Intracellular pH modulates quinary structure

Protein Science

Volumn , Issue , 2015, Pages 1748-1755

  Cohen, Rachel D ^a   Guseman, Alex J ^a   Pielak, Gary J ^a,b,c  

^a The University of North Carolina at Chapel Hill   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

amide proton exchange; in cell NMR; macromolecular crowding; pH; protein stability; quinary interactions

Indexed keywords

AMIDE; PROTEIN G; PROTEIN VARIANT;

AMINO ACID SEQUENCE; ARTICLE; CELL PH; CONTROLLED STUDY; EQUILIBRIUM CONSTANT; ESCHERICHIA COLI; IN VITRO STUDY; MACROMOLECULAR CROWDING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STABILITY; STRUCTURE ANALYSIS;

EID: 84973596353     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2765     Document Type: Article

References (67)

1. Pace CN, Grimsley GR, Scholtz JM (2009) Protein ionizable groups: pK values and their contribution to protein stability and solubility. J Biol Chem 284:13285–13289.
2. Zimmerman SB, Trach SO (1991) Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. J Mol Biol 222:599–620.
3. 13C] histidine. Science 188:266–268.
4. Serber Z, Keatinge-Clay AT, Ledwidge R, Kelly AE, Miller SM, Dötsch V (2001) High-resolution macromolecular NMR spectroscopy in living cells. J Am Chem Soc 123:2446–2447.
5. Smith AE, Zhang Z, Pielak GJ, Li C (2015) NMR studies of protein folding and binding in cells and cell-like environments. Curr Opin Struct Biol 30:7–16.
6. Wang Y, Sarkar M, Smith AE, Krois AS, Pielak GJ (2012) Macromolecular crowding and protein stability. J Am Chem Soc 134:16614–16618.
7. Benton LA, Smith AE, Young GB, Pielak GJ (2012) Unexpected effects of macromolecular crowding on protein stability. Biochemistry 51:9773–9775.
8. Senske M, Törk L, Born B, Havenith M, Herrmann C, Ebbinghaus S (2014) Protein stabilization by macromolecular crowding through enthalpy rather than entropy. J Am Chem Soc 136:9036–9041.
9. Sapir L, Harries D (2015) Is the depletion force entropic? Molecular crowding beyond steric interactions. Curr Opin Colloid Interface Sci 20:3–10.
10. McConkey EH (1982) Molecular evolution, intracellular organization, and the quinary structure of proteins. Proc Natl Acad Sci USA 79:3236–3240.
11. Srere PA (1987) Complexes of sequential metabolic enzymes. Annu Rev Biochem 56:89–124.
12. Wirth AJ, Gruebele M (2013) Quinary protein structure and the consequences of crowding in living cells: leaving the test-tube behind. Bioessays 35:984–993.
13. Gershenson A (2014) Deciphering protein stability in cells. J Mol Biol 426:4–6.
14. Majumder S, Xue J, DeMott CM, Reverdatto S, Burz DS, Shekhtman A (2015) Probing protein quinary interactions by in-cell nuclear magnetic resonance spectroscopy. Biochemistry 54:2727–2738.
15. Monteith WB, Cohen RD, Smith AE, Guzman-Cisneros E, Pielak GJ (2015) Quinary structure modules protein stability in cells. Proc Natl Acad Sci USA 112:1739–1742.
16. Kyne C, Ruhle B, Gautier VW, Crowley PB (2015) Specific ion effects on macromolecular interactions in Escherichia coli extracts. Protein Sci 24:310–318.
17. Gronenborn AM, Filpula DR, Essig NZ, Achari A, Whitlow M, Wingfield PT, Clore GM (1991) A novel, highly stable fold of the immunoglobulin binding domain of Streptococcal protein G. Science 253:657–660.
18. Gallagher T, Alexander P, Bryan P, Gilliland GL (1994) Two crystal structures of the B1 immunoglobulin-binding domain of streptococcal protein G and comparison with NMR. Biochemistry 33:4721–4729.
19. Reardon PN, Spicer LD (2005) Multidimensional NMR spectroscopy for protein characterization and assignment inside cells. J Am Chem Soc 127:10848–10849.
20. Crowley PB, Chow E, Papkovskaia T (2011) Protein interactions in the Escherichia coli cytosol: an impediment to in-cell NMR spectroscopy. ChemBiochem 12:1043–1048.
21. 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 50:9225–9236.
22. Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181:223–230.
23. Sarkar M, Li C, Pielak GJ (2013) Soft interactions and crowding. Biophys Rev 5:187–194.
24. Minton AP (1981) Excluded volume as a determinant of macromolecular structure and reactivity. Biopolymers 20:2093–2120.
25. Linderstrøm-Lang K (1924) On the ionisation of proteins. CR Trav Lab Carlsberg 15:1–29.
26. Matthew JB, Richards FM (1983) The pH dependence of hydrogen exchange in proteins. J Biol Chem 258:3039–3044.
27. Yang A, Honig B (1993) On the pH dependence of protein stability. J Mol Biol 231:459–474.
28. Myer YP, Harbury HA (1965) Optical rotatory dispersion of cytochrome c. Proc Natl Acad Sci USA 54:1391–1398.
29. Myer YP (1968) Conformation of cytochromes. III. Effect of urea, temperature, extrinsic ligands, and pH variation on the conformation of horse heart ferricytochrome c. Biochemistry 7:765–775.
30. Jeng M-F, Englander SW (1991) Stable submolecular folding units in a non-compact form of cytochrome c. J Mol Biol 221:1045–1061.
31. Fink AL, Calciano LJ, Goto Y, Kurotsu T, Palleros DR (1994) Classification of acid denaturation of proteins: intermediates and unfolded states. Biochemistry 33:12504–12511.
32. Yang A, Honig B (1994) Structural origins of pH and ionic strength effects on protein stability: acid denaturation of sperm whale apomyoglobin. J Mol Biol 237:602–614.
33. Spitzer J, Poolman B (2009) The role of biomacromolecular crowding, ionic strength, and physicochemical gradients in the complexities of life's emergence. Microbiol Mol Biol Rev 73:371–388.
34. Zhou P, Wagner G (2010) Overcoming the solubility limit with solubility-enhancement tags: successful applications in biomolecular NMR studies. J Biomol NMR 46:23–31.
35. Englander SW, Kallenbach NR (1983) Hydrogen exchange and structural dynamics of proteins and nucleic acids. Q Rev Biophys 16:521–655.
36. 1H exchange to asses macromolecular crowding effects on globular-protein stability. Methods Enzymol 466:1–16.
37. Linderstrøm-Lang K. Deuterium exchange and protein structure. In: Neuberger A, Ed. (1958) Symposium on protein structure. London: Methuen.
38. Hvidt AA, Nielsen SO (1966) Hydrogen exchange in proteins. Adv Protein Chem 21:287–386.
39. Molday RS, Englander SW, Kallen RG (1972) Primary structure effects on peptide group hydrogen exchange. Biochemistry 11:150–158.
40. Bai Y, Milne JS, Mayne L, Englander SW (1993) Primary structure effects on peptide group hydrogen exchange. Proteins 17:75–86.
41. Smith AE, Zhou LZ, Pielak GJ (2015) Hydrogen exchange of disordered proteins in Escherichia coli. Protein Sci 24:706–713.
42. Smith AE, Sarkar M, Young GB, Pielak GJ (2013) Amide proton exchange of a dynamic loop in cell extracts. Protein Sci 22:1313–1319.
43. Zhang YZ (1995) Protein and peptide structure and interactions studied by hydrogen exchange and NMR. PhD Dissertation, University of Pennsylvania, Philadelphia.
44. Alexander P, Orban J, Bryan P (1992) Kinetic analysis of folding and unfolding the 56 amino acid IgG-binding domain of streptococcal protein G. Biochemistry 31:7243–7248.
45. Monteith WB, Pielak GJ (2014) Residue level quantification of protein stability in living cells. Proc Natl Acad Sci USA 111:11336–11340.
46. Englander SW, Sosnick TR, Englander JJ, Mayne L (1996) Mechanisms and uses of hydrogen exchange. Curr Opin Struct Biol 6:18–23.
47. McAllister RG, Konermann L (2015) Challenges in the interpretation of protein H/D exchange data: a molecular dynamics simulation perspective. Biochemistry 54:2683–2692.
48. Orban J, Alexander P, Bryan P, Khare D (1995) Assessment of stability differences in the protein G B1 and B2 domains from hydrogen-deuterium exchange: comparison with calorimetric data. Biochemistry 34:15291–15300.
49. Shimba N, Serber Z, Ledwidge R, Miller SM, Craik CS, Dötsch V (2003) Quantitative identification of the protonation state of histidines in vitro and in vivo. Biochemistry 42:9227–9234.
50. Davison TS, Nie X, Ma W, Lin Y, Kay C, Benchimol S, Arrowsmith CH (2001) Structure and functionality of a designed p53 dimer. J Mol Biol 307:605–617.
51. Henderson LJ (1908) Concerning the relationship between the strength of acids and their capacity to preserve neutrality. Am J Physiol 21:173–179.
52. Hasselbalch K (1916) Die Berechnung der Wasserstoffzahl des blutes auf der freien und gebundenen Kohlensaure desselben, und die Sauerstoffbindung des Blutes als Funktion der Wasserstoffzahl. Biochemistry Z 78:112–144.
53. Kelly AE, Ou HD, Withers R, Dötsch V (2002) Low-conductivity buffers for high-sensitivity NMR measurements. J Am Chem Soc 124:12013–12019.
54. Bryant JE, Lecomte JTJ, Lee AL, Young GB, Pielak GJ (2005) Protein dynamics in living cells (Retracted article. See vol 46, pg 8206). Biochemistry 44:9275–9279.
55. a measurements from nuclear magnetic resonance for the B1 and B2 immunoglobulin G-binding domains of protein G: comparison with calculated values for nuclear magnetic resonance and X-ray structures. Biochemistry 36:3580–3589.
56. Waudby CA, Camilloni C, Fitzpatrick AWP, Cabrita LD, Dobson CM, Vendruscolo M, Christodoulou J (2013) In-cell NMR characterization of the secondary structure populations of a disordered conformation of α-synuclein within E. coli cells. PloS ONE 8:e72286.
57. 1H NMR assignments and secondary structure of the streptococcal protein G B1-domain. Biochemistry 31:3604–3611.
58. Cummings JH, Macfarlane GT (1991) The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol 70:443–459.
59. Li C, Charlton LM, Lakkavaram A, Seagle C, Wang G, Young GB, Macdonald JM, Pielak GJ (2008) Differential dynamical effects of macromolecular crowding on an intrinsically disordered protein and a globular protein: implications for in-cell NMR spectroscopy. J Am Chem Soc 130:6310–6311.
60. Schlesinger AP, Wang Y, Tadeo X, Millet O, Pielak GJ (2011) Macromolecular crowding fails to fold a globular protein in cells. J Am Chem Soc 133:8082–8085.
61. Rule GS, Hitchens TK (2007) Fundamentals of protein NMR spectroscopy. Springer: Dordrecht.
62. Pielak GJ, Li C, Miklos AC, Schlesinger AP, Slade KM, Wang G-F, Zigoneanu IG (2009) Protein nuclear magnetic resonance under physiological conditions. Biochemistry 2009:226–234.
63. Minhaz Ud-Dean SM (2009) Nanoreactors for pH controlled sequential activity switching in multistep enzymatic processes. IET Nanobiotechnol 3:65–70.
64. Li L, Sham YY, Bikadi Z, Elmquist WF (2011) pH-dependent transport of pemetrexed by breast cancer resistance protein. Drug Metab Dispos 39:1478–1485.
65. Glasoe PK, Long FA (1960) Use of glass electrodes to measure acidities in deuterium oxide. J Phys Chem 64:188–190.
66. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277–293.
67. Johnson BA, Blevins RA (1994) NMR View: a computer program for the visualization and analysis of NMR data. J Biomol NMR 4:603–614.