Secretion genes as determinants of Bacillus anthracis chain length

Journal of Bacteriology

Volumn 194, Issue 15, 2012, Pages 3841-3850

  Nguyen Mau, Sao Mai ^a,b   Oh, So Young ^a,b   Kern, Valerie ^b   Missiakas, Dominique ^a,b   Schneewind, Olaf ^a,b  

^a ARGONNE NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HYDROLASE; PEPTIDOGLYCAN;

ARTICLE; BACILLUS ANTHRACIS; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL SECRETION SYSTEM; BACTERIUM MUTANT; GENETIC COMPLEMENTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION;

ADENOSINE TRIPHOSPHATASES; BACILLUS ANTHRACIS; BACTERIAL PROTEINS; GENE DELETION; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; MUTAGENESIS, INSERTIONAL;

BACILLI (CLASS); BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS);

EID: 84866308291     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00384-12     Document Type: Article

References (69)

1. Anderson VJ, Kern JW, McCool JW, Schneewind O, Missiakas DM. 2011. The SLH domain protein BslO is a determinant of Bacillus anthracis chain length. Mol. Microbiol. 81:192-205.
2. Archambaud C, Nahori MA, Pizarro-Cerda J, Cossart P, Dussurget O. 2006. Control of Listeria superoxide dismutase by phosphorylation. J. Biol. Chem. 281:31812-31822.
3. Beck K, Wu L-F, Brunner J, Müller M. 2000. Discrimination of SRP- and SecA/SecB-dependent substrates involves selective recognition of nascent chains by SRP and trigger factor. EMBO J. 19:134-143.
4. Bensing BA, Sullam PM. 2002. An accessory sec locus of Streptococcus gordonii is required for export of the surface protein GspB and for normal levels of binding to human platelets. Mol. Microbiol. 44:1081-1094.
5. Bensing BA, Sullam PM. 2010. Transport of preproteins by the accessory Sec system requires a specific domain adjacent to the signal peptide. J. Bacteriol. 192:4223-4232.
6. Braunstein M, Espinosa B, Chan J, Beisle JT, Jacobs WR, Jr. 2003. SecA2 functions in the secretion of superoxide dismutase A and in the virulence of Mycobacterium tuberculosis. Mol. Microbiol. 48:453-464.
7. Bruckner V, Kovacs J, Denes G. 1953. Structure of poly-D-glutamic acid isolated from capsulated strains of B. anthracis. Nature 172:508.
8. Choudhury B, et al. 2006. The structure of the major cell wall polysaccharide of Bacillus anthracis is species specific. J. Biol. Chem. 281:27932-27941.
9. Dalbey RE, Wickner W. 1985. Leader peptidase catalyzes the release of exported proteins from the outer surface of the Escherichia coli plasma membrane. J. Biol. Chem. 260:15925-15931.
10. Dixon TC, Fadl AA, Koehler TM, Swanson JA, Hanna PC. 2000. Early Bacillus anthracis-macrophage interactions: intracellular survival and escape. Cell. Microbiol. 2:453-463.
11. Duong F, Eichler J, Price A, Leonard MR, Wickner W. 1997. Biogenesis of the gram-negative bacterial envelope. Cell 91:567-573.
12. Economou A, Pogliano JA, Beckwith J, Oliver DB, Wickner W. 1995. SecA membrane cycling at SecYEG is driven by distinct ATP binding and hydrolysis events and is regulated by SecD and SecF. Cell 83:1171-1181.
13. Economou A, Wickner W. 1994. SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78:835-843.
14. Etienne-Toumelin I, Sirard JC, Duflot E, Mock M, Fouet A. 1995. Characterization of the Bacillus anthracis S-layer: cloning and sequencing of the structural gene. J. Bacteriol. 177:614-620.
15. Fagan RP, Fairweather NF. 2011. Clostridium difficile has two parallel and essential Sec secretion systems. J. Biol. Chem. 286:27483-27493.
16. Forsberg LS, et al. 3 May 2012. Localization and structural analysis of a conserved pyruvylated epitope in Bacillus anthracis secondary cell wall polysaccharides and characterization of the galactose deficient wall polysaccharide from avirulent B. anthracis CDC 684. Glycobiology. [Epub ahead of print.] doi:10.1093/glycob/cws080.
17. Fouet A, Mesnage S. 2002. Bacillus anthracis cell envelope components. Curr. Top. Microbiol. Immunol. 271:87-113.
18. Fulford W, Model P. 1984. Specificity of translational regulation by two DNA-binding proteins. J. Mol. Biol. 173:211-226.
19. Gaspar AH, et al. 2005. Bacillus anthracis sortase A (SrtA) anchors LPXTG motif-containing surface proteins to the cell wall envelope. J. Bacteriol. 187:4646-4655.
20. Görlich D, Rapoport TA. 1993. Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane. Cell 75:615-630.
21. Halic M, et al. 2006. Following the signal sequence from ribosomal tunnel exit to signal recognition particle. Nature 444:507-511.
22. Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-572.
23. Ito E, Strominger JL. 1964. Enzymatic synthesis of the peptide in bacterial uridine nucleotides. III. Purification and properties of L-lysine adding enzyme. J. Biol. Chem. 239:210-214.
24. Ito K, Bassford PJJ, Beckwith J. 1981. Protein localization in E. coli: is there a common step in the secretion of periplasmic and outer membrane proteins? Cell 24:707-717.
25. Jensen GB, Hensen BM, Eilenberg J, Mahillon J. 2003. The hidden lifestyles of Bacillus cereus and relatives. Environ. Microbiol. 5:631-640.
26. Kern J, Ryan C, Faull K, Schneewind O. 2010. Bacillus anthracis surfacelayer proteins assemble by binding to the secondary cell wall polysaccharide in a manner that requires csaB and tagO. J. Mol. Biol. 401:757-775.
27. Kern JW, Schneewind O. 2008. BslA, a pXO1-encoded adhesin of Bacillus anthracis. Mol. Microbiol. 68:504-515.
28. Kern JW, Schneewind O. 2009. BslA, the S-layer adhesin of Bacillus anthracis, is a virulence factor for anthrax pathogenesis. Mol. Microbiol. 75:324-332.
29. Kern JW, et al. 2011. Structure of the SLH domains from Bacillus anthracis surface array protein. J. Biol. Chem. 286:26042-26049.
30. Kern VJ, Kern JW, Theriot JA, Schneewind O, Missiakas D. 2012. Surface-layer (S-layer) proteins Sap and EA1 govern the binding of the S-layer-associated protein BslO at the cell septa of Bacillus anthracis. J. Bacteriol. 194:3833-3840.
31. Kim HU, Goepfert JM. 1974. A sporulation medium for Bacillus anthracis. J. Appl. Bacteriol. 37:265-267.
32. Koch R. 1876. DieÄ tiologie der Milzbrand-Krankheit, begründet auf die Entwicklungsgeschichte des Bacillus anthracis. Beitr. Biol. Pflanzen 2:277-310.
33. Kontinen VP, Saris P, Sarvas M. 1991. A gene (prsA) of Bacillus subtilis involved in a novel, late stage of protein export. Mol. Microbiol. 5:1273-1283.
34. Kyte J, Doolittle RF. 1982. A simple method for displaying the hydrophobic character of a protein. J. Mol. Biol. 157:105-132.
35. Lenz LL, Mohammadi S, Geissler A, Portnoy DA. 2003. SecA2-dependent secretion of autolytic enzymes promotes Listeria monocytogenes pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 100:12432-12437.
36. Lenz LL, Portnoy DA. 2002. Identification of a second Listeria secA gene associated with protein secretion and the rough phenotype. Mol. Microbiol. 45:1043-1056.
37. Maresso AW, Chapa TJ, Schneewind O. 2006. Surface protein IsdC and sortase B are required for heme-iron scavenging of Bacillus anthracis. J. Bacteriol. 188:8145-8152.
38. Marraffini LA, Schneewind O. 2007. Sortase C-mediated anchoring ofBasI to the cell wall envelope of Bacillus anthracis. J. Bacteriol. 189:6425-6436.
39. Marraffini LA, Schneewind O. 2006. Targeting proteins to the cell wall of sporulating Bacillus anthracis. Mol. Microbiol. 62:1402-1417.
40. Mesnage S, et al. 2000. Bacterial SLH domain proteins are non-covalently anchored to the cell surface via a conserved mechanism involving wall polysaccharide pyruvylation. EMBO J. 19:4473-4484.
41. Mesnage S, Tosi-Couture E, Fouet A. 1999. Production and cell surface anchoring of functional fusions between the SLH motifs of the Bacillus anthracis S-layer proteins and the Bacillus subtilis levansucrase. Mol. Microbiol. 31:927-936.
42. Mesnage S, Tosi-Couture E, Gounon P, Mock M, Fouet A. 1998. The capsule and S-layer: two independent and yet compatible macromolecular structures in Bacillus anthracis. J. Bacteriol. 180:52-58.
43. Mesnage S, Tosi-Couture E, Mock M, Gounon P, Fouet A. 1997. Molecular characterization of the Bacillus anthracis main S-layer component: evidence that it is the major cell-associated antigen. Mol. Microbiol. 23:1147-1155.
44. Mignot T, Mesnage S, Couture-Tosi E, Mock M, Fouet A. 2002. Developmental switch of S-layer protein synthesis in Bacillus anthracis. Mol. Microbiol. 43:1615-1627.
45. Miller JD, Bernstein HD, Walter P. 1994. Interaction of E. coli Ffh/4.5 Sribonucleoprotein and FtsY mimics that of mammalian signal recognition particle and its receptor. Nature 367:657-659.
46. Okinaka R, et al. 1999. Sequence, assembly and analysis of pX01 and pX02. J. Appl. Microbiol. 87:261-262.
47. Oliver DB, Beckwith J. 1981. E. coli mutant pleiotropically defective in the export of secreted proteins. Cell 25:765-772.
48. Preisz H. 1909. Experimentelle Studien über Virulenz, Empfänglichkeit und Immunität beim Milzbrand. Z. Immunitatsforsch. 5:341-452.
49. Randall LL. 1992. Peptide binding by chaperone SecB: implications for recognition of non-native structure. Science 257:241-245.
50. Ravel J, et al. 2009. The complete genome sequence of Bacillus anthracis Ames "ancestor." J. Bacteriol. 191:445-446.
51. Read TD, et al. 2003. The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature 423:81-86.
52. Richter GS, et al. 2009. Capsule anchoring in Bacillus anthracis occurs by a transpeptidation mechanism that is inhibited by capsidin. Mol. Microbiol. 71:404-420.
53. Rigel NW, Braunstein M. 2008. A new twist on an old pathway-accessory Sec systems. Mol. Microbiol. 69:291-302.
54. Ruthel G, Ribot WJ, Bavari S, Hoover T. 2004. Time-lapse confocal imaging of development of Bacillus anthracis in macrophages. J. Infect. Dis. 189:1313-1316.
55. Sardis MF, Economou A. 2010. SecA: a tale of two protomers. Mol. Microbiol. 76:1070-1081.
56. Schmidt TG, Skerra A. 2007. The Strep-tag system for one-step purification and high affinity detection or capturing of proteins. Nat. Protoc. 2:1528-1535.
57. Seepersaud R, Bensing BA, Yen YT, Sullam PM. 2010. Asp3 mediates multiple protein-protein interactions within the accessory Sec system of Streptococcus gordonii. Mol. Microbiol. 78:490-505.
58. Sibbald MJ, et al. 2006. Mapping the pathways to staphylococcal pathogenesis by comparative secretomics. Microbiol. Mol. Biol. Rev. 70:755-788.
59. Siboo IR, Chaffin DO, Rubens CE, Sullam PM. 2008. Characterization of the accessory Sec system of Staphylococcus aureus. J. Bacteriol. 190:6188-6196.
60. Steck TL, Yu J. 1973. Selective solubilization of proteins from red blood cell membranes by protein perturbants. J. Supramol. Struct. 1:220-232.
61. Sterne M. 1937. Avirulent anthrax vaccine. Onderstepoort J. Vet. Sci. Anim. Ind. 21:41-43.
62. Stoller G, et al. 1995. A ribosome-associated peptidyl-prolyl cis/trans isomerase identified as the trigger factor. EMBO J. 14:4939-4948.
63. Tam C, Glass EM, Anderson DM, Missiakas D. 2006. Transposon mutagenesis of Bacillus anthracis strain Sterne using bursa aurealis. Plasmid 56:74-77.
64. Tarlovsky Y, et al. 2010. A Bacillus anthracis S-layer homology protein that binds heme and mediates heme delivery to IsdC. J. Bacteriol. 192:3503-3511.
65. Vodkin MH, Leppla SH. 1983. Cloning of the protective antigen gene of Bacillus anthracis. Cell 34:693-697.
66. von Heijne G. 1992. Membrane protein structure prediction: hydrophobic analysis and the positive inside rule. J. Mol. Biol. 225:487-494.
67. Wild J, Rossmeissl P, Walter WA, Gross CA. 1996. Involvement of the DnaK-DnaJ-GrpE chaperone team in protein secretion in Escherichia coli. J. Bacteriol. 178:3608-3613.
68. Williams RC, et al. 2003. Production of Bacillus anthracis protective antigen is dependent on extracellular chaperone, PrsA. J. Biol. Chem. 278: 18056-18062.
69. Young JA, Collier JR. 2007. Anthrax toxin: receptor binding, internalization, pore formation and translocation. Annu. Rev. Biochem. 76:243-265.