Atomic force microscopy detects changes in the interaction forces between GroEL and substrate proteins

Biophysical Journal

Volumn 74, Issue 6, 1998, Pages 3256-3263

  Vinckier, Anja ^a,b   Gervasoni, Pietro ^b   Zaugg, Frank ^a   Ziegler, Urs ^b   Lindner, Peter ^b   Groscurth, Peter ^b   Plückthun, Andreas ^b   Semenza, Giorgio ^a,c  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALANINE; BETA LACTAMASE; CHAPERONIN; CITRATE SYNTHASE; CYSTINE; GLYCINE; MUTANT PROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; HYDROPHILICITY; HYDROPHOBICITY; MOLECULAR WEIGHT; NONHUMAN; PROTEIN DENATURATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE;

EID: 0031835964     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(98)78032-4     Document Type: Article

References (61)

1. 126→Val with known crystal structure. J. Mol. Biol. 258:732-735.
2. Allen, S., X. Y. Chen, J. Davies., M. C. Davies, A. C. Dawkes, J. C. Edwards, C. J. Roberts, J. Sefton, S. J. B. Tendler, and P. M. Williams. 1997. Detection of antigen-antibody binding events with the atomic force microscope. Biochemistry. 36:7457-7463.
3. Allen, S., J. Davies, A. C. Dawkes, M. C. Davies, J. C. Edwards, M. C. Parker, C. J. Roberts, J. Sefton, S. J. Tendler, and P. M. Williams. 1996. In situ observation of streptavidin-biotin binding on an immunoassy well surface using an atomic force microscope. FEBS Lett. 390:161-164.
4. Aoki, K., H. Taguchi, Y. Shindo, M. Yoshida, K. Ogasahara, K. Yutani, and N. Tanaka. 1997. Calorimetric observation of a GroEL-protein binding reaction with little contribution of hydrophobic interaction. J. Biol. Chem. 272:32158-32162.
5. Boisvert, D. C., J. Wang, Z. Otwinowski, A. L. Horwich, and P. B. Sigler. 1996. The 2.4 Å crystal structure of the bacterial chaperonin complexed with ATPγS. Nature Struct. Biol. 3:170-177.
6. Boland, T., and B. D. Ratner. 1995. Direct measurements of hydrogen bonding in DNA nucleotide bases by atomic force mciroscopy. Proc. Natl. Acad. Sci. USA. 92:5297-5301.
7. Braig, K., Z. Otwinowski, R. Hegde, D. C. Boisvert, A. Joachimiak, A. L. Horwich, and P. B. Sigler. 1994. The crystal structure of the bacterial chaperonin GroEL at 2.8 Å. Nature. 371:578-586.
8. Burston, S. G., N. A. Ranson, and A. R. Clarke. 1995. The origins and consequences of asymmetry in the chaperonin reaction cycle. J. Mol. Biol. 249:138-152.
9. Chen, S., A. M. Roseman, A. S. Hunter, S. P. Wood, S. G. Burston, N. A. Ranson, A. R. Clarke, and H. R. Saibil. 1994. Localization of a folding protein and shape changes in GroEL-GroES complexes imaged by cryo-electron microscopy. Nature. 371:261-264.
10. Cleveland, J. P., S. Manne, D. Bocek, and P. K. Hansma. 1993. A nondestructive method for determining the spring constant of cantilevers for scanning force microscopy. Rev. Sci. Intrum. 64:403-405.
11. Dammer, U., M. Hegner, D. Anselmetti, P. Wagner, M. Dreier, W. Huber, and H.-J. Güntherodt. 1996. Specific antigen/antibody interactions measured by force microscopy. Biophys. J. 70:2437-2441.
12. Dammer, U., O. Popescu, P. Wagner, D. Anselmetti, H.-J. Güntherodt, and G. N. Misevic. 1995. Binding strength between cell adhesion proteoglycans measured by atomic force microscopy. Science. 267:1173-1175.
13. DeRose, J. A., and J.-P. Revel. 1997. Examination of atomic (scanning) force microscopy probe tips with the transmission electron microscope. Microsc. Microanal. 3:203-213.
14. Detrich, H. W., M. A. Jordan, L. Wilson, and R. C. Williams, Jr. 1985. Mechanism of microtubule assembly. Changes in polymer structure and organization during assemby of sea urchin egg tubulin. J. Biol. Chem. 260:9479-9490.
15. Evans, E., D. Berk, and A. Leung. 1991. Detachment of agglutinin-bonded red blood cells. 1. Forces to rupture molecular-point attachments. Biophys. J. 59:838-848.
16. Evans, E., K. Ritchie, and R. Merkel. 1995. Sensitive force technique to probe molecular adhesion and structural linkage at biological interfaces. Biophys. J. 68:2580-2587.
17. Fenton, W. A., and A. L. Horwich. 1997. GroEL-mediated protein folding. Protein Sci. 6:743-760.
18. Fenton, W. A., Y. Kashi, K. Furtak, and A. L. Horwich. 1994. Residues in chaperonin GroEL required for polypeptide binding and release. Nature. 371:614-619.
19. Florin, E.-L., V. T. Moy, and H. E. Gaub. 1994. Adhesion forces between individual ligand-receptor pairs. Science. 264:415-417.
20. Fritz, J., D. Anselmetti, J. Jarchow, and X. Fernàndez-Busquets. 1997. Probing single biomolecules with atomic force microscopy. J. Struct. Biol. 119:165-171.
21. Gervasoni, P., P. Gehrig, and A. Plückthun. 1997. Two conformational states of β-lactamase bound to GroEL: a biophysical characterization. J. Mol. Biol. 275:663-675.
22. Gervasoni, P., and A. Plückthun. 1997. Folding intermediates of β-lactamase recognized by GroEL. FEBS Lett. 401:138-142.
23. Hartl, F. U. 1996. Molecular chaperones in cellular protein folding. Nature. 381:571-580.
24. Hinterdorfer, P., W. Baumgartner, H. J. Gruber, K. Schilcher, and H. Schindler. 1996. Detection and localization of individual antibody-antigen recognition events by atomic force microscopy. Proc. Natl. Acad. Sci. USA. 93:3477-3481.
25. Hoh, J. H., J. P. Cleveland, C. B. Prater, J.-P. Revel, and P. K. Hansma. 1992. Quantized adhesion detected with the atomic force microscope. J. Am. Chem. Soc. 114:4917-4918.
26. Israelachvili, J. N., editor. 1989. Intermolecular and Surface Forces, 3rd Ed. Academic Press, London.
27. Itzhaki, L. S., D. E. Otzen, and A. R. Fersht. 1995. Nature and consequences of GroEL-protein interactions. Biochemistry. 34:14581-14587.
28. Laminet, A. A., and A. Plückthun. 1989. The precursor of β-lactamase: purification, properties and folding kinetics. EMBO J. 8:1469-1477.
29. Leckband, D. 1995. The surface force apparatus - a tool for probing molecular protein interactions. Nature. 376:617-618.
30. Lee, G. U., D. A. Kidwell, and R. J. Colton. 1994a. Sensing discrete straptavidin-biotin interactions with atomic force microscopy. Langmuir. 10:354-357.
31. Lee, G. U., L. A. Chrisey, and R. J. Colton. 1994b. Direct measurements of the forces between complementary strands of DNA. Science. 266: 771-773.
32. Lin, Z., F. P. Schwarz, and E. Eisenstein. 1995. The hydrophobic nature of GroEL-substrate binding. J. Biol. Chem. 270:1011-1014.
33. Lindner, P., B. Guth, C. Wülfling, C. Krebber, B, Steipe, F. Müller, and A. Plückthun. 1992. Purification of native proteins from the cytoplasm and periplasm of Escherichia coli using IMAC and histidine tails: a comparison of proteins and protocols. Methods Enzymol. 4:41-56.
34. Ludwig, M., V. T. Moy, M. Rief, E.-L. Florin, and H. E. Gaub. 1994. Characterization of the adhesion force between avidin-functionalized AFM tips and biotinylated agarose beads. Microsc. Microanal. Microstruct. 5:321-328.
35. Mayhew, M., A. A. V. R. da Silva, J. Martin, H. Erdjument-Bromage, P. Tempst, and F. U. Hartl. 1996. Protein folding in the central cavity of the GroEL-GroES chaperonin complex. Nature. 379:420-426.
36. Mou, J., D. M. Czajkowsky, S. J. Sheng, R. Ho, and Z. Shao. 1996a. High resolution surface structure of E. coli GroES oligomer by atomic force microscopy. FEBS Lett. 381:161-164.
37. Mou, J., S. J. Sheng, R. Ho, and Z. Shao. 1996b. Chaperonins GroEL and GroES: views from atomic force microscopy. Biophys. J. 71:2213-2221.
38. Moy, V. T., E.-L. Florin, and H. E. Gaub. 1994. Intermolecular forces and energies between ligands and receptors. Science. 266:257-259.
39. Nakajima, H., Y. Kunioka, K. Nakano, K. Shimizu, M. Seto, and T. Ando. 1997. Scanning force microscopy of the interaction events between a single molecule of heavy meromyosin and actin. Biochem. Biophys. Res. Commun. 234:178-182.
40. Noy, A., D. V. Vezenov, J. F. Kayyem, T. J. Meade, and C. M. Lieber. 1997. Stretching and breaking duplex DNA by chemical force microscopy. Chem. Biol. 4:519-527.
41. Perrett, S., R. Zahn, G. Stenberg, and A. R. Fersht. 1997. Importance of electrostatic interaction in the rapid binding of polypeptides to GroEL. J. Mol. Biol. 269:892-901.
42. Pierres, A., A.-M. Benoliel, and P. Bongrand. 1996a. Measuring bonds between surface-associated molecules. J. Immunol. Methods 196: 105-120.
43. Pierres, A., A. M. Benoliel, P. Bongrand, and P. A. van der Merwe. 1996b. Determination of the lifetime and force dependence of interactions of single bonds between surface-detached CD2 and CD48 adhesion molecules. Proc. Natl. Acad. Sci. USA. 93:15114-15118.
44. 2 antibody fragments on an industrial substrate using scanning force microscopy. Ultramicroscopy. 62:149-155.
45. Roseman, A., S. Chen, H. White, K. Braig, and H. Saibil. 1996. The chaperonin ATPase cycle: mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell. 87:241-251.
46. Rye, H. S., S. G. Burston, W. A. Fenton, J. M. Beechem, Z. Xu, P. B. Sigler, and A. L. Horwich. 1997. Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature. 388:792-798.
47. Scheuring, S. 1996. A study of the E. coli chaperonin GroEL and GroEL/ GroES complexes using transmission electron and atomic force microscopy: its structure and function. Diploma thesis. Biozentrum, Basel, Switzerland.
48. Stuart, J. K., and V. Hlady. 1995. Effects of discrete protein-surface interactions in scanning force microscopy adhesion force measurements. Langmuir. 11:1368-1374.
49. Todd, M. J., G. H. Lorimer, and D. Thirumalai. 1996. Chaperonin-facilitated protein folding: optimization of rate and yield by an iterative annealing mechanism. Proc. Natl. Acad. Sci. USA. 93:4030-4035.
50. Vinckier, A. 1996. Applications of atomic force microscopy (AFM): development of a tapping mode AFM and study of microtubules. Ph.D. thesis. Katholieke Universiteit, Leuven, Belgium.
51. Vinckier, A., C. Dumortier, Y. Engelborghs, and L. Hellemans. 1996a. Dynamical and mechanical study of immobilized microtubules with atomic force microscopy. J. Vac. Sci. Technol. B. 14:1427-1431.
52. Vinckier, A., F. Hennau, K. Kjoller, and L. Hellemans. 1996b. Low-cost modification of a contact atomic force microscope (AFM) into a sound-activated tapping mode AFM for use in air and liquids. Rev. Sci. Instrum. 67:387-392.
53. Vinckier, A., I. Heyvaert, A. D'Hoore, T. McKittrick, C. Van Haesendonck, Y. Engelborghs, and L. Hellemans. 1995. Immobilizing and imaging microtubules by atomic force microscopy. Ultramicroscopy. 57: 337-343.
54. Weetall, H. H. 1976. Covalent coupling methods for inorganic support materials. Methods Enzymol. 44:134-148.
55. Weetall, H. H., and A. M. Filbert. 1974. Porous glass for affinity chromatography applications. Methods Enzymol. 34:59-72.
56. White, H. E., S. Chen, A. M. Roseman, O. Yifrach, A. Horovitz, and H. R. Saibil. 1997. Structural basis of allosteric changes in the GroEL mutant ARG 197→ALA. Nature Struct. Biol. 4:690-694.
57. Xu, Z. H., A. L. Horwich, and P. B. Sigler. 1997. The crystal structure of the asymmetric GroEL-GroES-ADP(7): subscript chaperonin complex. Nature. 388:741-750.
58. Zahn, R., S. E. Axmann, K.-P. Rücknagel, E. Jaeger, and A. Plückthun. 1994. Thermodynamic partitioning model for hydrophobic binding of polypeptides by GroEL. I. GroEL recognizes the signal sequences of β-lactamase precursor. J. Mol. Biol. 242:150-164.
59. Zahn, R., J. R. Harris, G. Pfeifer, A. Plückthun, and W. Baumeister. 1993. Two-dimensional crystals of the molecular chaperone GroEL reveal structural plasticity. J. Mol. Biol. 229:579-584.
60. Zahn, R., P. Lindner, S. E. Axmann, and A. Plückthun. 1996. Effect of single point mutations in citrate synthase on binding to GroEL. FEBS Lett. 380:152-156.
61. Zahn, R., and A. Plückthun. 1994. Thermodynamic partitioning model for hydrophobic binding of polypeptides by GroEL. II. GroEL recognizes thermally unfolded mature β-lactamase. J. Mol. Biol. 242:165-174.