7(6):539-552.
44. Friedlander G, Le Grimellec C, Giocondi MC, Amiel C (1987) Benzyl alcohol increases membrane fluidity and modulates cyclic AMP synthesis in intact renal epithelial cells. Biochim Biophys Acta 903(2):341-348.
45. McMahon HT, Gallop JL (2005) Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438(7068):590-596.
46. Kobayashi K, et al. (2003) Essential Bacillus subtilis genes. Proc Natl Acad Sci USA 100(8):4678-4683.
47. Sastre DE, Bisson-Filho A, de Mendoza D, Gueiros-Filho FJ (2016) Revisiting the cell biology of the acyl-ACP: phosphate transacylase PlsX suggests that the phospholipid synthesis and cell division machineries are not coupled in Bacillus subtilis. Mol Microbiol 100(4):621-634.
48. Takada H, et al. (2014) An essential enzyme for phospholipid synthesis associates with the Bacillus subtilis divisome. Mol Microbiol 91(2):242-255.
49. Grunewald J, Sieber SA, Mahlert C, Linne U, Marahiel MA (2004) Synthesis and derivatization of daptomycin: A chemoenzymatic route to acidic lipopeptide antibiotics. J Am Chem Soc 126(51):17025-17031.
50. Lohani CR, Taylor R, Palmer M, Taylor SD (2015) Solid-phase total synthesis of daptomycin and analogs. Org Lett 17(3):748-751.
51. Taylor R, et al. (2016) Two successive calcium-dependent transitions mediate membrane binding and oligomerization of daptomycin and the related antibiotic A54145. Biochim Biophys Acta 1858(9):1999-2005.
52. Blosser MC, Honerkamp-Smith AR, Han T, Haataja M, Keller SL (2015) Transbilayer Colocalization of Lipid Domains Explained via Measurement of Strong Coupling Parameters. Biophys J 109(11):2317-2327.
53. Putzel GG, Uline MJ, Szleifer I, Schick M (2011) Interleaflet coupling and domain registry in phase-separated lipid bilayers. Biophys J 100(4):996-1004.
54. Kiessling V, Wan C, Tamm LK (2009) Domain coupling in asymmetric lipid bilayers. Biochim Biophys Acta 1788(1):64-71.
55. Zhang T, et al. (2014) Cardiolipin prevents membrane translocation and permeabilization by daptomycin. J Biol Chem 289(17):11584-11591.
56. Ganchev DN, Hasper HE, Breukink E, de Kruijff B (2006) Size and orientation of the lipid II headgroup as revealed by AFM imaging. Biochemistry 45(19):6195-6202.
57. Muchova K, Wilkinson AJ, Barak I (2011) Changes of lipid domains in Bacillus subtilis cells with disrupted cell wall peptidoglycan. FEMS Microbiol Lett 325(1):92-98.
58. Schirner K, et al. (2015) Lipid-linked cell wall precursors regulate membrane association of bacterial actin MreB. Nat Chem Biol 11(1):38-45.
59. Reyes J, et al. (2015) A liaR deletion restores susceptibility to daptomycin and antimicrobial peptides in multidrug-resistant Enterococcus faecalis. J Infect Dis 211(8):1317-1325.
60. Camargo ILB da C, Neoh H-M, Cui L, Hiramatsu K (2008) Serial daptomycin selection generates daptomycin-nonsusceptible Staphylococcus aureus strains with a heterogeneous vancomycin-intermediate phenotype. Antimicrob Agents Chemother 52(12):4289-4299.
61. Muthaiyan A, Silverman JA, Jayaswal RK, Wilkinson BJ (2008) Transcriptional profiling reveals that daptomycin induces the Staphylococcus aureus cell wall stress stimulon and genes responsive to membrane depolarization. Antimicrob Agents Chemother 52(3):980-990.
62. Schneider T, Sahl HG (2010) An oldie but a goodie - cell wall biosynthesis as antibiotic target pathway. Int J Med Microbiol 300(2-3):161-169.
63. Weidenmaier C, Peschel A (2008) Teichoic acids and related cell wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 6(4):276-287.
64. Bhavsar AP, D'Elia MA, Sahakian TD, Brown ED (2007) The amino terminus of Bacillus subtilis TagB possesses separable localization and functional properties. J Bacteriol 189(19):6816-6823.
65. Paoletti L, Lu Y-J, Schujman GE, de Mendoza D, Rock CO (2007) Coupling of fatty acid and phospholipid synthesis in Bacillus subtilis. J Bacteriol 189(16):5816-5824.
66. Chazarreta-Cifre L, Martiarena L, de Mendoza D, Altabe SG (2011) Role of ferredoxin and flavodoxins in Bacillus subtilis fatty acid desaturation. J Bacteriol 193(16):4043-4048.
67. de Mendoza D, Cronan JE (1983) Thermal regulation of membrane lipid fluidity in bacteria. Trends Biochem Sci 8(2):49-52.
68. Beranova J, Jemioa-Rzeminska M, Elhottova D, Strzaka K, Konopasek I (2008) Metabolic control of the membrane fluidity in Bacillus subtilis during cold adaptation. Biochim Biophys Acta - Biomembr 1778(2):445-453.
69. Wenzel M, et al. (2011) Proteomic signature of fatty acid biosynthesis inhibition available for in vivo mechanism-of-action studies. Antimicrob Agents Chemother 55(6):2590-2596.
70. Wenzel M, et al. (2014) Small cationic antimicrobial peptides delocalize peripheral membrane proteins. Proc Natl Acad Sci USA 111(14):E1409-E1418.
71. Kingston AW, Subramanian C, Rock CO, Helmann JD (2011) A-DW-dependent stress response in Bacillus subtilis that reduces membrane fluidity. Mol Microbiol 81(1):69-79.
72. Epand RF, Schmitt MA, Gellman SH, Epand RM (2006) Role of membrane lipids in the mechanism of bacterial species selective toxicity by two α/β-antimicrobial peptides. Biochim Biophys Acta - Biomembr 1758(9):1343-1350.
73. Epand RF, et al. (2008) Dual mechanism of bacterial lethality for a cationic sequence-random copolymer that mimics host-defense antimicrobial peptides. J Mol Biol 379(1):38-50.
74. Epand RM, Epand RF (2009) Lipid domains in bacterial membranes and the action of antimicrobial agents. Biochim Biophys Acta 1788(1):289-294.
75. Jean-Francois F, et al. (2008) Aggregation of cateslytin β-sheets on negatively charged lipids promotes rigid membrane domains. A new mode of action for antimicrobial peptides? Biochemistry 47(24):6394-6402.
76. Cruzeiro-Hansson L, Mouritsen OG (1988) Passive ion permeability of lipid membranes modelled via lipid-domain interfacial area. Biochim Biophys Acta 944(1):63-72.
77. Bramkamp M, Lopez D (2015) Exploring the existence of lipid rafts in bacteria. Microbiol Mol Biol Rev 79(1):81-100.
78. Bach JN, Bramkamp M (2013) Flotillins functionally organize the bacterial membrane. Mol Microbiol 88(6):1205-1217.
79. Landgraf D, Okumus B, Chien P, Baker TA, Paulsson J (2012) Segregation of molecules at cell division reveals native protein localization. Nat Methods 9(5):480-482.
80. Zacharias DA, Violin JD, Newton AC, Tsien RY (2002) Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296(5569):913-916.
81. Tran TT, Munita JM, Arias CA (2015) Mechanisms of drug resistance: Daptomycin resistance. Ann N Y Acad Sci 1354:32-53.
82. Bertsche U, et al. (2011) Correlation of daptomycin resistance in a clinical Staphylococcus aureus strain with increased cell wall teichoic acid production and D-alanylation. Antimicrob Agents Chemother 55(8):3922-3928.
83. Bertsche U, et al. (2013) Increased cell wall teichoic acid production and D-alanylation are common phenotypes among daptomycin-resistant methicillin-resistant Staphylococcus aureus (MRSA) clinical isolates. PLoS One 8(6):e67398.
84. Peleg AY, et al. (2012) Whole genome characterization of the mechanisms of daptomycin resistance in clinical and laboratory derived isolates of Staphylococcus aureus. PLoS One 7(1):e28316.
85. Yang S-J, Mishra NN, Rubio A, Bayer AS (2013) Causal role of single nucleotide polymorphisms within the mprF gene of Staphylococcus aureus in daptomycin resistance. Antimicrob Agents Chemother 57(11):5658-5664.
86. Khatib TO, Stevenson H, Yeaman MR, Bayer AS, Pokorny A (2016) Binding of Daptomycin to Anionic Lipid Vesicles Is Reduced in the Presence of Lysyl-Phosphatidylglycerol. Antimicrob Agents Chemother 60(8):5051-5053.
87. Lewis RNAH, McElhaney RN (2009) The physicochemical properties of cardiolipin bilayers and cardiolipin-containing lipid membranes. Biochim Biophys Acta 1788(10):2069-2079.
88. Wolf D, et al. (2010) In-depth profiling of the LiaR response of Bacillus subtilis. J Bacteriol 192(18):4680-4693.
89. Miller C, et al. (2013) Adaptation of Enterococcus faecalis to daptomycin reveals an ordered progression to resistance. Antimicrob Agents Chemother 57(11):5373-5383.
90. Dubrac S, Bisicchia P, Devine KM, Msadek T (2008) A matter of life and death: Cell wall homeostasis and the WalKR (YycGF) essential signal transduction pathway. Mol Microbiol 70(6):1307-1322.
91. Hurdle JG, O'Neill AJ, Chopra I, Lee RE (2011) Targeting bacterial membrane function: an underexploited mechanism for treating persistent infections. Nat Rev Microbiol 9(1):62-75.