Abstract
Abstract Extracellular adhesins frequently compose large, highly-ordered structural assemblies that project away from the bacterial surface. These assemblies, known as pili or fimbriae, are rod-like polymeric structures that in some cases can extend up to several micrometers from the cell surface. Because these adhesin structures are critical to bacterial colonization of host cell surfaces, there is an incentive to understand their structure, assembly and mechanism of host cell attachment. Various methods in Nuclear Magnetic Resonance (NMR) spectroscopy have been used to address these topics, yielding structural information at the atomic level. Also, new methods in solid-state NMR spectroscopy have thus far been under-utilized in the study of large adhesin structures and offer a powerful approach to overcoming problems with crystallization to better understand the structures of these complexes. The following is a brief overview of the contributions of NMR to the study of bacterial adhesins with an emphasis on the future potential of solid-state NMR.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Alphonse S, Durand E, Douzi B, Waegele B, Darbon H, Filloux A, Voulhoux R, Bernard C (2009) Structure of the Pseudomonas aeruginosa XcpT pseudopilin, a major component of the type II secretion system. J Struct Biol 169:75–80
Anderson KL, Billington J, Pettigrew D, Cota E, Simpson P, Roversi P, Chen HA, Urvil P, du Merle L, Barlow PN, Medof ME, Smith RA, Nowicki B, Le Bouguénec C, Lea SM, Matthews S (2004) An atomic resolution model for assembly, architecture, and function of the Dr adhesins. Mol Cell 15:647–657
Audette GF, Irvin RT, Hazes B (2004) Crystallographic analysis of the Pseudomonas aeruginosa strain K122-4 monomeric pilin reveals a conserved receptor-binding architecture. Biochemistry 43:11427–11435
Balguerie A, Dos Reis S, Ritter C, Chaignepain S, Coulary-Salin B, Forge V, Bathany K, Lascu I, Schmitter JM, Riek R, Saupe SJ (2003) Domain organization and structure-function relationship of the HET-s prion protein of Podospora anserina. EMBO J 22:2071–2081
Barnhart MM, Pinkner JS, Soto GE, Sauer FG, Langermann S, Waksman G, Frieden C, Hultgren SJ (2000) PapD-like chaperones provide the missing information for folding of pilin proteins. Proc Natl Acad Sci USA 97:7709–7714
Batchelor M, Prasannan S, Daniell S, Reece S, Connerton I, Bloomberg G, Dougan G, Frankel G, Matthews S (2000) Structural basis for recognition of the translocated intimin receptor (Tir) by intimin from enteropathogenic Escherichia coli. EMBO J 19:2452–2464
Baxa U, Wickner RB, Steven AC, Anderson DE, Marekov LN, Yau WM, Tycko R (2007) Characterization of β-sheet structure in Ure2p1-89 yeast prion fibrils by solid-state nuclear magnetic resonance. Biochemistry 46:13149–13162
Castellani F, van Rossum BJ, Diehl A, Rehbein K, Oschkinat H (2003) Determination of solid-state NMR structures of proteins by means of three-dimensional 15N-13C-13C dipolar correlation spectroscopy and chemical shift analysis. Biochemistry 42:11476–11483
Castellani F, van Rossum B, Diehl A, Schubert M, Rehbein K, Oschkinat H (2002) Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy. Nature 420: 98–102
Choudhury D, Thompson A, Stojanoff V, Langermann S, Pinkner J, Hultgren SJ, Knight SD (1999) X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science 285:1061–1066
Cota E, Jones C, Simpson P, Altroff H, Anderson KL, du Merle L, Guignot J, Servin A, Le Bouguénec C, Mardon H, Matthews S (2006) The solution structure of the invasive tip complex from Afa/Dr fibrils. Mol Microbiol 62:356–366
Coustou V, Deleu C, Saupe S, Begueret J (1997) The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog. Proc Natl Acad Sci USA 94:9773–9778
Craig L, Taylor RK, Pique ME, Adair BD, Arvai AS, Singh M, Lloyd SJ, Shin DS, Getzoff ED, Yeager M, Forest KT, Tainer JA (2003) Type IV pilin structure and assembly: x-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol Cell 11:1139–1150
Epstein EA, Chapman MR (2008) Polymerizing the fibre between bacteria and host cells: the biogenesis of functional amyloid fibres. Cell Microbiol 10:1413–1420
Forest KT (2005) Structure and assembly of type IV pilins. In: Waksman G, Caparon M, Hultgren S (eds) Structural biology of bacterial pathogenesis. ASM Press, Washington, DC, pp 81–100
Fowler DM, Koulov AV, Balch WE, Kelly JW (2007) Functional amyloid – from bacteria to humans. Trends Biochem Sci 32:217–224
Franks WT, Zhou DH, Wylie BJ, Money BG, Graesser DT, Frericks HL, Sahota G, Rienstra CM (2005) Magic-angle spinning solid-state NMR spectroscopy of the beta1 immunoglobulin binding domain of protein G (GB1): 15N and 13C chemical shift assignments and conformational analysis. J Am Chem Soc 127:12291–12305
Golovanov AP, Balasingham S, Tzitzilonis C, Goult BT, Lian LY, Homberset H, Tonjum T, Derrick JP (2006a) Assignment of 1H, 13C, and 15N resonances for the PilP pilot protein from Neisseria meningitidis. J Biomol NMR 36(Suppl 1):68
Golovanov AP, Balasingham S, Tzitzilonis C, Goult BT, Lian LY, Homberset H, Tonjum T, Derrick JP (2006b) The solution structure of a domain from the Neisseria meningitidis lipoprotein PilP reveals a new β-sandwich fold. J Mol Biol 364: 186–195
Gossert AD, Bettendorff P, Puorger C, Vetsch M, Herrmann T, Glockshuber R, Wüthrich K (2008) NMR structure of the Escherichia coli type 1 pilus subunit FimF and its interactions with other pilus subunits. J Mol Biol 375:752–763
Gossert AD, Hiller S, Fiorito F, Wüthrich K (2007) NMR assignment of the E. coli type 1 pilus protein FimF. J Biomol NMR 38:195
Hammer ND, Schmidt JC, Chapman MR (2007) The curli nucleator protein, CsgB, contains an amyloidogenic domain that directs CsgA polymerization. Proc Natl Acad Sci USA 104: 12494–12499
Hazes B, Sastry PA, Hayakawa K, Read RJ, Irvin RT (2000) Crystal structure of Pseudomonas aeruginosa PAK pilin suggests a main-chain-dominated mode of receptor binding. J Mol Biol 299:1005–1017
Hedenstrom M, Emtenäs H, Pemberton N, Aberg V, Hultgren SJ, Pinkner JS, Tegman V, Almqvist F, Sethson I, Kihlberg J (2005) NMR studies of interactions between periplasmic chaperones from uropathogenic E. coli and pilicides that interfere with chaperone function and pilus assembly. Org Biomol Chem 3:4193–4200
Keizer DW, Slupsky CM, Kalisiak M, Campbell AP, Crump MP, Sastry PA, Hazes B, Irvin RT, Sykes BD (2001) Structure of a pilin monomer from Pseudomonas aeruginosa: implications for the assembly of pili. J Biol Chem 276:24186–24193
Kelly G, Prasannan S, Daniell S, Fleming K, Frankel G, Dougan G, Connerton I, Matthews S (1999) Structure of the cell-adhesion fragment of intimin from enteropathogenic Escherichia coli. Nat Struct Biol 6:313–318
Korotkova N, Cota E, Lebedin Y, Monpouet S, Guignot J, Servin AL, Matthews S, Moseley SL (2006) A subfamily of Dr adhesins of Escherichia coli bind independently to decay-accelerating factor and the N-domain of carcinoembryonic antigen. J Biol Chem 281:29120–29130
Korotkova N, Yang Y, Le Trong I, Cota E, Demeler B, Marchant J, Thomas WE, Stenkamp RE, Moseley SL, Matthews S (2008) Binding of Dr adhesins of Escherichia coli to carcinoembryonic antigen triggers receptor dissociation. Mol Microbiol 67:420–434
Korukottu J, Schneider R, Vijayan V, Lange A, Pongs O, Becker S, Baldus M, Zweckstetter M (2008) High-resolution 3D structure determination of kaliotoxin by solid-state NMR spectroscopy. PLoS One 3:e2359
Li YF, Poole S, Nishio K, Jang K, Rasulova F, McVeigh A, Savarino SJ, Xia D, Bullitt E (2009) Structure of CFA/I fimbriae from enterotoxigenic Escherichia coli. Proc Natl Acad Sci USA 106:10793–10798
Loquet A, Bardiaux B, Gardiennet C, Blanchet C, Baldus M, Nilges M, Malliavin T, Böckmann A (2008) 3D structure determination of the Crh protein from highly ambiguous solid-state NMR restraints. J Am Chem Soc 130:3579–3589
Luhrs T, Ritter C, Adrian M, Riek-Loher D, Bohrmann B, Dobeli H, Schubert D, Riek R (2005) 3D structure of Alzheimer’s amyloid-β(1–42) fibrils. Proc Natl Acad Sci USA 102:17342–17347
Mu XQ, Bullitt E (2006) Structure and assembly of P-pili: a protruding hinge region used for assembly of a bacterial adhesion filament. Proc Natl Acad Sci USA 103:9861–9866
Mu XQ, Jiang ZG, Bullitt E (2005) Localization of a critical interface for helical rod formation of bacterial adhesion P-pili. J Mol Biol 346:13–20
Mu XQ, Savarino SJ, Bullitt E (2008) The three-dimensional structure of CFA/I adhesion pili: traveler’s diarrhea bacteria hang on by a spring. J Mol Biol 376:614–620
Nishiyama M, Horst R, Eidam O, Herrmann T, Ignatov O, Vetsch M, Bettendorff P, Jelesarov I, Grütter MG, Wüthrich K, Glockshuber R, Capitani G (2005) Structural basis of chaperone-subunit complex recognition by the type 1 pilus assembly platform FimD. EMBO J 24: 2075–2086
Nishiyama M, Vetsch M, Puorger C, Jelesarov I, Glockshuber R (2003) Identification and characterization of the chaperone-subunit complex-binding domain from the type 1 pilus assembly platform FimD. J Mol Biol 330:513–525
Parge HE, Forest KT, Hickey MJ, Christensen DA, Getzoff ED, Tainer JA (1995) Structure of the fibre-forming protein pilin at 26 A resolution. Nature 378:32–38
Pellecchia M, Guntert P, Glockshuber R, Wüthrich K (1998) NMR solution structure of the periplasmic chaperone FimC. Nat Struct Biol 5:885–890
Pellecchia M, Sebbel P, Hermanns U, Wüthrich K, Glockshuber R (1999) Pilus chaperone FimC-adhesin FimH interactions mapped by TROSY-NMR. Nat Struct Biol 6:336–339
Petkova AT, Ishii Y, Balbach JJ, Antzutkin ON, Leapman RD, Delaglio F, Tycko R (2002) A structural model for Alzheimer’s β-amyloid fibrils based on experimental constraints from solid state NMR. Proc Natl Acad Sci USA 99:16742–16747
Petkova AT, Yau WM, Tycko R (2006) Experimental constraints on quaternary structure in Alzheimer’s β-amyloid fibrils. Biochemistry 45:498–512
Pettigrew D, Anderson KL, Billington J, Cota E, Simpson P, Urvil P, Rabuzin F, Roversi P, Nowicki B, du Merle L, Le Bouguénec C, Matthews S, Lea SM (2004) High resolution studies of the Afa/Dr adhesin DraE and its interaction with chloramphenicol. J Biol Chem 279:46851–46857
Ramboarina S, Fernandes PJ, Daniell S, Islam S, Simpson P, Frankel G, Booy F, Donnenberg MS, Matthews S (2005) Structure of the bundle-forming pilus from enteropathogenic Escherichia coli. J Biol Chem 280:40252–40260
Ramboarina S, Fernandes P, Simpson P, Frankel G, Donnenberg M, Matthews S (2004) Complete resonance assignments of bundlin (BfpA) from the bundle-forming pilus of enteropathogenic Escherichia coli. J Biomol NMR 29:427–428
Ritter C, Maddelein ML, Siemer AB, Luhrs T, Ernst M, Meier BH, Saupe SJ, Riek R (2005) Correlation of structural elements and infectivity of the HET-s prion. Nature 435:844–848
Romero D, Aguilar C, Losick R, Kolter R (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci USA 107:2230–2234
Sauer FG, Fütterer K, Pinkner JS, Dodson KW, Hultgren SJ, Waksman G (1999) Structural basis of chaperone function and pilus biogenesis. Science 285:1058–1061
Shewmaker F, Kryndushkin D, Chen B, Tycko R, Wickner RB (2009a) Two prion variants of Sup35p have in-register parallel β-sheet structures, independent of hydration. Biochemistry 48:5074–5082
Shewmaker F, McGlinchey RP, Thurber KR, McPhie P, Dyda F, Tycko R, Wickner RB (2009b) The functional curli amyloid is not based on in-register parallel β-sheet structure. J Biol Chem 284:25065–25076
Shewmaker F, Wickner RB, Tycko R (2006) Amyloid of the prion domain of Sup35p has an in-register parallel β-sheet structure. Proc Natl Acad Sci USA 103:19754–19759
Sperling LJ, Berthold DA, Sasser TL, Jeisy-Scott V, Rienstra CM (2010) Assignment strategies for large proteins by magic-angle spinning NMR: the 21-kDa disulfide-bond-forming enzyme DsbA. J Mol Biol 399:268–282
Sung MA, Chen HA, Matthews S (2001a) Sequential assignment and secondary structure of the triple-labelled carbohydrate-binding domain of papG from uropathogenic E. coli. J Biomol NMR 19:197–198
Sung MA, Fleming K, Chen HA, Matthews S (2001b) The solution structure of PapGII from uropathogenic Escherichia coli and its recognition of glycolipid receptors. EMBO Rep 2: 621–627
Tycko R (2006) Molecular structure of amyloid fibrils: insights from solid-state NMR. Q Rev Biophys 39:1–55
Velarde JJ, Varney KM, Inman KG, Farfan M, Dudley E, Fletcher J, Weber DJ, Nataro JP (2007) Solution structure of the novel dispersin protein of enteroaggregative Escherichia coli. Mol Microbiol 66:1123–1135
Vilar M, Chou HT, Luhrs T, Maji SK, Riek-Loher D, Verel R, Manning G, Stahlberg H, Riek R (2008) The fold of β-synuclein fibrils. Proc Natl Acad Sci USA 105:8637–8642
Waksman G, Hultgren SJ (2009) Structural biology of the chaperone-usher pathway of pilus biogenesis. Nat Rev Microbiol 7:765–774
Wang X, Hammer ND, Chapman MR (2008) The molecular basis of functional bacterial amyloid polymerization and nucleation. J Biol Chem 283:21530–21539
Wasmer C, Lange A, Van Melckebeke H, Siemer AB, Riek R, Meier BH (2008) Amyloid fibrils of the HET-s(218–289) prion form a β solenoid with a triangular hydrophobic core. Science 319:1523–1526
Wickner RB, Dyda F, Tycko R (2008) Amyloid of Rnq1p, the basis of the [PIN+] prion, has a parallel in-register β-sheet structure. Proc Natl Acad Sci USA 105:2403–2408
Xu XF, Tan YW, Lam L, Hackett J, Zhang M, Mok YK (2004) NMR structure of a type IVb pilin from Salmonella typhi and its assembly into pilus. J Biol Chem 279:31599–31605
Zavialov AV, Berglund J, Pudney AF, Fooks LJ, Ibrahim TM, MacIntyre S, Knight SD (2003) Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell 113:587–596
Zech SG, Wand AJ, McDermott AE (2005) Protein structure determination by high-resolution solid-state NMR spectroscopy: application to microcrystalline ubiquitin. J Am Chem Soc 127:8618–8626
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Shewmaker, F. (2011). The Application of NMR Techniques to Bacterial Adhesins. In: Linke, D., Goldman, A. (eds) Bacterial Adhesion. Advances in Experimental Medicine and Biology, vol 715. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0940-9_15
Download citation
DOI: https://doi.org/10.1007/978-94-007-0940-9_15
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-0939-3
Online ISBN: 978-94-007-0940-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)