Structural evidence of α-aminoacylated lipoproteins of Staphylococcus aureus

FEBS Journal

Volumn 278, Issue 5, 2011, Pages 716-728

  Asanuma, Miwako ^a,c   Kurokawa, Kenji ^b   Ichikawa, Rie ^a   Ryu, Kyoung Hwa ^b   Chae, Jun Ho ^b   Dohmae, Naoshi ^a   Lee, Bok Luel ^b   Nakayama, Hiroshi ^a  

^a RIKEN   (Japan)

^b Pusan National University   (South Korea)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

bacterial lipoprotein; Gram positive bacteria; mass spectrometry; N acyltransferase; SitC

Indexed keywords

BACTERIUM LIPOPROTEIN; CYSTEINE; FATTY ACID; LIPOPROTEIN; LIPOPROTEIN LIPASE; TRITON X 114; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; AMINOACYLATION; ARTICLE; BACTERIAL STRAIN; CELL LYSATE; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN STRUCTURE; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; TANDEM MASS SPECTROMETRY;

BACTERIAL PROTEINS; LIPOPROTEINS, HDL; STAPHYLOCOCCUS AUREUS; TANDEM MASS SPECTROMETRY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAMMALIA; POSIBACTERIA; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 79951905038     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07990.x     Document Type: Article

References (33)

1. Tokunaga M, Tokunaga H, &, Wu HC, (1982) Post-translational modification and processing of Escherichia coli prolipo (Pubitemid 12093249)
2. Buddelmeijer N, &, Young R, (2010) The essential Escherichia coli apolipoprotein N-acyltransferase (Lnt) exists as an extracytoplasmic thioester acyl-enzyme intermediate. Biochemistry 49, 341-346.
3. Fukuda A, Matsuyama S, Hara T, Nakayama J, Nagasawa H, &, Tokuda H, (2002) Aminoacylation of the N-terminal cysteine is essential for Lol-dependent release of lipoproteins from membranes but does not depend on lipoprotein sorting signals. J Biol Chem 277, 43512-43518. (Pubitemid 35285740)
4. Tokuda H, &, Matsuyama S, (2004) Sorting of lipoproteins to the outer membrane in E. coli. Biochim Biophys Acta 1693, 5-13. (Pubitemid 38970131)
5. Stoll H, Dengjel J, Nerz C, &, Götz F, (2005) Staphylococcus aureus deficient in lipidation of prelipoproteins is attenuated in growth and immune activation. Infect Immun 73, 2411-2423. (Pubitemid 40470844)
6. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, Bertero MG, Bessières P, Bolotin A, Borchert S, et al. (1997) The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390, 249-256. (Pubitemid 27513299)
7. Baba T, Takeuchi F, Kuroda M, Yuzawa H, Aoki K, Oguchi A, Nagai Y, Iwama N, Asano K, Naimi T, et al. (2002) Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359, 1819-1827. (Pubitemid 34607058)
8. Paulsen IT, Banerjei L, Myers GSA, Nelson KE, Seshadri R, Read TD, Fouts DE, Eisen JA, Gill SR, Heidelberg JF, et al. (2003) Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299, 2071-2074. (Pubitemid 36383734)
9. Tschumi A, Nai C, Auchli Y, Hunziker P, Gehrig P, Keller P, Grau T, &, Sander P, (2009) Identification of apolipoprotein N-acyltransferase (Lnt) in mycobacteria. J Biol Chem 284, 27146-27156.
10. Mühlradt PF, Kiess M, Meyer H, Süssmuth R, &, Jung G, (1997) Isolation, structure elucidation, and synthesis of a macrophage stimulatory lipopeptide from Mycoplasma fermentans acting at picomolar concentration. J Exp Med 185, 1951-1958. (Pubitemid 27247081)
11. Tawaratsumida K, Furuyashiki M, Katsumoto M, Fujimoto Y, Fukase K, Suda Y, &, Hashimoto M, (2009) Characterization of N-terminal structure of TLR2-activating lipoprotein in Staphylococcus aureus. J Biol Chem 284, 9147-9152.
12. Shimizu T, Kida Y, &, Kuwano K, (2005) A dipalmitoylated lipoprotein from Mycoplasma pneumoniae activates NF-κB through TLR1, TLR2, and TLR6. J Immunol 175, 4641-4646. (Pubitemid 41362004)
13. Hayashi S, Chang SY, Chang S, Giam CZ, &, Wu HC, (1985) Modification and processing of internalized signal sequences of prolipoprotein in Escherichia coli and in Bacillus subtilis. J Biol Chem 260, 5753-5759. (Pubitemid 15001138)
14. Navarre WW, Daefler S, &, Schneewind O, (1996) Cell wall sorting of lipoproteins in Staphylococcus aureus. J Bacteriol 178, 441-446. (Pubitemid 26030597)
15. Kurokawa K, Lee H, Roh KB, Asanuma M, Kim YS, Nakayama H, Shiratsuchi A, Choi Y, Takeuchi O, Kang HJ, et al. (2009) The triacylated ATP binding cluster transporter substrate-binding lipoprotein of Staphylococcus aureus functions as a native ligand for Toll-like receptor 2. J Biol Chem 284, 8406-8411.
16. Shimizu T, Kida Y, &, Kuwano K, (2007) Triacylated lipoproteins derived from Mycoplasma pneumoniae activate nuclear factor-κB through toll-like receptors 1 and 2. Immunology 121, 473-483. (Pubitemid 47030085)
17. Shimizu T, Kida Y, &, Kuwano K, (2008) A triacylated lipoprotein from Mycoplasma genitalium activates NF-κB through Toll-like receptor 1 (TLR1) and TLR2. Infect Immun 76, 3672-3678.
18. Takeuchi O, &, Akira S, (2010) Pattern recognition receptors and inflammation. Cell 140, 805-820.
19. Iwasaki A, &, Medzhitov R, (2004) Toll-like receptor control of the adaptive immune responses. Nat Immunol 5, 987-995. (Pubitemid 41057715)
20. Nagai Y, Garrett KP, Ohta S, Bahrun U, Kouro T, Akira S, Takatsu K, &, Kincade PW, (2006) Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity 24, 801-812. (Pubitemid 43867369)
21. Hashimoto M, Tawaratsumida K, Kariya H, Aoyama K, Tamura T, &, Suda Y, (2006) Lipoprotein is a predominant Toll-like receptor 2 ligand in Staphylococcus aureus cell wall components. Int Immunol 18, 355-362. (Pubitemid 43160148)
22. Bubeck Wardenburg J, Williams WA, &, Missiakas D, (2006) Host defenses against Staphylococcus aureus infection require recognition of bacterial lipoproteins. Proc Natl Acad Sci USA 103, 13831-13836. (Pubitemid 44413993)
23. Omueti KO, Beyer JM, Johnson CM, Lyle EA, &, Tapping RI, (2005) Domain exchange between human toll-like receptors 1 and 6 reveals a region required for lipopeptide discrimination. J Biol Chem 280, 36616-36625. (Pubitemid 41587738)
24. Buwitt-Beckmann U, Heine H, Wiesmüller KH, Jung G, Brock R, Akira S, &, Ulmer AJ, (2005) Toll-like receptor 6-independent signaling by diacylated lipopeptides. Eur J Immunol 35, 282-289. (Pubitemid 40123875)
25. Buwitt-Beckmann U, Heine H, Wiesmüller KH, Jung G, Brock R, Akira S, &, Ulmer AJ, (2006) TLR1- and TLR6-independent recognition of bacterial lipopeptides. J Biol Chem 281, 9049-9057. (Pubitemid 43864617)
26. Cockayne A, Hill PJ, Powell NBL, Bishop K, Sims C, &, Williams P, (1998) Molecular cloning of a 32-kilodalton lipoprotein component of a novel iron-regulated Staphylococcus epidermidis ABC transporter. Infect Immun 66, 3767-3774. (Pubitemid 28347835)
27. Müller P, Müller-Anstett M, Wagener J, Gao Q, Kaesler S, Schaller M, Biedermann T, &, Götz F, (2010) The Staphylococcus aureus lipoprotein SitC colocalizes with Toll-like receptor 2 (TLR2) in murine keratinocytes and elicits intracellular TLR2 accumulation. Infect Immun 78, 4243-4250.
28. Hutchings MI, Palmer T, Harrington DJ, &, Sutcliffe IC, (2009) Lipoprotein biogenesis in Gram-positive bacteria: knowing when to hold 'em, knowing when to fold 'em. Trends Microbiol 17, 13-21.
29. Lagerwerf FM, van de Weert M, Heerma W, &, Haverkamp J, (1996) Identification of oxidized methionine in peptides. Rapid Commun Mass Spectrom 10, 1905-1910. (Pubitemid 27059008)
30. Schenk M, Belisle JT, &, Modlin RL, (2009) TLR2 looks at lipoproteins. Immunity 31, 847-849.
31. Robichon C, Vidal-Ingigliardi D, &, Pugsley AP, (2005) Depletion of apolipoprotein N-acyltransferase causes mislocalization of outer membrane lipoproteins in Escherichia coli. J Biol Chem 280, 974-983.
32. Kodama K, Fukuzawa S, Nakayama H, Kigawa T, Sakamoto K, Yabuki T, Matsuda N, Shirouzu M, Takio K, Tachibana K, et al. (2006) Regioselective carbon-carbon bond formation in proteins with palladium catalysis; new protein chemistry by organometallic chemistry. ChemBioChem 7, 134-139. (Pubitemid 43076296)
33. Ujihara T, Sakurai I, Mizusawa N, &, Wada H, (2008) A method for analyzing lipid-modified proteins with mass spectrometry. Anal Biochem 374, 429-431.