GFP's Mechanical Intermediate States

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Saeger, John ^a   Hytönen, Vesa P ^a,b   Klotzsch, Enrico ^a   Vogel, Viola ^a  

^a ETH ZURICH   (Switzerland)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ABSORPTION SPECTROSCOPY; ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANIONIC CHROMOPHORE; ARTICLE; BARREL STATE; CHROMATOPHORE; CONTROLLED STUDY; CORKED STATE; DELETION MUTANT; FLAME PHOTOMETRY; FLUORESCENCE LIFETIME SPECTROSCOPY; MECHANICS; MODEL; MOLECULAR DYNAMICS; PROTEIN UNFOLDING; PROTON TRANSPORT; RIPPED STATE; SPECTROSCOPY;

CRYSTALLOGRAPHY, X-RAY; FLUORESCENCE; GREEN FLUORESCENT PROTEINS; HYDROGEN BONDING; KINETICS; LIGHT; MECHANICAL PHENOMENA; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; SPECTRUM ANALYSIS;

EID: 84868292566     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046962     Document Type: Article

References (69)

1. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC, (1994) Green fluorescent protein as a marker for gene expression. Science 263: 802-805.
2. Lemmon CA, Ohashi T, Erickson HP, (2011) Probing the Folded State of Fibronectin Type III Domains in Stretched Fibrils by Measuring Buried Cysteine Accessibility. J Biol Chem 286: 26375-26382.
3. Smith ML, Gourdon D, Little WC, Kubow KE, Eguiluz RA, et al. (2007) Force-induced unfolding of fibronectin in the extracellular matrix of living cells. PLoS Biol 5: e268.
4. Baneyx G, Baugh L, Vogel V, (2002) Fibronectin extension and unfolding within cell matrix fibrils controlled by cytoskeletal tension. Proc Natl Acad Sci U S A 99: 5139-5143.
5. Brown AE, Discher DE, (2009) Conformational changes and signaling in cell and matrix physics. Curr Biol 19: R781-789.
6. Johnson CP, Tang HY, Carag C, Speicher DW, Discher DE, (2007) Forced unfolding of proteins within cells. Science 317: 663-666.
7. Ohashi T, Kiehart DP, Erickson HP, (1999) Dynamics and elasticity of the fibronectin matrix in living cell culture visualized by fibronectin-green fluorescent protein. Proc Natl Acad Sci U S A 96: 2153-2158.
8. Meng F, Suchyna TM, Sachs F, (2008) A fluorescence energy transfer-based mechanical stress sensor for specific proteins in situ. FEBS J 275: 3072-3087.
9. Grashoff C, Hoffman BD, Brenner MD, Zhou R, Parsons M, et al. (2010) Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466: 263-266.
10. Meng F, Sachs F, (2011) Visualizing dynamic cytoplasmic forces with a compliance-matched FRET sensor. J Cell Sci 124: 261-269.
11. Kufer SK, Dietz H, Albrecht C, Blank K, Kardinal A, et al. (2005) Covalent immobilization of recombinant fusion proteins with hAGT for single molecule force spectroscopy. Eur Biophys J 35: 72-78.
12. Abu-Lail NI, Ohashi T, Clark RL, Erickson HP, Zauscher S, (2006) Understanding the elasticity of fibronectin fibrils: unfolding strengths of FN-III and GFP domains measured by single molecule force spectroscopy. Matrix Biol 25: 175-184.
13. Dietz H, Rief M, (2004) Exploring the energy landscape of GFP by single-molecule mechanical experiments. Proc Natl Acad Sci U S A 101: 16192-16197.
14. Mickler M, Dima RI, Dietz H, Hyeon C, Thirumalai D, et al. (2007) Revealing the bifurcation in the unfolding pathways of GFP by using single-molecule experiments and simulations. Proc Natl Acad Sci U S A 104: 20268-20273.
15. Perez-Jimenez R, Garcia-Manyes S, Ainavarapu SR, Fernandez JM, (2006) Mechanical unfolding pathways of the enhanced yellow fluorescent protein revealed by single molecule force spectroscopy. J Biol Chem 281: 40010-40014.
16. Hyeon C, Dima RI, Thirumalai D, (2006) Pathways and kinetic barriers in mechanical unfolding and refolding of RNA and proteins. Structure 14: 1633-1645.
17. Eyal E, Bahar I, (2008) Toward a molecular understanding of the anisotropic response of proteins to external forces: insights from elastic network models. Biophys J 94: 3424-3435.
18. Caraglio M, Imparato A, Pelizzola A, (2011) Direction-dependent mechanical unfolding and green fluorescent protein as a force sensor. Phys Rev E Stat Nonlin Soft Matter Phys 84: 021918.
19. Fowler SB, Best RB, Toca Herrera JL, Rutherford TJ, Steward A, et al. (2002) Mechanical unfolding of a titin Ig domain: structure of unfolding intermediate revealed by combining AFM, molecular dynamics simulations, NMR and protein engineering. J Mol Biol 322: 841-849.
20. Chen CS, (2008) Mechanotransduction- a field pulling together? J Cell Sci 121: 3285-3292.
21. Vogel V, (2006) Mechanotransduction involving multimodular proteins: converting force into biochemical signals. Annu Rev Biophys Biomol Struct 35: 459-488.
22. Ghosh K, Ingber DE, (2007) Micromechanical control of cell and tissue development: implications for tissue engineering. Adv Drug Deliv Rev 59: 1306-1318.
23. Lecuit T, Le Goff L, (2007) Orchestrating size and shape during morphogenesis. Nature 450: 189-192.
24. Schwartz MA, (2009) Cell biology. The force is with us. Science 323: 588-589.
25. Vogel V, Sheetz M, (2006) Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 7: 265-275.
26. DuFort CC, Paszek MJ, Weaver VM, (2011) Balancing forces: architectural control of mechanotransduction. Nat Rev Mol Cell Biol 12: 308-319.
27. Sotomayor M, Schulten K, (2007) Single-molecule experiments in vitro and in silico. Science 316: 1144-1148.
28. Thomas WE, Trintchina E, Forero M, Vogel V, Sokurenko EV, (2002) Bacterial adhesion to target cells enhanced by shear force. Cell 109: 913-923.
29. Lu H, Isralewitz B, Krammer A, Vogel V, Schulten K, (1998) Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophys J 75: 662-671.
30. Craig D, Gao M, Schulten K, Vogel V, (2004) Tuning the mechanical stability of fibronectin type III modules through sequence variations. Structure (Camb) 12: 21-30.
31. Hytonen VP, Vogel V, (2008) How force might activate talin's vinculin binding sites: SMD reveals a structural mechanism. PLoS Comput Biol 4: e24.
32. Chabria M, Hertig S, Smith ML, Vogel V, (2010) Stretching fibronectin fibres disrupts binding of bacterial adhesins by physically destroying an epitope. Nat Commun 1: 135.
33. Lv S, Dudek DM, Cao Y, Balamurali MM, Gosline J, et al. (2010) Designed biomaterials to mimic the mechanical properties of muscles. Nature 465: 69-73.
34. Schmidt C, Vogel V, (2010) Molecular shuttles powered by motor proteins: loading and unloading stations for nanocargo integrated into one device. Lab Chip 10: 2195-2198.
35. Rief M, Clausen-Schaumann H, Gaub HE, (1999) Sequence-dependent mechanics of single DNA molecules. Nat Struct Biol 6: 346-349.
36. Kufer SK, Puchner EM, Gumpp H, Liedl T, Gaub HE, (2008) Single-molecule cut-and-paste surface assembly. Science 319: 594-596.
37. Sharma D, Feng G, Khor D, Genchev GZ, Lu H, et al. (2008) Stabilization provided by neighboring strands is critical for the mechanical stability of proteins. Biophys J 95: 3935-3942.
38. Gao M, Craig D, Lequin O, Campbell ID, Vogel V, et al. (2003) Structure and functional significance of mechanically unfolded fibronectin type III1 intermediates. Proc Natl Acad Sci U S A 100: 14784-14789.
39. Dopf J, Horiagon TM, (1996) Deletion mapping of the Aequorea victoria green fluorescent protein. Gene 173: 39-44.
40. Li X, Zhang G, Ngo N, Zhao X, Kain SR, et al. (1997) Deletions of the Aequorea victoria green fluorescent protein define the minimal domain required for fluorescence. J Biol Chem 272: 28545-28549.
41. Heim R, Prasher DC, Tsien RY, (1994) Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc Natl Acad Sci U S A 91: 12501-12504.
42. Chattoraj M, King BA, Bublitz GU, Boxer SG, (1996) Ultra-fast excited state dynamics in green fluorescent protein: multiple states and proton transfer. Proc Natl Acad Sci U S A 93: 8362-8367.
43. Huang YM, Bystroff C, (2009) Complementation and reconstitution of fluorescence from circularly permuted and truncated green fluorescent protein. Biochemistry 48: 929-940.
44. Barstow B, Ando N, Kim CU, Gruner SM, (2008) Alteration of citrine structure by hydrostatic pressure explains the accompanying spectral shift. Proc Natl Acad Sci U S A 105: 13362-13366.
45. Jung K, Park J, Maeng P-J, Kim H, (2005) Fluorescence Quenching of Green Fluorescent Protein during Denaturation by Guanidine. Bull Korean Chem Soc 26: 413-417.
46. Yang F, Moss LG, Phillips GN Jr, (1996) The molecular structure of green fluorescent protein. Nat Biotechnol 14: 1246-1251.
47. Freddolino PL, Park S, Roux B, Schulten K, (2009) Force field bias in protein folding simulations. Biophys J 96: 3772-3780.
48. Freddolino PL, Schulten K, (2009) Common structural transitions in explicit-solvent simulations of villin headpiece folding. Biophys J 97: 2338-2347.
49. Lee EH, Hsin J, Sotomayor M, Comellas G, Schulten K, (2009) Discovery through the computational microscope. Structure 17: 1295-1306.
50. Lee EH, Hsin J, von Castelmur E, Mayans O, Schulten K, (2010) Tertiary and secondary structure elasticity of a six-Ig titin chain. Biophys J 98: 1085-1095.
51. Freddolino PL, Harrison CB, Liu Y, Schulten K, (2010) Challenges in protein folding simulations: Timescale, representation, and analysis. Nat Phys 6: 751-758.
52. Hsin J, Strumpfer J, Lee EH, Schulten K, (2011) Molecular origin of the hierarchical elasticity of titin: simulation, experiment, and theory. Annu Rev Biophys 40: 187-203.
53. Lee W, Strumpfer J, Bennett V, Schulten K, Marszalek PE, (2012) Mutation of conserved histidines alters tertiary structure and nanomechanics of consensus ankyrin repeats. J Biol Chem 287: 19115-19121.
54. Cheng S, Cetinkaya M, Grater F, (2010) How sequence determines elasticity of disordered proteins. Biophys J 99: 3863-3869.
55. Dittrich M, Freddolino PL, Schulten K, (2005) When light falls in LOV: a quantum mechanical/molecular mechanical study of photoexcitation in Phot-LOV1 of Chlamydomonas reinhardtii. J Phys Chem B 109: 13006-13013.
56. Nelson MT, Humphrey W, Gursoy A, Dalke A, Kale LV, et al. (1996) NAMD: A parallel, object oriented molecular dynamics program. International Journal of Supercomputer Applications and High Performance Computing 10: 251-268.
57. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. Journal of Physical Chemistry B 102: 3586-3616.
58. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML, (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79: 926-935.
59. Reuter N, Lin R, Thiel W, (2002) Green fluorescent proteins: Empirical force field for the neutral and deprotonated forms of the chromophore. Molecular dynamics simulation's of the wild type and S65T mutant. Journal of Physical Chemistry B 106: 6310-6321.
60. Darden T, York D, Pedersen L, (1993) Particle Mesh Ewald- an N.Log(N) Method for Ewald Sums in Large Systems. Journal of Chemical Physics 98: 10089-10092.
61. Farres J, Rechsteiner MP, Herold S, Frey AD, Kallio PT, (2005) Ligand binding properties of bacterial hemoglobins and flavohemoglobins. Biochemistry 44: 4125-4134.
62. Beaven GH, Holiday ER, (1952) Ultraviolet absorption spectra of proteins and amino acids. Adv Protein Chem 7: 319-386.
63. Fu CC, Lee HY, Chen K, Lim TS, Wu HY, et al. (2007) Characterization and application of single fluorescent nanodiamonds as cellular biomarkers. Proc Natl Acad Sci U S A 104: 727-732.
64. Lakowicz JR, Szmacinski H, Nowaczyk K, Berndt KW, Johnson M, (1992) Fluorescence lifetime imaging. Anal Biochem 202: 316-330.
65. Bastiaens PI, Squire A, (1999) Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in the cell. Trends Cell Biol 9: 48-52.
66. Heilemann M, Herten DP, Heintzmann R, Cremer C, Muller C, et al. (2002) High-resolution colocalization of single dye molecules by fluorescence lifetime imaging microscopy. Anal Chem 74: 3511-3517.
67. Wallrabe H, Periasamy A, (2005) Imaging protein molecules using FRET and FLIM microscopy. Curr Opin Biotechnol 16: 19-27.
68. Duncan RR, Bergmann A, Cousin MA, Apps DK, Shipston MJ, (2004) Multi-dimensional time-correlated single photon counting (TCSPC) fluorescence lifetime imaging microscopy (FLIM) to detect FRET in cells. J Microsc 215: 1-12.
69. Ruijgrok PV, Wuest R, Rebane AA, Renn A, Sandoghdar V, (2010) Spontaneous emission of a nanoscopic emitter in a strongly scattering disordered medium. Opt Express 18: 6360-6365.