Dual energy landscape: The functional state of the β-barrel outer membrane protein G molds its unfolding energy landscape

Proteomics

Volumn 10, Issue 23, 2010, Pages 4151-4162

  Damaghi, Mehdi ^a,b   Sapra, K Tanuj ^b,c   Köster, Stefan ^d   Yildiz, Özkan ^d   Kühlbrandt, Werner ^d   Muller, Daniel J ^a,b  

^a ETH ZURICH   (Switzerland)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

Author keywords

Atomic force microscopy; Interactions; Mechanical properties; Nanoproteomics; PH gating; Single molecule force spectroscopy

Indexed keywords

MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN G; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; ENERGY; ESCHERICHIA COLI; GENE SWITCHING; MOLECULAR INTERACTION; MOLECULE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; SPECTROSCOPY;

AMINO ACID MOTIFS; BACTERIAL OUTER MEMBRANE PROTEINS; ESCHERICHIA COLI PROTEINS; PORINS; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN UNFOLDING; THERMODYNAMICS;

ESCHERICHIA COLI;

EID: 78649652074     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000241     Document Type: Article

References (60)

1. Schulz, G. E., The structure of bacterial outer membrane proteins. Biochim. Biophys. Acta 2002, 1565, 308-317.
2. Xu, G. Z., Shi, B., McGroarty, E. J., Tien, H. T., Channel-closing activity of porins from Escherichia coli in bilayer lipid membranes. Biochim. Biophys. Acta 1986, 862, 57-64.
3. Heyde, M., Portalier, R., Regulation of major outer membrane porin proteins of Escherichia coli K 12 by pH. Mol. Gen. Genet. 1987, 208, 511-517.
4. Todt, J. C., Rocque, W. J., McGroarty, E. J., Effects of pH on bacterial porin function. Biochemistry 1992, 31, 10471-10478.
5. Todt, J. C., McGroarty, E. J., Acid pH decreases OmpF and OmpC channel size in vivo. Biochem. Biophys. Res. Commun. 1992, 189, 1498-1502.
6. Conlan, S., Zhang, Y., Cheley, S., Bayley, H., Biochemical and biophysical characterization of OmpG: A monomeric porin. Biochemistry 2000, 39, 11845-11854.
7. Schulz, G., Bacterial porins: structure and function. Curr. Opin. Cell Biol. 1993, 5, 701-707.
8. Muller, D. J., Engel, A., Voltage and pH-induced channel closure of porin OmpF visualized by atomic force microscopy. J. Mol. Biol. 1999, 285, 1347-1351.
9. Andersen, C., Schiffler, B., Charbit, A., Benz, R., PH-induced collapse of the extracellular loops closes Escherichia coli maltoporin and allows the study of asymmetric sugar binding. J. Biol. Chem. 2002, 277, 41318-41325.
10. Yildiz, O., Vinothkumar, K. R., Goswami, P., Kuhlbrandt, W., Structure of the monomeric outer-membrane porin OmpG in the open and closed conformation. EMBO J. 2006, 25, 3702-3713.
11. Subbarao, G. V., van den Berg, B., Crystal structure of the monomeric porin OmpG. J. Mol. Biol. 2006, 360, 750-759.
12. Liang, B., Tamm, L. K., Structure of outer membrane protein G by solution NMR spectroscopy. Proc. Natl. Acad. Sci. USA 2007, 104, 16140-16145.
13. Mari, S. A., Koster, S., Bippes, C., Yildiz, O. et al., pH-induced conformational change of the beta-barrel forming protein OmpG reconstituted into native E. coli lipids. J. Mol. Biol. 2010, 396, 610-616.
14. Kleinschmidt, J. H., Tamm, L. K., Folding intermediates of a β-barrel membrane protein. Kinetic evidence for a multi-step membrane insertion mechanism. Biochemistry 1996, 35, 12993-13000.
15. White, S. H., Wimley, W. C., Membrane protein folding and stability: Physical principles. Annu. Rev. Biophys. Biomol. Struct. 1999, 28, 319-365.
16. Kleinschmidt, J. H., Tamm, L. K., Secondary and tertiary structure formation of the beta-barrel membrane protein OmpA is synchronized and depends on membrane thickness. J. Mol. Biol. 2002, 324, 319-330.
17. Tamm, L. K., Hong, H., Liang, B., Folding and assembly of beta-barrel membrane proteins. Biochim. Biophys. Acta 2004, 1666, 250-263.
18. Bond, P. J., Sansom, M. S., The simulation approach to bacterial outer membrane proteins. Mol. Membr. Biol. 2004, 21, 151-161.
19. Wimley, W. C., White, S. H., Reversible unfolding of β-sheets in membranes: A calorimetric study. J. Mol. Biol. 2004, 342, 703-711.
20. Booth, P. J., Unravelling the folding of bacteriorhodopsin. Biochim. Biophys. Acta 2000, 1460, 4-14.
21. Surrey, T., Schmid, A., Jahnig, F., Folding and membrane insertion of the trimeric β-barrel protein OmpF. Biochemistry 1996, 35, 2283-2288.
22. Conlan, S., Bayley, H., Folding of a monomeric porin, OmpG, in detergent solution. Biochemistry 2003, 42, 9453-9465.
23. Hong, H., Park, S., Jimenez, R. H. F., Rinehart, D., Tamm, L. K., Role of aromatic side chains in the folding and thermodynamic stability of integral membrane proteins. J. Am. Chem. Soc. 2007, 129, 8320-8327.
24. Buchanan, S. K., Beta-barrel proteins from bacterial outer membranes: structure, function and refolding. Curr. Opin. Struct. Biol. 1999, 9, 455-461.
25. Huysmans, G. H. M., Baldwin, S. A., Brockwell, D. J., Radford, S. E., The transition state for folding of an outer membrane protein. Proc. Natl. Acad. Sci. USA 2010, 107, 4099-4104.
26. Sapra, K. T., Damaghi, M., Koester, S., Yildiz, O. et al., One b hairpin after the other: Exploring mechanical unfolding pathways of the transmembrane β-barrel protein OmpG. Angew. Chem. Int. Ed. 2009, 48, 8306-8308.
27. Janovjak, H., Kessler, M., Gaub, H. E., Oesterhelt, D., Muller, D. J., Unfolding pathways of native bacteriorhodopsin depend on temperature. EMBO J. 2003, 22, 5220-5229.
28. Kedrov, A., Janovjak, H., Sapra, K. T., Muller, D. J., Deciphering molecular interactions of native membrane proteins by single-molecule force spectroscopy. Annu. Rev. Biophys. Biomol. Struct. 2007, 36, 233-260.
29. Engel, A., Gaub, H. E., Structure and mechanics of membrane proteins. Annu. Rev. Biochem. 2008, 77, 127-148.
30. Evans, E., Ritchie, K., Dynamic strength of molecular adhesion bonds. Biophys. J. 1997, 72, 1541-1555.
31. Evans, E., Kinoshita, K., Using force to probe single-molecule receptor-cytoskeletal anchoring beneath the surface of a living cell. Methods Cell Biol. 2007, 83C, 373-396.
32. Muller, D. J., Engel, A., Atomic force microscopy and spectroscopy of native membrane proteins. Nat. Protoc. 2007, 2, 2191-2197.
33. Butt, H.-J., Jaschke, M., Calculation of thermal noise in atomic force microscopy. Nanotechnology 1995, 6, 1-7.
34. Damaghi, M., Bippes, C., Koester, S., Mari, S. A. et al., pH-dependent interactions guide the folding and gate the transmembrane pore of the beta-barrel membrane protein OmpG. J. Mol. Biol. 2010, 397, 878-882.
35. Bell, G. I., Models for the specific adhesion of cells to cells. Science 1978, 200, 618-627.
36. Evans, E., Energy landscapes of biomolecular adhesion and receptor anchoring at interfaces explored with dynamic force spectroscopy. Faraday Discuss. 1998, 111, 1-16.
37. Bieri, O., Wirz, J., Hellrung, B., Schutkowski, M. et al., The speed limit for protein folding measured by triplet-triplet energy transfer. Proc. Natl. Acad. Sci. USA 1999, 96, 9597-9601.
38. Krieger, F., Fierz, B., Bieri, O., Drewello, M., Kiefhaber, T., Dynamics of unfolded polypeptide chains as model for the earliest steps in protein folding. J. Mol. Biol. 2003, 332, 265-274.
39. Gräter, F., Grubmüller, H., Fluctuations of primary ubiquitin folding intermediates in a force clamp. J. Struct. Biol. 2007, 157, 557-569.
40. Nunes, J., Hensen, U., Ge, L., Lipinsiky, M. et al., A "force buffer" protecting immunoglobulin titin. Angew. Chem. Int. Ed. 2010, 49, 3528-3531.
41. Dietz, H., Berkemeier, F., Bertz, M., Rief, M., Anisotropic deformation response of single protein molecules. Proc. Natl. Acad. Sci. USA 2006, 103, 12724-12728.
42. Howard, J., Mechanics of Motor Proteins and the Cytoskeleton, Sinauer Associates Inc., Sunderland, Massachusetts 2001.
43. Carrion-Vazquez, M., Marszalek, P. E., Oberhauser, A. F., Fernandez, J. M., Atomic force microscopy captures length phenotypes in single proteins. Proc. Natl. Acad. Sci. USA 1999, 96, 11288-11292.
44. Williams, P. M., Fowler, S. B., Best, R. B., Toca-Herrera, J. L. et al., Hidden complexity in the mechanical properties of titin. Nature 2003, 422, 446-449.
45. Janovjak, H., Struckmeier, J., Hubain, M., Kedrov, A. et al., Probing the energy landscape of the membrane protein bacteriorhodopsin. Structure 2004, 12, 871-879.
46. Kedrov, A., Appel, M., Baumann, H., Ziegler, C., Muller, D. J., Examining the dynamic energy landscape of an antiporter upon inhibitor binding. J. Mol. Biol. 2008, 375, 1258-1266.
47. Sapra, K. T., Balasubramanian, G. P., Labudde, D., Bowie, J. U., Muller, D. J., Point mutations in membrane proteins reshape energy landscape and populate different unfolding pathways. J. Mol. Biol. 2008, 376, 1076-1090.
48. Sapra, K. T., Park, P. S., Palczewski, K., Muller, D. J., Mechanical properties of bovine rhodopsin and bacteriorhodopsin: possible roles in folding and function. Langmuir 2008, 24, 1330-1337.
49. Evans, E., Probing the relation between force-lifetime-and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct. 2001, 30, 105-128.
50. Bippes, C., Zeltina, A., Casagrande, F., Ratera, M. et al., Substrate binding tunes conformational flexibility and kinetic stability of an amino acid antiporter. J. Biol. Chem. 2009, 28, 18651-18663.
51. Sapra, K. T., Park, P. S. H., Filipek, S., Engel, A. et al., Detecting molecular interactions that stabilize bovine rhodopsin. J. Mol. Biol. 2006, 358, 255-269.
52. Park, P. S., Sapra, K. T., Jastrzebska, B., Maeda, T. et al., Modulation of molecular interactions and function by rhodopsin palmitylation. Biochemistry 2009, 48, 4294-4304.
53. Frauenfelder, H., Sligar, S. G., Wolynes, P. G., The energy landscapes and motions of proteins. Science 1991, 254, 1598-1603.
54. Wolynes, P. G., Onuchic, J. N., Thirumalai, D., Navigating the folding routes. Science 1995, 267, 1619-1620.
55. Dill, K. A., Chan, H. S., From Levinthal to pathways to funnels. Nat. Struct. Biol. 1997, 4, 10-19.
56. Sanders, C. R., Nagy, J. K., Misfolding of membrane proteins in health and disease: the lady or the tiger? Curr. Opin. Struct. Biol. 2000, 10, 438-442.
57. Horovitz, A., Serrano, L., Avron, B., Bycroft, M., Fersht, A. R., Strength and co-operativity of contributions of surface salt bridges to protein stability. J. Mol. Biol. 1990, 216, 1031-1044.
58. Ishii, M., Kunimura, J. S., Jeng, H. T., Penna, T. C., Cholewa, O., Evaluation of the pH- and thermal stability of the recombinant green fluorescent protein (GFP) in the presence of sodium chloride. Appl. Biochem. Biotechnol. 2007, 137-140, 555-571.
59. Ellis, R. J., Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr. Opin. Struct. Biol. 2001, 11, 114-119.
60. Muller, D. J., Kessler, M., Oesterhelt, F., Moeller, C. et al., Stability of bacteriorhodopsin alpha-helices and loops analyzed by single-molecule force spectroscopy. Biophys. J. 2002, 83, 3578-3588.