Tightening the knot in phytochrome by single-molecule atomic force microscopy

Biophysical Journal

Volumn 96, Issue 4, 2009, Pages 1508-1514

  Bornschlögl, Thomas ^a   Anstrom, David M ^b   Mey, Elisabeth ^b   Dzubiella, Joachim ^b   Rief, Matthias ^a,c   Forest, Katrina T ^b  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c Munich Center for Integrated Protein Science   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APOPHYTOCHROME; PHYTOCHROME; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; COVALENT BOND; MOLECULAR DYNAMICS; NONHUMAN; PHOTOCONVERSION; PHOTORECEPTOR; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN STABILITY; PROTEIN STRUCTURE; SINGLE MOLECULE ATOMIC FORCE MICROSCOPY; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; DEINOCOCCUS; PHOTOSTIMULATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; SPECTROSCOPY;

BINDING SITES; COMPUTER SIMULATION; DEINOCOCCUS; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; PHOTIC STIMULATION; PHYTOCHROME; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; SPECTRUM ANALYSIS;

EID: 62649138263     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.11.012     Document Type: Article

References (45)

1. Wagner, J. R., J. S. Brunzelle, K. T. Forest, and R. D. Vierstra. 2005. A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome. Nature. 438:325-331. (Pubitemid 41643944)
2. Misaghi, S., P. J. Galardy, W. J. Meester, H. Ovaa, H. L. Ploegh, et al. 2005. Structure of the ubiquitin hydrolase UCH-L3 complexed with a suicide substrate. J. Biol. Chem. 280:1512-1520.
3. Shi, D., R. Gallegos, J. DePonte 3rd, H. Morizono, X. Yu, et al. 2002. Crystal structure of a transcarbamylase-like protein from the anaerobic bacterium Bacteroides fragilis at 2.0 Å resolution. J. Mol. Biol. 320:899-908.
4. Khatib, F., M. T. Weirauch, and C. A. Rohl. 2006. Rapid knot detection and application to protein structure prediction. Bioinformatics. 22:e252-e259. (Pubitemid 44288294)
5. Lai, Y. L., S. C. Yen, S. H. Yu, and J. K. Hwang. 2007. pKNOT: the protein KNOT web server. Nucleic Acids Res. 35:W420-W424.
6. Kolesov, G., P. Virnau, M. Kardar, and L. A. Mirny. 2007. Protein knot server: detection of knots in protein structures. Nucleic Acids Res. 35:W425-W428.
7. Virnau, P., L. A. Mirny, and M. Kardar. 2006. Intricate knots in proteins: function and evolution. PLoS Comput Biol. 2:e122.
8. Yeates, T. O., T. S. Norcross, and N. P. King. 2007. Knotted and topologically complex proteins as models for studying folding and stability. Curr. Opin. Chem. Biol. 11:595-603. (Pubitemid 350180574)
9. Rockwell, N. C., Y. S. Su, and J. C. Lagarias. 2006. Phytochrome structure and signaling mechanisms. Annu. Rev. Plant Biol. 57:837-858. (Pubitemid 44061047)
10. Hughes, J., T. Lamparter, F. Mittmann, E. Hartmann, W. Gartner, et al. 1997. A prokaryotic phytochrome. Nature. 386:663.
11. Karniol, B., J. R. Wagner, J. M. Walker, and R. D. Vierstra. 2005. Phylogenetic analysis of the phytochrome superfamily reveals distinct microbial subfamilies of photoreceptors. Biochem. J. 392:103-116. (Pubitemid 41689406)
12. Wagner, J. R., J. Zhang, J. S. Brunzelle, R. D. Vierstra, and K. T. Forest. 2007. High resolution structure of Deinococcus bacteriophytochrome yields new insights into phytochrome architecture and evolution. J. Biol. Chem. 282:12298-12309. (Pubitemid 47100678)
13. Oberhauser, A. F., and M. Carrion-Vazquez. 2008. Mechanical biochemistry of proteins one molecule at a time. J. Biol. Chem. 283:6617-6621.
14. Bertz, M., and M. Rief. 2008. Mechanical unfoldons as building blocks of maltose-binding protein. J. Mol. Biol. 378:447-458.
15. Mickler, M., R. I. Dima, H. Dietz, C. Hyeon, D. Thirumalai, et al. 2007. Revealing the bifurcation in the unfolding pathways of GFP by using single-molecule experiments and simulations. Proc. Natl. Acad. Sci. USA. 104:20268-20273.
16. Forman, J. R., and J. Clarke. 2007. Mechanical unfolding of proteins: insights into biology, structure and folding. Curr. Opin. Struct. Biol. 17:58-66.
17. Taylor, W. R., and K. Lin. 2003. Protein knots: a tangled problem. Nature. 421:25.
18. Sulkowska, J. I., P. Sulkowski, P. Szymczak, and M. Cieplak. 2008. Tightening of knots in proteins. Phys. Rev. Lett. 100:058106.
19. Bao, X. R., H. J. Lee, and S. R. Quake. 2003. Behavior of complex knots in single DNA molecules. Phys. Rev. Lett. 91:265506.
20. Arai, Y., R. Yasuda, K. Akashi, Y. Harada, H. Miyata, et al. 1999. Tying a molecular knot with optical tweezers. Nature. 399:446-448.
21. Wang, T., and A. Ikai. 1999. Protein stretching III: force-extension curves of tethered bovine carbonic anhydrase b to the silicon substrate under native, intermediate and denaturing conditions. Jpn. J. Appl. Phys. 38:3912-3917.
22. Wang, T., H. Arakawa, and A. Ikai. 2002. Reversible stretching of a monomeric unit in a dimeric bovine carbonic anhydrase B with the atomic force microscope. Ultramicroscopy. 91:253-259.
23. Yang, G., C. Cecconi, W. A. Baase, I. R. Vetter, W. A. Breyer, et al. 2000. Solid-state synthesis and mechanical unfolding of polymers of T4 lysozyme. Proc. Natl. Acad. Sci. USA. 97:139-144.
24. Dombkowski, A. A. 2003. Disulfide by design: a computational method for the rational design of disulfide bonds in proteins. Bioinformatics. 19:1852-1853.
25. Dietz, H., and M. Rief. 2006. Protein structure by mechanical triangulation. Proc. Natl. Acad. Sci. USA. 103:1244-1247. (Pubitemid 43191150)
26. Dietz, H., F. Berkemeier, M. Bertz, and M. Rief. 2006. Anisotropic deformation response of single protein molecules. Proc. Natl. Acad. Sci. USA. 103:12724-12728. (Pubitemid 44298628)
27. Case, D. A. 2006. AMBER9.0. University of California, San Francisco.
28. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:27-38.
29. Dietz, H., M. Bertz, M. Schlierf, F. Berkemeier, T. Bornschlogl, et al. 2006. Cysteine engineering of polyproteins for single-molecule force spectroscopy. Nat. Protocols. 1:80-84.
30. Noack, S., N. Michael, R. Rosen, and T. Lamparter. 2007. Protein conformational changes of Agrobacterium phytochrome Agp1 during chromophore assembly and photoconversion. Biochemistry. 46:4164-4176. (Pubitemid 46536078)
31. Yamamoto, K. T., and S. Tokutomi. 1989. Formation of aggregates of tryptic fragments derived from the carboxyl-terminal half of pea phytochrome and localization of the site of contact between the fragments by amino-terminal amino acid sequence analysis. Photochem. Photobiol. 50:113-120.
32. Jones, A. M., and H. P. Erickson. 1989. Domain structure of phytochrome from Avena sativa visualized by electron microscopy. Photochem. Photobiol. 49:479-483.
33. Bustamante, C., J. F. Marko, E. D. Siggia, and S. Smith. 1994. Entropic elasticity of lambda-phage DNA. Science. 265:1599-1600.
34. Wallin, S., K. B. Zeldovich, and E. I. Shakhnovich. 2007. The folding mechanics of a knotted protein. J. Mol. Biol. 368:884-893. (Pubitemid 46527616)
35. Lua, R. C., and A. Y. Grosberg. 2006. Statistics of knots, geometry of conformations, and evolution of proteins. PLoS Comput Biol. 2:e45.
36. Taylor, W. R. 2007. Protein knots and fold complexity: some new twists. Comput. Biol. Chem. 31:151-162.
37. Linke, W. A., and A. Grutzner. 2008. Pulling single molecules of titin by AFM-recent advances and physiological implications. Pflugers Arch. 456:101-115.
38. Ulijasz, A. T., G. Cornilescu, D. von Stetten, S. Kaminski, M. A. Mroginski, et al. 2008. Characterization of two thermostable cyanobacterial phytochromes reveals global movements in the chromophore-binding domain during photoconversion. J. Biol. Chem. 283:21251-21266.
39. Yoshihara, S., M. Katayama, X. Geng, and M. Ikeuchi. 2004. Cyanobacterial phytochrome-like PixJ1 holoprotein shows novel reversible photoconversion between blue- and green-absorbing forms. Plant Cell Physiol. 45:1729-1737.
40. Rockwell, N. C., S. L. Njuguna, L. Roberts, E. Castillo, V. L. Parson, et al. 2008. A second conserved GAF domain cysteine is required for the blue/green photoreversibility of cyanobacteriochrome Tlr0924 from Thermosynechococcus elongatus. Biochemistry. 47:7304-7316.
41. Virnau, P., Y. Kantor, and M. Kardar. 2005. Knots in globule and coil phases of a model polyethylene. J. Am. Chem. Soc. 127:15102-15106. (Pubitemid 41547376)
42. Mallam, A. L., S. C. Onuoha, J. G. Grossmann, and S. E. Jackson. 2008. Knotted fusion proteins reveal unexpected possibilities in protein folding. Mol. Cell. 30:642-648.
43. Mallam, A. L., and S. E. Jackson. 2006. Probing nature's knots: the folding pathway of a knotted homodimeric protein. J. Mol. Biol. 359:1420-1436.
44. Mallam, A. L., and S. E. Jackson. 2005. Folding studies on a knotted protein. J. Mol. Biol. 346:1409-1421. (Pubitemid 40248838)
45. Rief, M., M. Gautel, F. Oesterhelt, J. M. Fernandez, and H. E. Gaub. 1997. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science. 276:1109-1112. (Pubitemid 27218118)