Engineering the Salmonella type III secretion system to export spider silk monomers

Molecular Systems Biology

Volumn 5, Issue , 2009, Pages

  Widmaier, Daniel M ^a   Tullman Ercek, Danielle ^a   Mirsky, Ethan A ^a   Hill, Rena ^a   Govindarajan, Sridhar ^b   Minshull, Jeremy ^b   Voigt, Christopher A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b DNA20 Inc   (United States)

Author keywords

Automated DNA synthesis; Biomaterials; Cellular engineering; Genetic parts; Systems biology

Indexed keywords

CHAPERONE; MONOMER; SYNTHETIC DNA; BACTERIAL PROTEIN; FIBROIN; HYBRID PROTEIN; MEMBRANE PROTEIN; SPI 2 PROTEIN, SALMONELLA; SPI-2 PROTEIN, SALMONELLA; SPI1 PROTEIN, SALMONELLA;

AMINO TERMINAL SEQUENCE; ARTICLE; CODON USAGE; CONTROLLED STUDY; DNA SYNTHESIS; GENETIC CODE; GENETIC STABILITY; GENETIC TRANSCRIPTION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN SECRETION; SALMONELLA; SERICULTURE; SPIDER; TYPE III SECRETION SYSTEM; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; GENETICS; HUMAN; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN TRANSPORT; SECRETION; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

ARANEAE; HARNESS; NEGIBACTERIA; SALMONELLA;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; FIBROINS; HUMANS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN ENGINEERING; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SALMONELLA; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SPIDERS;

EID: 70349303484     PISSN: 17444292     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2009.62     Document Type: Article

References (85)

1. Akeda Y, Galan JE (2005) Chaperone release and unfolding of substrates in type III secretion. Nature 437: 911-915
2. Altier C (2005) Genetic and environmental control of Salmonella invasion. J Microbiol 43: 85-92
3. Arcidiacono S, Mello C, Kaplan D, Cheley S, Bayley H (1998) Purification and characterization of recombinant spider silk expressed in Escherichia coli. Appl Microbiol Biotechnol 49: 31-38
4. Bajaj V, Lucas RL, Hwang C, Lee CA (1996) Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol Microbiol 22: 703-714
5. Bayer TS, Widmaier DM, Temme K, Mirsky EA, Santi DV, Voigt CA (2009) Synthesis of methyl halides from biomass using engineered microbes. J Am Chem Soc 131: 6508-6515
6. Bendtsen JD, Nielsen H, Widdick D, Palmer T, Brunak S (2005) Prediction of twin-arginine signal peptides. BMC Bioinformatics 6: 167
7. Berks BC (1996) A common export pathway for proteins binding complex redox cofactors? Mol Microbiol 22: 393-404
8. Boyd AP, Grosdent N, Totemeyer S, Geuijen C, Bleves S, Iriartes M, Lambermont I, Octave JN, Cornelis GR (2000) Yersinia enterocolitica can deliver Yop proteins into a wide range of cell types: Development of a delivery system for heterologous proteins. Eur J Cell Biol 79: 659-671
9. Bronstein PA, Miao EA, Miller SI (2000) InvB is a type III secretion chaperone specific for SspA. J Bacteriol 182: 6638-6644
10. Chen LM, Briones G, Donis RO, Galan JE (2006) Optimization of the delivery of heterologous proteins by the Salmonella enterica serovar Typhimurium type III secretion system for vaccine development. Infect Immun 74: 5826-5833
11. Choi JH, Lee SY (2004) Secretory and extracellular production of recombinant proteins using Escherichia coli. Appl Microbiol Biotechnol 64: 625-635
12. Collazo CM, Galan JE (1996) Requirement for exported proteins in secretion through the invasion-associated type III system of Salmonella typhimurium. Infect Immun 64: 3524-3531
13. Darwin KH, Miller VL (1999) InvF is required for expression of genes encoding proteins secreted by the SPI1 type III secretion apparatus in Salmonella typhimurium. J Bacteriol 181: 4949-4954
14. Darwin KH, Miller VL (2000) The putative invasion protein chaperone SicA acts together with InvF to activate the expression of Salmonella typhimurium virulence genes. Mol Microbiol 35: 949-960
15. Darwin KH, Miller VL (2001) Type III secretion chaperone-dependent regulation: activation of virulence genes by SicA and InvF in Salmonella typhimurium. EMBO J 20: 1850-1862
16. DeLisa MP, Tullman D, Georgiou G (2003) Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc Natl Acad Sci USA 100: 6115-6120
17. Economou A, Wickner W (1994) Seca promotes preprotein translocation by undergoing Atp-driven cycles of membrane insertion and deinsertion. Cell 78: 835-843
18. Ehrbar K, Friebel A, Miller SI, Hardt WD (2003) Role of the Salmonella pathogenicity island 1 (SPI-1) protein InvB in type III secretion of SopE and SopE2, two Salmonella effector proteins encoded outside of SPI-1. J Bacteriol 185: 6950-6967
19. Eichelberg K, Galan JE (1999) Differential regulation of Salmonella typhimurium type III secreted proteins by pathogenicity island 1 (SPI-1)-encoded transcriptional activators InvF and hilA. Infect Immun 67: 4099-4105
20. Ellermeier CD, Ellermeier JR, Slauch JM (2005) HilD, HilC and RtsA constitute a feed forward loop that controls expression of the SPI1 type three secretion system regulator hilA in Salmonella enterica serovar Typhimurium. Mol Microbiol 57: 691-705
21. Enninga J, Mounier J, Sansonetti P, Tran Van Nhieu G (2005) Secretion of type III effectors into host cells in real time. Nat Methods 2: 959-965
22. Fahnestock SR, Irwin SL (1997) Synthetic spider dragline silk proteins and their production in Escherichia coli. Appl Microbiol Biotechnol 47: 23-32
23. Feldman MF, Muller S, Wuest E, Cornelis GR (2002) SycE allows secretion of YopE-DHFR hybrids by the Yersinia enterocolitica type III Ysc system. Mol Microbiol 46: 1183-1197
24. Fu Y, Galan JE (1998) Identification of a specific chaperone for SptP, a substrate of the centisome 63 type III secretion system of Salmonella typhimurium. J Bacteriol 180: 3393-3399
25. Fu Z, Hamid SB, Razak CN, Basri M, Salleh AB, Rahman RN (2003) Secretory expression in Escherichia coli and single-step purification of a heat-stable alkaline protease. Protein Expr Purif 28: 63-68
26. Galan JE, Collmer A (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284: 1322-1328
27. Georgiou G, Segatori L (2005) Preparative expression of secreted proteins in bacteria: status report and future prospects. Curr Opin Biotechnol 16: 538-545
28. Gerchman Y, Weiss R (2004) Teaching bacteria a new language. Proc Natl Acad Sci USA 101: 2221-2222
29. Gosline JM, Guerette PA, Ortlepp CS, Savage KN (1999) The mechanical design of spider silks: from fibroin sequence to mechanical function. J Exp Biol 202: 3295-3303
30. Guerette PA, Ginzinger DG, Weber BH, Gosline JM (1996) Silk properties determined by gland-specific expression of a spider fibroin gene family. Science 272: 112-115
31. Gustafsson C, Govindarajan S, Minshull J (2004) Codon bias and heterologous protein expression. Trends Biotechnol 22: 346-353
32. Harvey BR, Georgiou G, Hayhurst A, Jeong KJ, Iverson BL, Rogers GK (2004) Anchored periplasmic expression, a versatile technology for the isolation of high-affinity antibodies from Escherichia coli-expressed libraries. Proc Natl Acad Sci USA 101: 9193-9198
33. Higashide W, Zhou D (2006) The first 45 amino acids of SopA are necessary for InvB binding and SPI-1 secretion. J Bacteriol 188: 2411-2420
34. Hofmann S, Hagenmuller H, Koch AM, Muller R, Vunjak-Novakovic G, Kaplan DL, Merkle HP, Meinel L (2007) Control of in vitro tissue-engineered bone-like structures using human mesenchymal stem cells and porous silk scaffolds. Biomaterials 28: 1152-1162
35. Hong KH, Miller VL (1998) Identification of a novel Salmonella invasion locus homologous to Shigella ipgDE. J Bacteriol 180: 1793-1802
36. Huemmerich D, Helsen CW, Quedzuweit S, Oschmann J, Rudolph R, Scheibel T (2004a) Primary structure elements of spider dragline silks and their contribution to protein solubility. Biochemistry 43: 13604-13612
37. Huemmerich D, Scheibel T, Vollrath F, Cohen S, Gat U, Ittah S (2004b) Novel assembly properties of recombinant spider dragline silk proteins. Curr Biol 14: 2070-2074
38. Hussain NK, Jenna S, Glogauer M, Quinn CC, Wasiak S, Guipponi M, Antonarakis SE, Kay BK, Stossel TP, Lamarche-Vane N, McPherson PS (2001) Endocytic protein intersectin-l regulates actin assembly via Cdc42 and N-WASP. Nat Cell Biol 3: 927-932
39. Kalir S, McClure J, Pabbaraju K, Southward C, Ronen M, Leibler S, Surette MG, Alon U (2001) Ordering genes in a flagella pathway by analysis of expression kinetics from living bacteria. Science 292: 2080-2083
40. Karavolos MH, Roe AJ, Wilson M, Henderson J, Lee JJ, Gally DL, Khan CM (2005) Type III secretion of the Salmonella effector protein SopE is mediated via an N-terminal amino acid signal and not an mRNA sequence. J Bacteriol 187: 1559-1567
41. Kluge JA, Rabotyagova U, Leisk GG, Kaplan DL (2008) Spider silks and their applications. Trends Biotechnol 26: 244-251
42. Knodler LA, Bertero M, Yip C, Strynadka NC, Steele-Mortimer O (2006) Structure-based mutagenesis of SigE verifies the importance of hydrophobic and electrostatic residues in type III chaperone function. Mol Microbiol 62: 928-940
43. Konjufca V, Wanda SY, Jenkins MC, Curtiss III R (2006) A recombinant attenuated Salmonella enterica serovar Typhimurium vaccine encoding Eimeria acervulina antigen offers protection against E acervulina challenge. Infect Immun 74: 6785-6796
44. Kubori T, Galan JE (2002) Salmonella type III secretion-associated protein InvE controls translocation of effector proteins into host cells. J Bacteriol 184: 4699-4708
45. Kubori T, Matsushima Y, Nakamura D, Uralil J, Lara-Tejero M, Sukhan A, Galan JE, Aizawa SI (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280: 602-605
46. Lazaris A, Arcidiacono S, Huang Y, Zhou JF, Duguay F, Chretien N, Welsh EA, Soares JW, Karatzas CN (2002) Spider silk fibers spun from soluble recombinant silk produced in mammalian cells. rffrt Science 295: 472-476
47. Lee PA, Tullman-Ercek D, Georgiou G (2006) The bacterial twin-arginine translocation pathway. Annu Rev Microbiol 60: 373-395
48. Lee SH, Galan JE (2004) Salmonella type III secretion-associated chaperones confer secretion-pathway specificity. Mol Microbiol 51: 483-495
49. Lee SM, Pippel E, Gosele U, Dresbach C, Qin Y, Chandran CV, Brauniger T, Hause G, Knez M (2009) Greatly increased toughness of infiltrated spider silk. Science 324: 488-492
50. Lee VT, Schneewind O (2002) Yop fusions to tightly folded protein domains and their effects on Yersinia enterocolitica type III secretion. J Bacteriol 184: 3740-3745
51. Lewis RV (2006) Spider silk: ancient ideas for new biomaterials. Chem Rev 106: 3762-3774
52. Lucas RL, Lee CA (2000) Unravelling the mysteries of virulence gene regulation in Salmonella typhimurium. Mol Microbiol 36: 1024-1033
53. Lucic MR, Forbes BE, Grosvenor SE, Carr JM, Wallace JC, Forsberg G (1998) Secretion in Escherichia coli and phage-display of recombinant insulin-like growth factor binding protein-2. J Biotechnol 61: 95-108
54. Lundberg U, Vinatzer U, Berdnik D, von Gabain A, Baccarini M (1999) Growth phase-regulated induction of Salmonella-induced macrophage apoptosis correlates with transient expression of SPI-1 genes. J Bacteriol 181: 3433-3437
55. Majander K, Anton L, Antikainen J, Lang H, Brummer M, Korhonen TK, Westerlund-Wikstrom B (2005) Extracellular secretion of polypeptides using a modified Escherichia coli flagellar secretion apparatus. Nat Biotechnol 23: 475-481
56. Marlovits TC, Kubori T, Lara-Tejero M, Thomas D, Unger VM, Galan JE (2006) Assembly of the inner rod determines needle length in the type III secretion injectisome. Nature 441: 637-640
57. Marlovits TC, Kubori T, Sukhan A, Thomas DR, Galan JE, Unger VM (2004) Structural insights into the assembly of the type III secretion needle complex. Science 306: 1040-1042
58. Nielsen H, Engelbrecht J, Brunak S, vonHeijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10: 1-6
59. Pohlschroder M, Hartmann E, Hand NJ, Dilks K, Haddad A (2005) Diversity and evolution of protein translocation. Annu Rev Microbiol 59: 91-111
60. Prince JT, McGrath KP, DiGirolamo CM, Kaplan DL (1995) Construction, cloning, and expression of synthetic genes encoding spider dragline silk. Biochemistry 34: 10879-10885
61. Rising A, Nimmervoll H, Grip S, Fernandez-Arias A, Storckenfeldt E, Knight DP, Vollrath F, Engstrom W (2005) Spider silk proteins-mechanical property and gene sequence. Zoolog Sci 22: 273-281
62. Rodrigue A, Chanal A, Beck K, Muller M, Wu LF (1999) Co-translocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial Tat pathway. J Biol Chem 274: 13223-13228
63. Russmann H, Kubori T, Sauer J, Galan JE (2002) Molecular and functional analysis of the type III secretion signal of the Salmonella enterica InvJ protein. Mol Microbiol 46: 769-779
64. Russmann H, Shams H, Poblete F, Fu Y, Galan JE, Donis RO (1998) Delivery of epitopes by the Salmonella type III secretion system for vaccine development. Science 281: 565-568 (Pubitemid 28357372)
65. Sargent F, Bogsch EG, Stanley NR, Wexler M, Robinson C, Berks BC, Palmer T (1998) Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J 17: 3640-3650
66. Schlumberger MC, Muller AJ, Ehrbar K, Winnen B, Duss I, Stecher B, Hardt WD (2005) Real-time imaging of type III secretion: Salmonella SipA injection into host cells. Proc Natl Acad Sci USA 102: 12548-12553
67. Seidel A, Liivak O, Calve S, Adaska J, Ji G, Yang Z, Grubb D, Zax D, Jelinski L (2000) Regenerated spider silk: processing, properties and structure. Macromolecules 33: 775-780
68. Somerville C (2007) Biofuels. Curr Biol 17: R115-R119 Sorensen HP, Mortensen KK (2005) Advanced genetic strategies for recombinant protein expression in Escherichia coli. J Biotechnol 115: 113-128
69. Stebbins CE, Galan JE (2001) Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414: 77-81
70. Swanson BO, Blackledge TA, Summers AP, Hayashi CY (2006) Spider dragline silk: correlated and mosaic evolution in high-performance biological materials. Evolution 60: 2539-2551
71. Tartera C, Metcalf ES (1993) Osmolarity and growth-phase overlap in regulation of Salmonella typhi adherence to and invasion of human intestinal cells. Infect Immun 61: 3084-3089
72. Temme K, Salis H, Tullman-Ercek D, Levskaya A, Hong SH, Voigt CA (2008) Induction and relaxation dynamics of the regulatory network controlling the type III secretion system encoded within Salmonella pathogenicity island 1. J Mol Biol 377: 47-61
73. Tong L, Lin Q, Wong WK, Ali A, Lim D, Sung WL, Hew CL, Yang DS (2000) Extracellular expression, purification, and characterization of a winter flounder antifreeze polypeptide from Escherichia coli. Protein Expr Purif 18: 175-181
74. Tucker SC, Galan JE (2000) Complex function for SicA, a Salmonella enterica serovar typhimurium type III secretion-associated chaperone. J Bacteriol 182: 2262-2268
75. Vegh BM, Gal P, Dobo J, Zavodszky P, Vonderviszt F (2006) Localization of the flagellum-specific secretion signal in Salmonella flagellin. Biochem Biophys Res Commun 345: 93-98
76. Vendrely C, Scheibel T (2007) Biotechnological production of spider-silk proteins enables new applications. Macromol Biosci 7: 401-409
77. Vollrath F, Knight DP (2001) Liquid crystalline spinning of spider silk. Nature 410: 541-548
78. Wang Y, Blasioli DJ, Kim HJ, Kim HS, Kaplan DL (2006a) Cartilage tissue engineering with silk scaffolds and human articular chondrocytes. Biomaterials 27: 4434-4442
79. Wang Y, Kim HJ, Vunjak-Novakovic G, Kaplan DL (2006b) Stem cell-based tissue engineering with silk biomaterials. Biomaterials 27: 6064-6082
80. Wickner W, Schekman R (2005) Protein translocation across biological membranes. Science 310: 1452-1456
81. Wittrup KD (2000) The single cell as a microplate well. Nat Biotechnol 18: 1039-1040
82. Wood MW, Williams C, Upadhyay A, Gill AC, Philippe DL, Galyov EE, van den Elsen JM, Bagby S (2004) Structural analysis of Salmonella enterica effector protein SopD. Biochim Biophys Acta 1698: 219-226
83. Zhang S, Santos RL, Tsolis RM, Stender S, Hardt WD, Baumler AJ, Adams LG (2002) The Salmonella enterica serotype typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infect Immun 70: 3843-3855
84. Zhang YHP, Himmel ME, Mielenz JR (2006) Outlook for cellulase improvement: screening and selection strategies. Biotechnol Adv 24: 452-481
85. Zhou SD, Yomano LP, Saleh AZ, Davis FC, Aldrich HC, Ingram LO (1999) Enhancement of expression and apparent secretion of Erwinia chrysanthemi endoglucanase (encoded by celZ) in Escherichia coli B. Appl Environ Microbiol 65: 2439-2445