Mechanical forces regulate the reactivity of a thioester bond in a bacterial adhesin

Journal of Biological Chemistry

Volumn 292, Issue 21, 2017, Pages 8988-8997

  Echelman, Daniel J ^a   Lee, Alex Q ^a   Fernández, Julio M ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MOLECULES;

BACTERIAL ADHESION; COMPLEMENT SYSTEMS; MECHANICAL FORCE; POTENTIAL SUBSTRATE; PROTEOLYTIC CLEAVAGE; SINGLE-MOLECULE ASSAYS; STREPTOCOCCUS PYOGENES; STRUCTURAL STUDIES;

LIGANDS;

ADHESIN; HISTAMINE; METHYLAMINE; NUCLEOPHILE; THIOESTER; DISULFIDE;

ATOMIC FORCE MICROSCOPY; BACTERIUM ADHERENCE; BACTERIUM PILUS; CONTROLLED STUDY; COVALENT BOND; LIGAND BINDING; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN UNFOLDING; REVIEW; STREPTOCOCCUS PYOGENES; THIOESTER DOMAIN; CHEMISTRY; PROTEIN FOLDING;

ADHESINS, BACTERIAL; DISULFIDES; HISTAMINE; METHYLAMINES; PROTEIN FOLDING; STREPTOCOCCUS PYOGENES;

EID: 85019684904     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M117.777466     Document Type: Review

References (43)

1. Scheffner, M., Nuber, U., and Huibregtse, J. M. (1995) Protein ubiquitination involving an e1-e2-e3 enzyme ubiquitin thioester cascade. Nature 373, 81-83
2. Bhaumik, P., Koski, M. K., Glumoff, T., Hiltunen, J. K., and Wierenga, R. K. (2005) Structural biology of the thioester-dependent degradation and synthesis of fatty acids. Curr. Opin. Struct. Biol. 15, 621-628
3. Mitchell, C. A., Shi, C., Aldrich, C. C., and Gulick, A. M. (2012) Structure of pa1221, a nonribosomal peptide synthetase containing adenylation and peptidyl carrier protein domains. Biochemistry 51, 3252-3263
4. Garcia-Ferrer, I., Arêde, P., Gómez-Blanco, J., Luque, D., Duquerroy, S., Castón, J. R., Goulas, T., and Gomis-Rüth, F. X. (2015) Structural and functional insights into Escherichia coli α2-macroglobulin endopeptidase snap-trap inhibition. Proc. Natl. Acad. Sci. U.S.A. 112, 8290-8295
5. Law, S. K., and Dodds, A. W. (1997) The internal thioester and the covalent binding properties of the complement proteins c3 and c4. Protein Sci. 6, 263-274
6. Wong, S. G., and Dessen, A. (2014) Structure of a bacterialα2-macroglobulin reveals mimicry of eukaryotic innate immunity. Nat. Commun. 5, 4917
7. Dodds, A. W., Ren, X. D., Willis, A. C., and Law, S. K. (1996) The reaction mechanism of the internal thioester in the human complement component c4. Nature 379, 177-179
8. Sim, R. B., Twose, T. M., Paterson, D. S., and Sim, E. (1981) The covalentbinding reaction of complement component c3. Biochem. J. 193, 115-127
9. Linke-Winnebeck, C., Paterson, N. G., Young, P. G., Middleditch, M. J., Greenwood, D. R., Witte, G., and Baker, E. N. (2014) Structural model for covalent adhesion of the Streptococcus pyogenes pilus through a thioester bond. J. Biol. Chem. 289, 177-189
10. Pointon, J. A., Smith, W. D., Saalbach, G., Crow, A., Kehoe, M. A., and Banfield, M. J. (2010) A highly unusual thioester bond in a pilus adhesin is required for efficient host cell interaction. J. Biol. Chem. 285, 33858-33866
11. Walden, M., Edwards, J. M., Dziewulska, A. M., Bergmann, R., Saalbach, G., Kan, S. Y., Miller, O. K., Weckener, M., Jackson, R. J., Shirran, S. L., Botting, C. H., Florence, G. J., Rohde, M., Banfield, M. J., and Schwarz-Linek, U. (2015) An internal thioester in a pathogen surface protein mediates covalent host binding. Elife 4, 10.7554/eLife.06638
12. Rivas-Pardo, J. A., Eckels, E. C., Popa, I., Kosuri, P., Linke, W. A., and Fernández, J. M. (2016) Work done by titin protein folding assists muscle contraction. Cell Rep. 14, 1339-1347
13. Möller, J., Lühmann, T., Chabria, M., Hall, H., and Vogel, V. (2013) Macrophages lift off surface-bound bacteria using a filopodium-lamellipodium hook-and-shovel mechanism. Sci. Rep. 3, 2884
14. Johnson, C. P., Tang, H. Y., Carag, C., Speicher, D. W., and Discher, D. E. (2007) Forced unfolding of proteins within cells. Science 317, 663-666
15. Alegre-Cebollada, J., Kosuri, P., Giganti, D., Eckels, E., Rivas-Pardo, J. A., Hamdani, N., Warren, C. M., Solaro, R. J., Linke, W. A., and Fernández, J. M. (2014) S-Glutathionylation of cryptic cysteines enhances titin elasticity by blocking protein folding. Cell 156, 1235-1246
16. Echelman, D. J., Alegre-Cebollada, J., Badilla, C. L., Chang, C., Ton-That, H., and Fernández, J. M. (2016) CnaA domains in bacterial pili are efficient dissipaters of large mechanical shocks. Proc. Natl. Acad. Sci. U.S.A. 113, 2490-2495
17. Baker, E. N., Squire, C. J., and Young, P. G. (2015) Self-generated covalent cross-links in the cell-surface adhesins of Gram-positive bacteria. Biochem. Soc. Trans. 43, 787-794
18. Reardon-Robinson, M. E., and Ton-That, H. (2015) Disulfide-bond-forming pathways in Gram-positive bacteria. J. Bacteriol. 198, 746-754
19. Ainavarapu, S. R., Brujic, J., Huang, H. H., Wiita, A. P., Lu, H., Li, L., Walther, K. A., Carrion-Vazquez, M., Li, H., and Fernandez, J. M. (2007) Contour length and refolding rate of a small protein controlled by engineered disulfide bonds. Biophys. J. 92, 225-233
20. Smith, W. D., Pointon, J. A., Abbot, E., Kang, H. J., Baker, E. N., Hirst, B. H., Wilson, J. A., Banfield, M. J., and Kehoe, M. A. (2010) Roles of minor pilin subunits spy0125 and spy0130 in the serotype m1 Streptococcus pyogenes strain sf370. J. Bacteriol. 192, 4651-4659
21. Alegre-Cebollada, J., Badilla, C. L., and Fernández, J. M. (2010) Isopeptide bonds block the mechanical extension of pili in pathogenic Streptococcus pyogenes. J. Biol. Chem. 285, 11235-11242
22. Peng, Q., and Li, H. (2009) Domain insertion effectively regulates the mechanical unfolding hierarchy of elastomeric proteins: toward engineering multifunctional elastomeric proteins. J. Am. Chem. Soc. 131, 14050-14056
23. Pangburn, M. K. (1992) Spontaneous reformation of the intramolecular thioester in complement protein c3 and low temperature capture of a conformational intermediate capable of reformation. J. Biol. Chem. 267, 8584-8590
24. Wiita, A. P., Ainavarapu, S. R., Huang, H. H., and Fernandez, J. M. (2006) Force-dependent chemical kinetics of disulfide bond reduction observed with single-molecule techniques. Proc. Natl. Acad. Sci. U.S.A. 103, 7222-7227
25. Oberhauser, A. F., Hansma, P. K., Carrion-Vazquez, M., and Fernandez, J. M. (2001) Stepwise unfolding of titin under force-clamp atomic force microscopy. Proc. Natl. Acad. Sci. U.S.A. 98, 468-472
26. Schlierf, M., Li, H., and Fernandez, J. M. (2004) The unfolding kinetics of ubiquitin captured with single-molecule force-clamp techniques. Proc. Natl. Acad. Sci. U.S.A. 101, 7299-7304
27. Mitchell, S. C., and Zhang, A. Q. (2001) Methylamine in human urine. Clin. Chim. Acta 312, 107-114
28. Kahn, T. B., Fernández, J. M., and Perez-Jimenez, R. (2015) Monitoring oxidative folding of a single protein catalyzed by the disulfide oxidoreductase dsba. J. Biol. Chem. 290, 14518-14527
29. Popa, I., Rivas-Pardo, J. A., Eckels, E. C., Echelman, D. J., Badilla, C. L., Valle-Orero, J., and Fernández, J. M. (2016) A halotag anchored ruler for week-long studies of protein dynamics. J. Am. Chem. Soc. 138, 10546-10553
30. Nilsson, B., and Nilsson Ekdahl, K. (2012) The tick-over theory revisited: is c3 a contact-activated protein? Immunobiology 217, 1106-1110
31. Nishida, N., Walz, T., and Springer, T. A. (2006) Structural transitions of complement component c3 and its activation products. Proc. Natl. Acad. Sci. U.S.A. 103, 19737-19742
32. Khan, S. A., Sekulski, J. M., and Erickson, B. W. (1986) Peptide models of protein metastable binding sites: competitive kinetics of isomerization and hydrolysis. Biochemistry 25, 5165-5171
33. Janssen, B. J., Huizinga, E. G., Raaijmakers, H. C., Roos, A., Daha, M. R., Nilsson-Ekdahl, K., Nilsson, B., and Gros, P. (2005) Structures of complement component c3 provide insights into the function and evolution of immunity. Nature 437, 505-511
34. Prussin, C., and Metcalfe, D. D. (2003) IgE, mast cells, basophils, and eosinophils. J. Allergy Clin. Immunol. 111, S486-S494
35. Stone, K. D., Prussin, C., and Metcalfe, D. D. (2010) Ige, mast cells, basophils, and eosinophils. J. Allergy Clin. Immunol. 125, S73-S80
36. Schwartz, D. J., Kalas, V., Pinkner, J. S., Chen, S. L., Spaulding, C. N., Dodson, K. W., and Hultgren, S. J. (2013) Positively selected fimh residues enhance virulence during urinary tract infection by altering fimh conformation. Proc. Natl. Acad. Sci. U.S.A. 110, 15530-15537
37. Sauer, M. M., Jakob, R. P., Eras, J., Baday, S., Eriş, D., Navarra, G., Bernèche, S., Ernst, B., Maier, T., and Glockshuber, R. (2016) Catch-bond mechanism of the bacterial adhesin fimh. Nat. Commun. 7, 10738
38. George, N. P., Wei, Q., Shin, P. K., Konstantopoulos, K., and Ross, J. M. (2006) Staphylococcus aureus adhesion via spa, clfa, and sdrcde to immo-bilized platelets demonstrates shear-dependent behavior. Arterioscler. Thromb. Vasc. Biol. 26, 2394-2400
39. Ding, A. M., Palmer, R. J., Jr., Cisar, J. O., and Kolenbrander, P. E. (2010) Shear-enhanced oral microbial adhesion. Appl. Environ. Microbiol. 76, 1294-1297
40. Carrion-Vazquez, M., Oberhauser, A. F., Fowler, S. B., Marszalek, P. E., Broedel, S. E., Clarke, J., and Fernandez, J. M. (1999) Mechanical and chemical unfolding of a single protein: a comparison. Proc. Natl. Acad. Sci. U.S.A. 96, 3694-3699
41. Popa, I., Kosuri, P., Alegre-Cebollada, J., Garcia-Manyes, S., and Fernandez, J. M. (2013) Force dependency of biochemical reactions measured by single-molecule force-clamp spectroscopy. Nat. Protoc. 8, 1261-1276
42. Florin, E. L., Rief, M., Lehmann, H., Ludwig, M., Dornmair, C., Moy, V. T., and Gaub, H. E. (1995) Sensing specific molecular interactions with the atomic force microscope. Biosens. Bioelectron. 10, 895-901
43. Bustamante, C., Marko, J. F., Siggia, E. D., and Smith, S. (1994) Entropic elasticity of λ-phage DNA. Science 265, 1599-1600