Quinary protein structure and the consequences of crowding in living cells: Leaving the test-tube behind

BioEssays

Volumn 35, Issue 11, 2013, Pages 984-993

  Wirth, Anna Jean ^a   Gruebele, Martin ^a,b,c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b University of Illinois at Urbana Champaign   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Association; In vivo; Protein folding; Signaling

Indexed keywords

PROTEIN; WATER;

ARTICLE; CYTOPLASM; HYDRODYNAMICS; IN VIVO STUDY; MACROMOLECULAR CROWDING; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STRUCTURE; QUINARY STRUCTURE; WHOLE CELL;

ASSOCIATION; IN VIVO; PROTEIN FOLDING; SIGNALING;

CELL LINE; CYTOPLASM; HUMANS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEINS; SIGNAL TRANSDUCTION; WATER;

EID: 84885372912     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201300080     Document Type: Article

References (90)

1. Gierasch LM, Gershenson A. 2009. Post-reductionist protein science, or putting Humpty Dumpty back together again. Nat Chem Biol 5: 774-7.
2. Kuczera K, Gao J, Tidor B, Karplus M. 1990. Free energy of sickling. A simulation analysis. Proc Natl Acad Sci USA 87: 8481-5.
3. Martin RB. 1998. Free energies and equilibria of peptide bond hydrolysis and formation. Biopolymers 45: 351-3.
4. Srere PA. 1987. Complexes of sequential metabolic enzymes. Annu Rev Biochem 56: 89-124.
5. McConkey EH. 1982. Molecular evolution, intracellular organization, and the quinary structure of proteins. Proc Natl Acad Sci USA 79: 3236-40.
6. Kim SJ, Dumont C, Gruebele M. 2008. Simulation-based fitting of protein-protein interaction potentials to SAXS experiments. Biophys J 94: 4924-31.
7. Minton AP. 1981. Excluded volume as a determinant of macromolecular structure and reactivity. Biopolymers 20: 2093-120.
8. Minton AP. 2001. The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J Biol Chem 276: 10577-80.
9. Cheung MS, Klimov D, Thirumalai D. 2005. Molecular crowding enhances native state stability and refolding rates of globular proteins. Proc Natl Acad Sci USA 102: 4753-8.
10. Perham M, Stagg L, Wittung-Stafshede P. 2007. Macromolecular crowding increases structural content of folded proteins. FEBS Lett 581: 5065-9.
11. Minton AP. 2005. Models for excluded volume interaction between an unfolded protein and rigid macromolecular cosolutes: macromolecular crowding and protein stability revisited. Biophys J 88: 971-85.
12. Dhar A, Samiotakis A, Ebbinghaus S, Nienhaus L, et al. 2010. Structure, function, and folding of phosphoglycerate kinase are strongly perturbed by macromolecular crowding. Proc Natl Acad Sci USA 107: 17586-91.
13. Hong JA, Gierasch LM. 2010. Macromolecular crowding remodels the energy landscape of a protein by favoring a more compact unfolded state. J Am Chem Soc 132: 10445-52.
14. Zhou H-X, Rivas G, Minton AP. 2008. Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Annu Rev Biophys 37: 375-97.
15. Qin S, Zhou H-X. 2009. Atomistic modeling of macromolecular crowding predicts modest increases in protein folding and binding stability. Biophys J 97: 12-9.
16. McGuffee SR, Elcock AH. 2010. Diffusion, crowding & protein stability in a dynamic molecular model of the bacterial cytoplasm. PLoS Comput Biol 6: e1000694.
17. Wang Q, Zhuravleva A, Gierasch LM. 2011. Exploring weak, transient protein-protein interactions in crowded in vivo environments by in-cell nuclear magnetic resonance spectroscopy. Biochemistry 50: 9225-36.
18. Verkman AS. 2002. Solute and macromolecule diffusion in cellular aqueous compartments. Trends Biochem Sci 27: 27-33.
19. Dix JA, Verkman AS. 2008. Crowding effects on diffusion in solutions and cells. Annu Rev Biophys 37: 247-63.
20. Weber SC, Spakowitz AJ, Theriot JA. 2012. Nonthermal ATP-dependent fluctuations contribute to the in vivo motion of chromosomal loci. Proc Natl Acad Sci USA 109: 7338-43.
21. Wang Y, Li C, Pielak GJ. 2010. Effects of proteins on protein diffusion. J Am Chem Soc 132: 9392-7.
22. Harada R, Tochio N, Kigawa T, Sugita Y, et al. 2013. Reduced native state stability in crowded cellular environment due to protein-protein interactions. J Am Chem Soc 135: 3696-701.
23. Dixit PD, Maslov S. 2013. Evolutionary capacitance and control of protein stability in protein-protein interaction networks. PLoS Comput Biol 9: e1003023.
24. Bamford C, Tipper C, Compton R. 1985. Diffusion-Limited Reactions. Elsevier. p. 213-53.
25. Wolynes PG. 1976. Slip boundary conditions and the hydrodynamic effect on diffusion controlled reactions. J Chem Phys 65: 450.
26. Frembgen-Kesner T, Elcock AH. 2010. Absolute protein-protein association rate constants from flexible, coarse-grained Brownian dynamics simulations: the role of intermolecular hydrodynamic interactions in Barnase-Barstar association. Biophys J 99: L75-7.
27. Frembgen-Kesner T, Elcock AH. 2009. Striking effects of hydrodynamic interactions on the simulated diffusion and folding of proteins. J Chem Theory Comput 5: 242-56.
28. Ando T, Skolnick J. 2013. On the importance of hydrodynamic interactions in lipid membrane formation. Biophys J 104: 96-105.
29. Williams MA, Goodfellow JM, Thornton JM. 1994. Buried waters and internal cavities in monomeric proteins. Protein Sci 3: 1224-35.
30. Timasheff SN. 2002. Protein hydration, thermodynamic binding, and preferential hydration. Biochemistry 41: 13473-82.
31. Ebbinghaus S, Kim SJ, Heyden M, Yu X, et al. 2007. An extended dynamical hydration shell around proteins. Proc Natl Acad Sci USA 104: 20749-52.
32. Persson E, Halle B. 2008. Cell water dynamics on multiple time scales. Proc Natl Acad Sci USA 105: 6266-71.
33. Meister K, Ebbinghaus S, Xu Y, Duman JG, et al. 2013. Long-range protein-water dynamics in hyperactive insect antifreeze proteins. Proc Natl Acad Sci USA 110: 1617-22.
34. Papoian GA, Ulander J, Wolynes PG. 2003. Role of water mediated interactions in protein-protein recognition landscapes. J Am Chem Soc 125: 9170-8.
35. Langhorst U, Backmann J, Loris R, Steyaert J. 2000. Analysis of a water mediated protein-protein interactions within RNase T1. Biochemistry 39: 6586-93.
36. Reichmann D, Phillip Y, Carmi A, Schreiber G. 2008. On the contribution of water-mediated interactions to protein-complex stability. Biochemistry 47: 1051-60.
37. Ikura T, Urakubo Y, Ito N. 2004. Water-mediated interaction at a protein-protein interface. Chem Phys 307: 111-9.
38. Nooren I, Thornton JM. 2003. Diversity of protein-protein interactions. EMBO J 22: 3486-92.
39. Sekhar A, Lam HN, Cavagnero S. 2012. Protein folding rates and thermodynamic stability are key determinants for interaction with the Hsp70 chaperone system. Protein Sci 21: 1489-502.
40. Welsh MJ, Dedman JR, Brinkley BR, Means AR. 1978. Calcium-dependent regulator protein: localization in mitotic apparatus of eukaryotic cells. Proc Natl Acad Sci USA 75: 1867-71.
41. Bowie JU, Sauer RT. 1989. Equilibrium dissociation and unfolding of the arc repressor dimer. Biochemistry 28: 7139-43.
42. Ou L, Ferreira AM, Otieno S, Xiao L, et al. 2011. Incomplete folding upon binding mediates Cdk4/Cyclin D complex activation by tyrosine phosphorylation of inhibitor p27 protein. J Biol Chem 286: 30142-51.
43. Ovádi J, Srere PA. 2000. Macromolecular compartmentation and channeling. Int Rev Cytol 192: 255-80.
44. Dang CV, Ferguson B, Burke DJ, Garcia V, et al. 1985. Interactions of aminoacyl-tRNA synthetases in high-molecular-weight multienzyme complexes from rat liver. Biochim Biophys Acta 829: 319-26.
45. Lee SW, Cho BH, Park SG, Kim S. 2004. Aminoacyl-tRNA synthetase complexes: beyond translation. J Cell Sci 117: 3725-34.
46. Hausmann CD, Ibba M. 2008. Aminoacyl-tRNA synthetase complexes: molecular multitasking revealed. FEMS Microbiol Rev 32: 705-21.
47. Guo M, Ignatov M, Musier-Forsyth K, Schimmel P, et al. 2008. Crystal structure of tetrameric form of human lysyl-tRNA synthetase: implications for multisynthetase complex formation. Proc Natl Acad Sci USA 105: 2331-6.
48. Weber SC, Brangwynne CP. 2012. Getting RNA and protein in phase. Cell 149: 1188-91.
49. Muschol M, Rosenberger F. 1997. Liquid-liquid phase separation in supersaturated lysozyme solutions and associated precipitate formation/crystallization. J Chem Phys 107: 1953.
50. Brangwynne CP, Eckmann CR, Courson DS, Rybarska A, et al. 2009. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324: 1729-32.
51. Li P, Banjade S, Cheng H-C, Kim S, et al. 2012. Phase transitions in the assembly of multivalent signalling proteins. Nature 483: 336-40.
52. Wu H. 2013. Higher-order assemblies in a new paradigm of signal transduction. Cell 153: 287-92.
53. Denos S, Dhar A, Gruebele M. 2012. Crowding effects on the small, fast-folding protein lambda(6-85). Faraday Discuss 157: 451-62.
54. Cino EA, Karttunen M, Choy WY. 2012. Effects of molecular crowding on the dynamics of intrinsically disordered proteins. PLoS ONE 7: e49876.
55. Cai W, Hong H, (eds). 2012. Protein-protein interactions - computational and experimental tools. InTech, New York, DOI: 10.5772/2679
56. Renault M, Tommassen-van Boxtel R, Bos MP, Post JA, et al. 2012. Cellular solid-state nuclear magnetic resonance spectroscopy. Proc Natl Acad Sci USA 109: 4863-8.
57. Selenko P, Wagner G. 2007. Looking into live cells with in-cell NMR spectroscopy. J Struct Biol 158: 244-53.
58. Ghaemmaghami S, Oas TG. 2001. Quantitative protein stability measurement in vivo. Nat Struct Biol 8: 879-82.
59. Xu K, Zhong G, Zhuang X. 2013. Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 339: 452-6.
60. Jones SA, Shim S-H, He J, Zhuang X. 2011. Fast, three-dimensional super-resolution imaging of live cells. Nat Methods 8: 499-505.
61. Ebbinghaus S, Gruebele M. 2011. Protein folding landscapes in the living cell. J Phys Chem Lett 2: 314-9.
62. Zuzuarregui A, Kupka T, Bhatt B, Dohnal I, et al. 2012. M-Track: detecting short-lived protein-protein interactions in vivo. Nat Methods 9: 594-6.
63. Gallego O, Specht T, Brach T, Kumar A, et al. 2013. Detection and characterization of protein interactions in vivo by a simple live-cell imaging method. PLoS ONE 8: e62195.
64. Wang Q, Cheung MS. 2012. A physics-based approach of coarse-graining the cytoplasm of Escherichia coli (CGCYTO). Biophys J 102: 2353-61.
65. Roberts E, Stone JE, Luthey-Schulten Z. 2013. Lattice microbes: high-performance stochastic simulation method for the reaction-diffusion master equation. J Comp Chem 34: 245-55.
66. Douglas J, Dudowicz J, Freed K. 2009. Crowding induced self-assembly and enthalpy-entropy compensation. Phys Rev Lett 103: 135701.
67. Kim YC, Mittal J. 2012. Crowding induced entropy-enthalpy compensation in protein association equilibria. Phys Rev Lett 110: 208102.
68. Jiao M, Li H-T, Chen J, Minton AP, et al. 2010. Attractive protein-polymer interactions markedly alter the effect of macromolecular crowding on protein association equilibria. Biophys J 99: 914-23.
69. Rosen J, Kim YC, Mittal J. 2011. Modest protein-crowder attractive interactions can counteract enhancement of protein association by intermolecular excluded volume interactions. J Phys Chem B 115: 2683-9.
70. Ebbinghaus S, Dhar A, McDonald D, Gruebele M. 2010. Protein folding stability and dynamics imaged in a living cell. Nat Methods 7: 319-23.
71. Ignatova Z, Gierasch LM. 2004. Monitoring protein stability and aggregation in vivo by real-time flourescent labeling. Proc Natl Acad Sci USA 101: 523-8.
72. Ignatova Z, Krishnan B, Bombardier JP, Marcelino AMC, et al. 2007. From the test tube to the cell: exploring the floding and aggregation of a beta-clam protein. Biopolymers 88: 157-63.
73. Phillip Y, Kiss V, Schreiber G. 2012. Protein-binding dynamics imaged in a living cell. Proc Natl Acad Sci USA 109: 1461-6.
74. Mir M, Wang Z, Shen Z, Bednarz M, et al. 2011. Optical measurement of cycle-dependent cell growth. Proc Nat Acad Sci USA 108: 13124-9.
75. Tzur A, Kafri R, LeBleu VS, Lahav G, et al. 2009. Cell growth and size homeostasis in proliferating animal cells. Science 325: 167.
76. Hinde E, Cardarelli F, Digman MA, Gratton E. 2012. Changes in chromatin compaction during the cell cycle revealed by micrometer-scale measurement of molecular flow in the nucleus. Biophys J 102: 691-7.
77. Hynes TR, Randal M, Kennedy LA, Eigenbrot C, et al. 1990. X-ray crystal-structure of the protease inhibitor domain of alzheimers amyloid beta-protein precursor. Biochemistry 29: 10018-22.
78. Buczek O, Krowarsch D, Otlewski J. 2002. Thermodynamics of single peptide bond cleavage in bovine pancreatic trypsin inhibitor (BPTI). Protein Sci 11: 924-32.
79. Scholtz JM, Baldwin RL. 1992. The mechanism of alpha-helix formation by peptides. Annu Rev Biophys Biomol Struct 21: 95-118.
80. Wieczorek R, Dannenberg JJ. 2005. Enthalpies of hydrogen-bonds in α-helical peptides. An ONIOM DFT/AM1 study. J Am Chem Soc 127: 14534-5.
81. Doig AJ, Williams DH. 1991. Is the hydrophobic effect stabilizing or destabilizing in proteins? Exp Cell Res 217: 389-98.
82. Jones K, Wittung-Stafshede P. 2003. The largest protein observed to fold by two-state kinetic mechanism does not obey contact-order correlation. J Am Chem Soc 125: 9606-7.
83. Nguyen H, Jäger M, Kelly J, Gruebele M. 2005. Engineering beta-sheet protein toward the folding speed limit. J Phys Chem B 109: 15182-6.
84. Shiroishi M, Yokota A, Tsumoto K, Kondo H, et al. 2001. Structural evidence for entropic contribution of salt bridge formation to a protein antigen-antibody interaction. The case of hen lysozyme-HyHEL-10 Fv complex. J Biol Chem 276: 23042-50.
85. Fersht AR. 1987. The hydrogen bond in molecular recognition. Trends Biochem Sci 12: 301-4.
86. Klotz IM, Langebman NR, Dahnall DW. 1970. Quaternary structure of proteins. Annu Rev Biochem 39: 25-62.
87. Vaynberg J, Fukuda T, Chen K, Vinogradova O, et al. 2005. Structure of an ultraweak protein-protein complex and its crucial role in regulation of cell morphology and motility. Mol Cell 17: 513-23.
88. Huang X, Poy F, Zhang RG, Joachimiak A, et al. 2000. Structure of a WW domain containing fragment of dystrophin in complex with beta-dystroglycan. Nat Struct Biol 7: 634-8.
89. Shaanan B. 1983. Structure of human oxyhemoglobin at 2.1Å resolution. J Mol Biol 171: 31-59.
90. Pellicena P, Karow DS, Boon EM, Marletta MA, et al. 2004. Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases. Proc Natl Acad Sci USA 101: 12854-9.