Two distinct regions in the model protein Peb1 are critical for its heterologous transport out of Escherichia coli

Microbial Cell Factories

Volumn 9, Issue , 2010, Pages

  Anton, Lena ^a   Majander, Katariina ^a   Savilahti, Harri ^b   Laakkonen, Liisa ^a   Westerlund Wikström, Benita ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; ESCHERICHIA COLI PROTEIN; PEPTIDASE 2; PROTEIN PEB 1; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; PEB1 PROTEIN, CAMPYLOBACTER; RECOMBINANT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL SECRETION SYSTEM; BACTERIAL STRAIN; BIOINFORMATICS; CELL MEMBRANE; CYTOPLASM; ESCHERICHIA COLI; FLAGELLUM; NONHUMAN; OUTER MEMBRANE; PLASMID; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTAGENESIS; PROTEIN TERTIARY STRUCTURE; SECRETION; TRANSPORT AT THE CELLULAR LEVEL;

CAMPYLOBACTER JEJUNI; ESCHERICHIA COLI;

AMINO ACID SEQUENCE; ANTIGENS, BACTERIAL; BIOLOGICAL TRANSPORT; ESCHERICHIA COLI; FLAGELLA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PERIPLASM; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS;

EID: 78649536917     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/1475-2859-9-97     Document Type: Article

References (66)

1. Gerlach RG, Hensel M. Protein secretion systems and adhesins: the molecular armory of Gram-negative pathogens. Int J Med Microbiol 2007, 297(6):401-415. 10.1016/j.ijmm.2007.03.017, 17482513.
2. Saier MH. Protein secretion and membrane insertion systems in gram-negative bacteria. J Membr Biol 2006, 214(2):75-90. 10.1007/s00232-006-0049-7, 17546510.
3. Cegelski L, Marshall GR, Eldridge GR, Hultgren SJ. The biology and future prospects of antivirulence therapies. Nat Rev Microbiol 2008, 6(1):17-27. 10.1038/nrmicro1818, 2211378, 18079741.
4. Ni Y, Chen R. Extracellular recombinant protein production from Escherichia coli. Biotechnol Lett 2009, 31(11):1661-1670. 10.1007/s10529-009-0077-3, 19597765.
5. Mergulhao FJ, Summers DK, Monteiro GA. Recombinant protein secretion in Escherichia coli. Biotechnol Adv 2005, 23(3):177-202. 10.1016/j.biotechadv.2004.11.003, 15763404.
6. Desvaux M, Hebraud M, Talon R, Henderson IR. Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue. Trends Microbiol 2009, 17(4):139-145. 10.1016/j.tim.2009.01.004, 19299134.
7. Oldham ML, Khare D, Quiocho FA, Davidson AL, Chen J. Crystal structure of a catalytic intermediate of the maltose transporter. Nature 2007, 450(7169):515-521. 10.1038/nature06264, 18033289.
8. Tsukazaki T, Mori H, Fukai S, Ishitani R, Mori T, Dohmae N, Perederina A, Sugita Y, Vassylyev DG, Ito K, Nureki O. Conformational transition of Sec machinery inferred from bacterial SecYE structures. Nature 2008, 455(7215):988-991. 10.1038/nature07421, 2590585, 18923527.
9. Yeo HJ, Waksman G. Unveiling molecular scaffolds of the type IV secretion system. J Bacteriol 2004, 186(7):1919-1926. 10.1128/JB.186.7.1919-1926.2004, 374423, 15028675.
10. Backert S, Meyer TF. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr Opin Microbiol 2006, 9(2):207-217. 10.1016/j.mib.2006.02.008, 16529981.
11. Cianciotto NP. Type II secretion: a protein secretion system for all seasons. Trends Microbiol 2005, 13(12):581-588. 10.1016/j.tim.2005.09.005, 16216510.
12. Dautin N, Bernstein HD. Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu Rev Microbiol 2007, 61:89-112. 10.1146/annurev.micro.61.080706.093233, 17506669.
13. Holland IB, Schmitt L, Young J. Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway (review). Mol Membr Biol 2005, 22(1-2):29-39. 10.1080/09687860500042013, 16092522.
14. Cornelis GR. The type III secretion injectisome. Nat Rev Microbiol 2006, 4(11):811-825. 10.1038/nrmicro1526, 17041629.
15. Dawson RJ, Hollenstein K, Locher KP. Uptake or extrusion: crystal structures of full ABC transporters suggest a common mechanism. Mol Microbiol 2007, 65(2):250-257. 10.1111/j.1365-2958.2007.05792.x, 17578454.
16. Pei ZH, Ellison RT, Blaser MJ. Identification, purification, and characterization of major antigenic proteins of Campylobacter jejuni. J Biol Chem 1991, 266(25):16363-16369.
17. Pei Z, Burucoa C, Grignon B, Baqar S, Huang XZ, Kopecko DJ, Bourgeois AL, Fauchere JL, Blaser MJ. Mutation in the peb1A locus of Campylobacter jejuni reduces interactions with epithelial cells and intestinal colonization of mice. Infect Immun 1998, 66(3):938-943. 107999, 9488379.
18. Kervella M, Pages JM, Pei Z, Grollier G, Blaser MJ, Fauchere JL. Isolation and characterization of two Campylobacter glycine-extracted proteins that bind to HeLa cell membranes. Infect Immun 1993, 61(8):3440-3448. 281021, 8335374.
19. Leon-Kempis Mdel R, Guccione E, Mulholland F, Williamson MP, Kelly DJ. The Campylobacter jejuni PEB1a adhesin is an aspartate/glutamate-binding protein of an ABC transporter essential for microaerobic growth on dicarboxylic amino acids. Mol Microbiol 2006, 60(5):1262-1275. 10.1111/j.1365-2958.2006.05168.x, 16689801.
20. Pei Z, Blaser MJ. PEB1, the major cell-binding factor of Campylobacter jejuni, is a homolog of the binding component in gram-negative nutrient transport systems. J Biol Chem 1993, 268(25):18717-18725.
21. Majander K, Anton L, Antikainen J, Lang H, Brummer M, Korhonen TK, Westerlund-Wikstrom B. Extracellular secretion of polypeptides using a modified Escherichia coli flagellar secretion apparatus. Nat Biotechnol 2005, 23(4):475-481. 10.1038/nbt1077, 15806100.
22. Chevance FF, Hughes KT. Coordinating assembly of a bacterial macromolecular machine. Nat Rev Microbiol 2008, 6(6):455-465. 10.1038/nrmicro1887, 18483484.
23. Hughes KT, Gillen KL, Semon MJ, Karlinsey JE. Sensing structural intermediates in bacterial flagellar assembly by export of a negative regulator. Science 1993, 262(5137):1277-1280. 10.1126/science.8235660, 8235660.
24. Oliver DB, Cabelli RJ, Dolan KM, Jarosik GP. Azide-resistant mutants of Escherichia coli alter the SecA protein, an azide-sensitive component of the protein export machinery. Proc Natl Acad Sci USA 1990, 87(21):8227-8231. 10.1073/pnas.87.21.8227, 54928, 2146683.
25. Galan JE, Wolf-Watz H. Protein delivery into eukaryotic cells by type III secretion machines. Nature 2006, 444(7119):567-573. 10.1038/nature05272, 17136086.
26. SignalP Website. , http://www.cbs.dtu.dk/services/SignalP/
27. TatP Website. , http://www.cbs.dtu.dk/services/TatP/
28. Type-III effector prediction Website. , http://www.effectors.org/
29. LipoP 1.0 Website. , http://www.cbs.dtu.dk/services/LipoP/
30. SecretomeP Website. , http://www.cbs.dtu.dk/services/SecretomeP/
31. Hu P, Janga SC, Babu M, Diaz-Mejia JJ, Butland G, Yang W, Pogoutse O, Guo X, Phanse S, Wong P, Chandran S, Christopoulos C, Nazarians-Armavil A, Nasseri NK, Musso G, Ali M, Nazemof N, Eroukova V, Golshani A, Paccanaro A, Greenblatt JF, Moreno-Hagelsieb G, Emili A. Global functional atlas of Escherichia coli encompassing previously uncharacterized proteins. PLoS Biol 2009, 7(4):e96. 10.1371/journal.pbio.1000096, 2672614, 19402753.
32. Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y. The complete genome sequence of Escherichia coli K-12. Science 1997, 277(5331):1453-1474. 10.1126/science.277.5331.1453, 9278503.
33. BioCyc Website. , http://www.biocyc.org/ECOLI/
34. KEGG Database Website. , http://www.genome.jp/kegg-bin/show_pathway?org_name=eco&mapno=03070&mapscale=1.0
35. Sargent F, Stanley NR, Berks BC, Palmer T. Sec-independent protein translocation in Escherichia coli. A distinct and pivotal role for the TatB protein. J Biol Chem 1999, 274(51):36073-36082. 10.1074/jbc.274.51.36073, 10593889.
36. Journet L, Hughes KT, Cornelis GR. Type III secretion: a secretory pathway serving both motility and virulence (review). Mol Membr Biol 2005, 22(1-2):41-50. 10.1080/09687860500041858, 16092523.
37. Westermark M, Oscarsson J, Mizunoe Y, Urbonaviciene J, Uhlin BE. Silencing and activation of ClyA cytotoxin expression in Escherichia coli. J Bacteriol 2000, 182(22):6347-6357. 10.1128/JB.182.22.6347-6357.2000, 94780, 11053378.
38. Francetic O, Belin D, Badaut C, Pugsley AP. Expression of the endogenous type II secretion pathway in Escherichia coli leads to chitinase secretion. EMBO J 2000, 19(24):6697-6703. 10.1093/emboj/19.24.6697, 305903, 11118204.
39. Ren CP, Chaudhuri RR, Fivian A, Bailey CM, Antonio M, Barnes WM, Pallen MJ. The ETT2 gene cluster, encoding a second type III secretion system from Escherichia coli, is present in the majority of strains but has undergone widespread mutational attrition. J Bacteriol 2004, 186(11):3547-3560. 10.1128/JB.186.11.3547-3560.2004, 415751, 15150243.
40. Ren CP, Beatson SA, Parkhill J, Pallen MJ. The Flag-2 locus, an ancestral gene cluster, is potentially associated with a novel flagellar system from Escherichia coli. J Bacteriol 2005, 187(4):1430-1440. 10.1128/JB.187.4.1430-1440.2005, 545627, 15687208.
41. Sauvonnet N, Gounon P, Pugsley AP. PpdD type IV pilin of Escherichia coli K-12 can Be assembled into pili in Pseudomonas aeruginosa. J Bacteriol 2000, 182(3):848-854. 10.1128/JB.182.3.848-854.2000, 94355, 10633126.
42. van der Woude MW, Henderson IR. Regulation and function of Ag43 (flu). Annu Rev Microbiol 2008, 62:153-169. 10.1146/annurev.micro.62.081307.162938, 18785838.
43. Shrivastava S, Mande SS. Identification and functional characterization of gene components of Type VI Secretion system in bacterial genomes. PLoS One 2008, 3(8):e2955. 10.1371/journal.pone.0002955, 2492809, 18698408.
44. Blomfield IC, McClain MS, Eisenstein BI. Type 1 fimbriae mutants of Escherichia coli K12: characterization of recognized afimbriate strains and construction of new fim deletion mutants. Mol Microbiol 1991, 5(6):1439-1445. 10.1111/j.1365-2958.1991.tb00790.x, 1686292.
45. Barnhart MM, Chapman MR. Curli biogenesis and function. Annu Rev Microbiol 2006, 60:131-147. 10.1146/annurev.micro.60.080805.142106, 2838481, 16704339.
46. Hsiao CD, Sun YJ, Rose J, Wang BC. The crystal structure of glutamine-binding protein from Escherichia coli. J Mol Biol 1996, 262(2):225-242. 10.1006/jmbi.1996.0509, 8831790.
47. Yao N, Trakhanov S, Quiocho FA. Refined 1.89-A structure of the histidine-binding protein complexed with histidine and its relationship with many other active transport/chemosensory proteins. Biochemistry 1994, 33(16):4769-4779. 10.1021/bi00182a004, 8161536.
48. Hu Y, Fan CP, Fu G, Zhu D, Jin Q, Wang DC. Crystal structure of a glutamate/aspartate binding protein complexed with a glutamate molecule: structural basis of ligand specificity at atomic resolution. J Mol Biol 2008, 382(1):99-111. 10.1016/j.jmb.2008.06.091, 18640128.
49. Wai SN, Lindmark B, Soderblom T, Takade A, Westermark M, Oscarsson J, Jass J, Richter-Dahlfors A, Mizunoe Y, Uhlin BE. Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 2003, 115(1):25-35. 10.1016/S0092-8674(03)00754-2, 14532000.
50. Bendtsen JD, Kiemer L, Fausboll A, Brunak S. Non-classical protein secretion in bacteria. BMC Microbiol 2005, 5:58. 10.1186/1471-2180-5-58, 1266369, 16212653.
51. Bendtsen JD, Wooldridge KG. Non-classical Secretion. Bacterial secreted proteins: secretory mechanisms and role in pathogenesis 2009, 225-235. Norfolk, UK: Caister Academic Press, Wooldridge KG.
52. Jeffery CJ. Moonlighting proteins: old proteins learning new tricks. Trends Genet 2003, 19(8):415-417. 10.1016/S0168-9525(03)00167-7, 12902157.
53. Xia XX, Han MJ, Lee SY, Yoo JS. Comparison of the extracellular proteomes of Escherichia coli B and K-12 strains during high cell density cultivation. Proteomics 2008, 8(10):2089-2103. 10.1002/pmic.200700826, 18425732.
54. Sambrook J, Russell DW. Molecular cloning: a laboratory manual 2001, Cold Spring Harbor, New York, USA: CSHL Press, 3.
55. Donnenberg MS, Kaper JB. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 1991, 59(12):4310-4317. 259042, 1937792.
56. Majander K, Korhonen TK, Westerlund-Wikstrom B. Simultaneous display of multiple foreign peptides in the FliD capping and FliC filament proteins of the Escherichia coli flagellum. Appl Environ Microbiol 2005, 71(8):4263-4268. 10.1128/AEM.71.8.4263-4268.2005, 1183357, 16085812.
57. Genbank Website. , http://www.ncbi.nlm.nih.gov/Genbank/
58. Hienonen E, Romantschuk M, Fenel F, Taira S. Transcript stabilization by mRNA sequences from hrpA of Pseudomonas syringae. J Biotechnol 2007, 128(2):258-267. 10.1016/j.jbiotec.2006.10.010, 17125870.
59. Haapa S, Taira S, Heikkinen E, Savilahti H. An efficient and accurate integration of mini-Mu transposons in vitro: a general methodology for functional genetic analysis and molecular biology applications. Nucleic Acids Res 1999, 27(13):2777-2784. 10.1093/nar/27.13.2777, 148488, 10373596.
60. Poussu E, Vihinen M, Paulin L, Savilahti H. Probing the alpha-complementing domain of E. coli beta-galactosidase with use of an insertional pentapeptide mutagenesis strategy based on Mu in vitro DNA transposition. Proteins 2004, 54(4):681-692. 10.1002/prot.10467, 14997564.
61. Taira S, Tuimala J, Roine E, Nurmiaho-Lassila EL, Savilahti H, Romantschuk M. Mutational analysis of the Pseudomonas syringae pv. tomato hrpA gene encoding Hrp pilus subunit. Mol Microbiol 1999, 34(4):737-744. 10.1046/j.1365-2958.1999.01635.x, 10564513.
62. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph 1996, 14(1):33-8. 27-8, 10.1016/0263-7855(96)00018-5, 8744570.
63. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and Clustal × version 2.0. Bioinformatics 2007, 23(21):2947-2948. 10.1093/bioinformatics/btm404, 17846036.
64. Fraczkiewicz R, Braun W. Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules. J Comp Chem 1998, 19(3):319-333.
65. Protein Data Bank Website. , http://www.rcsb.org/pdb/
66. Grant SG, Jessee J, Bloom FR, Hanahan D. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci USA 1990, 87(12):4645-4649. 10.1073/pnas.87.12.4645, 54173, 2162051.