Probing the applicability of autotransporter based surface display with the EstA autotransporter of Pseudomonas stutzeri A15

Microbial Cell Factories

Volumn 11, Issue , 2012, Pages

  Nicolay, Toon ^a   Lemoine, Lynn ^a   Lievens, Elke ^a   Balzarini, Sam ^a   Vanderleyden, Jos ^a   Spaepen, Stijn ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Autodisplay; Beta barrel; Outer membrane protein; Proteinase K; Secretion; Type V secretion system

Indexed keywords

BETA LACTAMASE; CARRIER PROTEIN; ESTA AUTOTRANSPORTER PROTEIN; PROTEINASE K; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PSEUDOMONAS STUTZERI; PSEUDOMONAS STUTZERI A15; WHOLE CELL;

BACTERIAL PROTEINS; CARBOXYLIC ESTER HYDROLASES; CELL MEMBRANE; GENE EXPRESSION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PSEUDOMONAS STUTZERI;

ESCHERICHIA COLI; NEGIBACTERIA; PSEUDOMONAS STUTZERI;

EID: 84870864144     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/1475-2859-11-158     Document Type: Article

References (53)

1. Economou A, Christie PJ, Fernandez RC, Palmer T, Plano GV, Pugsley AP. Secretion by numbers: Protein traffic in prokaryotes. Mol Microbiol 2006, 62(2):308-319. 10.1111/j.1365-2958.2006.05377.x, 17020575.
2. Abdallah MA, Van Pittius NCG, Champion PAD, Cox J, Luirink J, Vandenbroucke-Grauls CMJE, Appelmelk BJ, Bitter W. Type VII secretion - mycobacteria show the way. Nat Rev Microbiol 2007, 5(11):883-891. 10.1038/nrmicro1773, 17922044.
3. 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.
4. Leyton DL, Rossiter AE, Henderson IR. From self sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis. Nat Rev Microbiol 2012, 10(3):213-225. 10.1038/nrmicro2733, 22337167.
5. Nishimura K, Tajima N, Yoon Y-H, Park S-Y, Tame JRH. Autotransporter passenger proteins: virulence factors with common structural themes. J Mol Med-Jmm 2010, 88(5):451-458.
6. Jose J, Meyer TF. The autodisplay story, from discovery to biotechnical and biomedical applications. Microbiol Mol Biol R 2007, 71(4):600-619.
7. Ko H-J, Park E, Song J, Yang TH, Lee HJ, Kim KH, Choi I-G. Functional cell surface display and controlled secretion of diverse agarolytic enzymes by Escherichia coli with a novel ligation-independent cloning vector based on the autotransporter YfaL. Appl Environ Microbiol 2012, 78(9):3051-3058. 10.1128/AEM.07004-11, 3346495, 22344647.
8. Sevastsyanovich YR, Leyton DL, Wells TJ, Wardius CA, Tveen-Jensen K, Morris FC, Knowles TJ, Cunningham AF, Cole JA, Henderson IR. A generalised module for the selective extracellular accumulation of recombinant proteins. Microb Cell Fact 2012, 11:69. 10.1186/1475-2859-11-69, 3419692, 22640772.
9. Biondo R, da Silva FA, Vicente EJ, Souza Sarkis JE, Schenberg AC. Synthetic phytochelatin surface display in Cupriavidus metallidurans CH34 for enhanced metals bioremediation. Environ Sci Technol 2012, 46(15):8325-8332. 10.1021/es3006207, 22794785.
10. Valls M, Atrian S, de Lorenzo V, Fernandez LA. Engineering a mouse metallothionein on the cell surface of Ralstonia eutropha CH34 for immobilization of heavy metals in soil. Nat Biotechnol 2000, 18(6):661-665. 10.1038/76516, 10835606.
11. Valls M, de Lorenzo V, Gonzalez-Duarte R, Atrian S. Engineering outer-membrane proteins in Pseudomonas putida for enhanced heavy-metal bioadsorption. J Inorg Biochem 2000, 79(1-4):219-223.
12. Jose J, Maas RM, Teese MG. Autodisplay of enzymes-Molecular basis and perspectives. J Biotechnol 2012, 161(2):92-103. 10.1016/j.jbiotec.2012.04.001, 22569038.
13. Garcia-Valdes E, Mulet M, Lalucat J. Insights into the life styles of Pseudomonas stutzeri. Pseudomonas 2010, 177-198. New York: Springer, Ramos JL, Filloux A, 1.
14. Nicolay T, Devleeschouwer K, Vanderleyden J, Spaepen S. Characterization of Esterase A, a Pseudomonas stutzeri A15 autotransporter. Appl Environ Microbiol 2012, 78(8):2533-2542. 10.1128/AEM.07690-11, 3318783, 22307303.
15. van den Berg B. Crystal structure of a full-length autotransporter. J Mol Biol 2011, 396(3):627-633.
16. Wilhelm S, Rosenau F, Kolmar H, Jaeger K-E. Autotransporters with GDSL passenger domains: Molecular physiology and biotechnological applications. ChemBioChem 2011, 12(10):1476-1485. 10.1002/cbic.201100013, 21598370.
17. Yang TH, Pan JG, Seo YS, Rhee JS. Use of Pseudomonas putida EstA as an anchoring motif for display of a periplasmic enzyme on the surface of Escherichia coli. Appl Environ Microbiol 2004, 70(12):6968-6976. 10.1128/AEM.70.12.6968-6976.2004, 535197, 15574889.
18. Yang TH, Kwon M-A, Song JK, Pan JG, Rhee JS. Functional display of Pseudomonas and Burkholderia lipases using a translocator domain of EstA autotransporter on the cell surface of Escherichia coli. J Biotechnol 2010, 146(3):126-129. 10.1016/j.jbiotec.2010.01.022, 20138931.
19. Becker S, Theile S, Heppeler N, Michalczyk A, Wentzel A, Wilhelm S, Jaeger KE, Kolmar H. A generic system for the Escherichia coli cell-surface display of lipolytic enzymes. FEBS Lett 2005, 579(5):1177-1182. 10.1016/j.febslet.2004.12.087, 15710409.
20. Wilhelm S, Rosenau F, Becker S, Buest S, Hausmann S, Kolmar H, Jaeger KE. Functional cell-surface display of a lipase-specific chaperone. ChemBioChem 2007, 8(1):55-60. 10.1002/cbic.200600203, 17173269.
21. Vermeiren H, Willems A, Schoofs G, de Mot R, Keijers V, Hai WL, Vanderleyden J. The rice inoculant strain Alcaligenes faecalis A15 is a nitrogen-fixing Pseudomonas stutzeri. Syst Appl Microbiol 1999, 22(2):215-224. 10.1016/S0723-2020(99)80068-X, 10390872.
22. You CB, Song W, Wang HX, Li JP, Lin M, Hai WL. Associative nitrogen fixation of Alcaligenes faecalis with rice plant. Biol Nitrogen Fix Newsl Sydney Univ 1983, 11:92-103.
23. Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinforma 2008, 9:40.
24. Jong WS, Soprova Z, de Punder K, Ten Hagen-Jongman CM, Wagner S, Wickstrom D, de Gier JW, Andersen P, van der Wel NN, Luirink J. A structurally informed autotransporter platform for efficient heterologous protein secretion and display. Microb Cell Fact 2012, 11(1):85. 10.1186/1475-2859-11-85, 3521207, 22709508.
25. Lum M, Morona R. IcsA autotransporter passenger promotes increased fusion protein expression on the cell surface. Microb Cell Fact 2012, 11:20. 10.1186/1475-2859-11-20, 3298707, 22309506.
26. Marin E, Bodelon G, Fernandez LA. Comparative analysis of the biochemical and functional properties of C-terminal domains of autotransporters. J Bacteriol 2010, 192(21):5588-5602. 10.1128/JB.00432-10, 2953703, 20802036.
27. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Meth 2011, 8(10):785-786.
28. Kjaergaard K, Hasman H, Schembri MA, Klemm P. Antigen 43-mediated autotransporter display, a versatile bacterial cell surface presentation system. J Bacteriol 2002, 184(15):4197-4204. 10.1128/JB.184.15.4197-4204.2002, 135209, 12107137.
29. Schultheiss E, Paar C, Schwab H, Jose J. Functional esterase surface display by the autotransporter pathway in Escherichia coli. J Mol Catal B: Enzym 2002, 18(1-3):89-97.
30. Schultheiss E, Weiss S, Winterer E, Maas R, Heinzle E, Jose J. Esterase autodisplay: Enzyme engineering and whole-cell activity determination in microplates with pH sensors. Appl Environ Microbiol 2008, 74(15):4782-4791. 10.1128/AEM.01575-07, 2519334, 18515492.
31. Leyton DL, Sevastsyanovich YR, Browning DF, Rossiter AE, Wells TJ, Fitzpatrick RE, Overduin M, Cunningham AF, Henderson IR. Size and conformation limits to secretion of disulfide-bonded loops in autotransporter proteins. J Biol Chem 2011, 286(49):42283-42291. 10.1074/jbc.M111.306118, 3234927, 22006918.
32. Jong WSP, ten Hagen-Jongman CM, den Blaauwen T, Slotboom DJ, Tame JRH, Wickstrom D, de Gier J-W, Otto BR, Luirink J. Limited tolerance towards folded elements during secretion of the autotransporter Hbp. Mol Microbiol 2007, 63(5):1524-1536. 10.1111/j.1365-2958.2007.05605.x, 17302825.
33. Shu X, Shaner NC, Yarbrough CA, Tsien RY, Remington SJ. Novel chromophores and buried charges control color in mFruits. Biochemistry US 2006, 45(32):9639-9647.
34. Yang F, Moss LG, Phillips GN. The molecular structure of green fluorescent protein. Nat Biotechnol 1996, 14(10):1246-1251. 10.1038/nbt1096-1246, 9631087.
35. Rekas A, Alattia J-R, Nagai T, Miyawaki A, Ikura M. Crystal structure of venus, a yellow fluorescent protein with improved maturation and reduced environmental sensitivity. J Biol Chem 2002, 277(52):50573-50578. 10.1074/jbc.M209524200, 12370172.
36. Kim MH, Choi W-C, Kang HO, Lee JS, Kang BS, Kim K-J, Derewenda ZS, Oh T-K, Lee CH, Lee J-K. The molecular structure and catalytic mechanism of a quorum-quenching N-acyl-L-homoserine lactone hydrolase. P Natl Acad Sci USA 2005, 102(49):17606-17611.
37. Jelsch C, Mourey L, Masson JM, Samama JP. Crystal structure of Escherichia coli TEM1 beta-lactamase at 1.8 A resolution. Proteins 1993, 16(4):364-383. 10.1002/prot.340160406, 8356032.
38. Lattemann CT, Maurer J, Gerland E, Meyer TF. Autodisplay: Functional display of active beta-lactamase on the surface of Escherichia coli by the AIDA-I autotransporter. J Bacteriol 2000, 182(13):3726-3733. 10.1128/JB.182.13.3726-3733.2000, 94543, 10850987.
39. Klauser T, Kramer J, Otzelberger K, Pohlner J, Meyer TF. Characterization of the Neisseria IgA(beta) core: The essential unit for outer-membrane targeting and extracellular protein secretion. J Mol Biol 1993, 234(3):579-593. 10.1006/jmbi.1993.1613, 8254661.
40. Suzuki T, Lett MC, Sasakawa C. Extracellular transport of VirG protein in Shigella. J Biol Chem 1995, 270(52):30874-30880. 10.1074/jbc.270.52.30874, 8537341.
41. Maurer J, Jose J, Meyer TF. Characterization of the essential transport function of the AIDA-I autotransporter and evidence supporting structural predictions. J Bacteriol 1999, 181(22):7014-7020. 94176, 10559167.
42. Oliver DC, Huang G, Fernandez RC. Identification of secretion determinants of the Bordetella pertussis BrkA autotransporter. J Bacteriol 2003, 185(2):489-495. 10.1128/JB.185.2.489-495.2003, 145336, 12511495.
43. St Geme JW, Cutter D. The Haemophilus influenzae Hia adhesin is an autotransporter protein that remains uncleaved at the C terminus and fully cell associated. J Bacteriol 2000, 182(21):6005-6013. 10.1128/JB.182.21.6005-6013.2000, 94733, 11029419.
44. Van Gerven N, Sleutel M, Deboeck F, De Greve H, Hernalsteens JP. Surface display of the receptor-binding domain of the F17a-G fimbrial adhesin through the autotransporter AIDA-I leads to permeability of bacterial cells. Microbiol-Sgm 2009, 155:468-476.
45. Binder U, Matschiner G, Theobald I, Skerra A. High-throughput sorting of an anticalin library via EspP-mediated functional display on the Escherichia coli cell surface. J Mol Biol 2010, 400(4):783-802. 10.1016/j.jmb.2010.05.049, 20630471.
46. Jose J, Kramer J, Klauser T, Pohlner J, Meyer TF. Absence of periplasmic DsbA oxidoreductase facilitates export of cysteine-containing passenger proteins to the Escherichia coli cell surface via the IgA(beta) autotransporter pathway. Gene 1996, 178(1-2):107-110.
47. Klauser T, Pohlner J, Meyer TF. Extracellular transport of Cholera-toxin B-subunit using Neisseria IgA protease beta-domain: Conformation-dependent outer-membrane translocation. EMBO J 1990, 9(6):1991-1999. 551908, 2189728.
48. Klauser T, Pohlner J, Meyer TF. Selective extracellular release of Cholera toxin-B subunit by Escherichia coli: Dissection of Neisseria IgA-beta-mediated outer-membrane transport. EMBO J 1992, 11(6):2327-2335. 556700, 1600950.
49. Veiga E, de Lorenzo V, Fernandez LA. Structural tolerance of bacterial autotransporters for folded passenger protein domains. Mol Microbiol 2004, 52(4):1069-1080. 10.1111/j.1365-2958.2004.04014.x, 15130125.
50. Skillman KM, Barnard TJ, Peterson JH, Ghirlando R, Bernstein HD. Efficient secretion of a folded protein domain by a monomeric bacterial autotransporter. Mol Microbiol 2005, 58(4):945-958. 10.1111/j.1365-2958.2005.04885.x, 16262782.
51. Rutherford N, Charbonneau ME, Berthiaume F, Betton JM, Mourez M. The periplasmic folding of a cysteineless autotransporter passenger domain interferes with its outer membrane translocation. J Bacteriol 2006, 188(11):4111-4116. 10.1128/JB.01949-05, 1482886, 16707702.
52. Renn JP, Junker M, Besingi RN, Braselmann E, Clark PL. ATP-independent control of autotransporter virulence protein transport via the folding properties of the secreted protein. Chem Biol 2012, 19(2):287-296. 10.1016/j.chembiol.2011.11.009, 22209629.
53. Qiu DR, Damron FH, Mima T, Schweizer HP, Yu HD. P-BAD-based shuttle vectors for functional analysis of toxic and highly regulated genes in Pseudomonas and Burkholderia spp. and other bacteria. Appl Environ Microbiol 2008, 74(23):7422-7426. 10.1128/AEM.01369-08, 2592904, 18849445.