Charge-dependent secretion of an intrinsically disordered protein via the autotransporter pathway

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 45, 2013, Pages

  Kang'ethe, Wanyoike ^a   Bernstein, Harris D ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Bacterial pathogenesis; Membrane protein assembly; Type Va secretion

Indexed keywords

ADENYLATE CYCLASE TOXIN; AMINO ACID; CALCIUM; CHIMERIC PROTEIN; POLYPEPTIDE;

ARTICLE; BORDETELLA PERTUSSIS; CONFORMATION; ESCHERICHIA COLI O157; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; RECEPTOR BINDING;

BACTERIAL PATHOGENESIS; MEMBRANE PROTEIN ASSEMBLY; TYPE VA SECRETION;

ADENYLATE CYCLASE TOXIN; BACTERIAL SECRETION SYSTEMS; BORDETELLA PERTUSSIS; COMPUTATIONAL BIOLOGY; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; KINETICS; MEMBRANE TRANSPORT PROTEINS; OLIGONUCLEOTIDES; PLASMIDS; PROTEIN CONFORMATION; PROTEIN FOLDING; SERINE ENDOPEPTIDASES;

EID: 84887306808     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1310345110     Document Type: Article

References (62)

1. Leyton DL, Rossiter AE, Henderson IR (2012) From self sufficiency to dependence: Mechanisms and factors important for autotransporter biogenesis. Nat Rev Microbiol 10(3):213-225.
2. Junker M, et al. (2006) Pertactin β-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc Natl Acad Sci USA 103(13):4918-4923.
3. Oomen CJ, et al. (2004) Structure of the translocator domain of a bacterial autotransporter. EMBO J 23(6):1257-1266.
4. Barnard TJ, Dautin N, Lukacik P, Bernstein HD, Buchanan SK (2007) Autotransporter structure reveals intra-barrel cleavage followed by conformational changes. Nat Struct Mol Biol 14(12):1214-1220.
5. van den Berg B (2010) Crystal structure of a full-length autotransporter. J Mol Biol 396(3):627-633.
6. Ruiz-Perez F, et al. (2009) Roles of periplasmic chaperone proteins in the biogenesis of serine protease autotransporters of Enterobacteriaceae. J Bacteriol 191(21): 6571-6583.
7. Ieva R, Bernstein HD (2009) Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc Natl Acad Sci USA 106(45):19120-19125.
8. Ieva R, Tian P, Peterson JH, Bernstein HD (2011) Sequential and spatially restricted interactions of assembly factors with an autotransporter β domain. Proc Natl Acad Sci USA 108(31):E383-E391.
9. Sauri A, et al. (2009) The Bam (Omp85) complex is involved in secretion of the autotransporter haemoglobin protease. Microbiology 155(Pt 12):3982-3991.
10. Voulhoux R, Bos MP, Geurtsen J, Mols M, Tommassen J (2003) Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299(5604): 262-265.
11. Wu T, et al. (2005) Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121(2):235-245.
12. Hagan CL, Kim S, Kahne D (2010) Reconstitution of outer membrane protein assembly from purified components. Science 328(5980):890-892.
13. Dautin N, Bernstein HD (2007) Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu Rev Microbiol 61:89-112.
14. Junker M, Besingi RN, Clark PL (2009) Vectorial transport and folding of an autotransporter virulence protein during outer membrane secretion. Mol Microbiol 71(5): 1323-1332.
15. Pohlner J, Halter R, Beyreuther K, Meyer TF (1987) Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325(6103):458-462.
16. Skillman KM, Barnard TJ, Peterson JH, Ghirlando R, Bernstein HD (2005) Efficient secretion of a folded protein domain by a monomeric bacterial autotransporter. Mol Microbiol 58(4):945-958.
17. Jong WS, et al. (2007) Limited tolerance towards folded elements during secretion of the autotransporter Hbp. Mol Microbiol 63(5):1524-1536.
18. Ieva R, Skillman KM, Bernstein HD (2008) Incorporation of a polypeptide segment into the β-domain pore during the assembly of a bacterial autotransporter. Mol Microbiol 67(1):188-201.
19. Peterson JH, Tian P, Ieva R, Dautin N, Bernstein HD (2010) Secretion of a bacterial virulence factor is driven by the folding of a C-terminal segment. Proc Natl Acad Sci USA 107(41):17739-17744.
20. Saurí A, et al. (2011) Autotransporter β-domains have a specific function in protein secretion beyond outer-membrane targeting. J Mol Biol 412(4):553-567.
21. Pavlova O, Peterson JH, Ieva R, Bernstein HD (2013) Mechanistic link between β barrel assembly and the initiation of autotransporter secretion. Proc Natl Acad Sci USA 110(10):E938-E947.
22. Klauser T, Pohlner J, Meyer TF (1992) Selective extracellular release of cholera toxin B subunit by Escherichia coli: Dissection of Neisseria Igaβ-mediated outer membrane transport. EMBO J 11(6):2327-2335.
23. Renn JP, Junker M, Besingi RN, Braselmann E, Clark PL (2012) ATP-independent control of autotransporter virulence protein transport via the folding properties of the secreted protein. Chem Biol 19(2):287-296.
24. Alder NN, Theg SM (2003) Energetics of protein transport across biological membranes. A study of the thylakoid DeltapH-dependent/cpTat pathway. Cell 112(2): 231-242.
25. Driessen AJ (1992) Precursor protein translocation by the Escherichia coli translocase is directed by the protonmotive force. EMBO J 11(3):847-853.
26. Shi LX, Theg SM (2013) Energetic cost of protein import across the envelope membranes of chloroplasts. Proc Natl Acad Sci USA 110(3):930-935.
27. Lattman EE, Rose GD (1993) Protein folding-What's the question? Proc Natl Acad Sci USA 90(2):439-441.
28. Glaser P, Sakamoto H, Bellalou J, Ullmann A, Danchin A (1988) Secretion of cyclolysin, the calmodulin-sensitive adenylate cyclase-haemolysin bifunctional protein of Bordetella pertussis. EMBO J 7(12):3997-4004.
29. Rose T, Sebo P, Bellalou J, Ladant D (1995) Interaction of calcium with Bordetella pertussis adenylate cyclase toxin. Characterization of multiple calcium-binding sites and calcium-induced conformational changes. J Biol Chem 270(44):26370-26376.
30. Chenal A, et al. (2010) Calcium-induced folding and stabilization of the intrinsically disordered RTX domain of the CyaA toxin. Biophys J 99(11):3744-3753.
31. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6(3):197-208.
32. Chenal A, Guijarro JI, Raynal B, Delepierre M, Ladant D (2009) RTX calcium binding motifs are intrinsically disordered in the absence of calcium: Implication for protein secretion. J Biol Chem 284(3):1781-1789.
33. Baumann U, Wu S, Flaherty KM, McKay DB (1993) Three-dimensional structure of the alkaline protease of Pseudomonas aeruginosa: A two-domain protein with a calcium binding parallel beta roll motif. EMBO J 12(9):3357-3364.
34. Iwaki M, Ullmann A, Sebo P (1995) Identification by in vitro complementation of regions required for cell-invasive activity of Bordetella pertussis adenylate cyclase toxin. Mol Microbiol 17(6):1015-1024.
35. Bejerano M, Nisan I, Ludwig A, Goebel W, Hanski E (1999) Characterization of the Cterminal domain essential for toxic activity of adenylate cyclase toxin. Mol Microbiol 31(1):381-392.
36. Bauche C, et al. (2006) Structural and functional characterization of an essential RTX subdomain of Bordetella pertussis adenylate cyclase toxin. J Biol Chem 281(25): 16914-16926.
37. Dautin N, Barnard TJ, Anderson DE, Bernstein HD (2007) Cleavage of a bacterial autotransporter by an evolutionarily convergent autocatalytic mechanism. EMBO J 26(7): 1942-1952.
38. Barnard TJ, et al. (2012) Molecular basis for the activation of a catalytic asparagine residue in a self-cleaving bacterial autotransporter. J Mol Biol 415(1):128-142.
39. Blenner MA, Shur O, Szilvay GR, Cropek DM, Banta S (2010) Calcium-induced folding of a beta roll motif requires C-terminal entropic stabilization. J Mol Biol 400(2): 244-256.
40. Sotomayor Pérez AC, et al. (2010) Characterization of the regions involved in the calcium-induced folding of the intrinsically disordered RTX motifs from the bordetella pertussis adenylate cyclase toxin. J Mol Biol 397(2):534-549.
41. Hewlett EL, Gordon VM, McCaffery JD, Sutherland WM, Gray MC (1989) Adenylate cyclase toxin from Bordetella pertussis. Identification and purification of the holotoxin molecule. J Biol Chem 264(32):19379-19384.
42. Vojtova-Vodolanova J, et al. (2009) Oligomerization is involved in pore formation by Bordetella adenylate cyclase toxin. FASEB J 23(9):2831-2843.
43. Rutherford N, Charbonneau ME, Berthiaume F, Betton JM, Mourez M (2006) The periplasmic folding of a cysteineless autotransporter passenger domain interferes with its outer membrane translocation. J Bacteriol 188(11):4111-4116.
44. Celik N, et al. (2012) A bioinformatic strategy for the detection, classification and analysis of bacterial autotransporters. PLoS ONE 7(8):e43245.
45. Petsko GA, Ringe D (2003) Protein Structure and Function (Sinauer, Sunderland, MA).
46. Kumar S, Nussinov R (1999) Salt bridge stability in monomeric proteins. J Mol Biol 293(5): 1241-1255.
47. Spahich NA, Hood DW, Moxon ER, St Geme JW III (2012) Inactivation of Haemophilus influenzae lipopolysaccharide biosynthesis genes interferes with outer membrane localization of the hap autotransporter. J Bacteriol 194(7):1815-1822.
48. Teh MY, Tran EN, Morona R (2012) Absence of O antigen suppresses Shigella flexneri IcsA autochaperone region mutations. Microbiology 158(Pt 11):2835-2850.
49. Heijne G (1986) The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans-membrane topology. EMBO J 5(11): 3021-3027.
50. Krishtalik LI, Cramer WA (1995) On the physical basis for the cis-positive rule describing protein orientation in biological membranes. FEBS Lett 369(2-3):140-143.
51. Geibel S, Procko E, Hultgren SJ, Baker D, Waksman G (2013) Structural and energetic basis of folded-protein transport by the FimD usher. Nature 496(7444):243-246.
52. Selkrig J, et al. (2012) Discovery of an archetypal protein transport system in bacterial outer membranes. Nat Struct Mol Biol 19(5):506-510, S1.
53. Leyton DL, et al. (2011) Size and conformation limits to secretion of disulfide-bonded loops in autotransporter proteins. J Biol Chem 286(49):42283-42291.
54. Saurí A, Ten Hagen-Jongman CM, van Ulsen P, Luirink J (2012) Estimating the size of the active translocation pore of an autotransporter. J Mol Biol 416(3):335-345.
55. Akiyama Y, Ito K (1990) SecY protein, a membrane-embedded secretion factor of E. coli, is cleaved by the ompT protease in vitro. Biochem Biophys Res Commun 167(2): 711-715.
56. Szabady RL, Peterson JH, Skillman KM, Bernstein HD (2005) An unusual signal peptide facilitates late steps in the biogenesis of a bacterial autotransporter. Proc Natl Acad Sci USA 102(1):221-226.
57. Amann E, Ochs B, Abel KJ (1988) Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene 69(2):301-315.
58. Cardona ST, Valvano MA (2005) An expression vector containing a rhamnoseinducible promoter provides tightly regulated gene expression in Burkholderia cenocepacia. Plasmid 54(3):219-228.
59. Ulbrandt ND, Newitt JA, Bernstein HD (1997) The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell 88(2):187-196.
60. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat Methods 8(10):785-786.
61. Bryson K, Cozzetto D, Jones DT (2007) Computer-assisted protein domain boundary prediction using the DomPred server. Curr Protein Pept Sci 8(2):181-188.
62. Kelley LA, Sternberg MJ (2009) Protein structure prediction on the Web: A case study using the Phyre server. Nat Protoc 4(3):363-371.