Distinctive solvation patterns make renal osmolytes diverse

Biophysical Journal

Volumn 105, Issue 9, 2013, Pages 2166-2174

  Jackson Atogi, Ruby ^a   Sinha, Prem Kumar ^a   Rösgen, Jörg ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETAINE; INOSITOL; PHOSPHORYLCHOLINE; SOLVENT; SORBITOL; TAURINE;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; KIDNEY; METABOLISM; OSMOSIS; SOLUBILITY;

BETAINE; INOSITOL; KIDNEY; MODELS, MOLECULAR; MOLECULAR CONFORMATION; OSMOSIS; PHOSPHORYLCHOLINE; SOLUBILITY; SOLVENTS; SORBITOL; TAURINE;

EID: 84887344839     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.09.019     Document Type: Article

References (66)

1. A. Garcia-Perez, and M.B. Burg Renal medullary organic osmolytes Physiol. Rev. 71 1991 1081 1115
2. P.H. Yancey, and M.B. Burg Distribution of major organic osmolytes in rabbit kidneys in diuresis and antidiuresis Am. J. Physiol. 257 1989 F602 F607
3. T. Nakanishi, O. Uyama, and M. Sugita Osmotically regulated taurine content in rat renal inner medulla Am. J. Physiol. 261 1991 F957 F962
4. M.B. Burg, and P.F. Kador Sorbitol, osmoregulation, and the complications of diabetes J. Clin. Invest. 81 1988 635 640
5. D.P. Peterson, and K.M. Murphy P.H. Yancey Effects of dietary protein and salt on rat renal osmolytes: covariation in urea and GPC contents Am. J. Physiol. 263 1992 F594 F600
6. J.G. Kirkwood, and F.P. Buff The statistical mechanical theory of solutions. I J. Chem. Phys. 19 1951 774 777
7. A. Ben-Naim Inversion of the Kirkwood-Buff theory of solutions: application to water-ethanol system J. Chem. Phys. 67 1977 4884 4890
8. J. Rösgen, B.M. Pettitt, and D.W. Bolen Uncovering the basis for nonideal behavior of biological molecules Biochemistry 43 2004 14472 14484
9. D.R. Canchi, and P. Jayasimha A.E. Garcia Molecular mechanism for the preferential exclusion of TMAO from protein surfaces J. Phys. Chem. B 116 2012 12095 12104
10. J. Rösgen, B.M. Pettitt, and D.W. Bolen An analysis of the molecular origin of osmolyte-dependent protein stability Protein Sci. 16 2007 733 743
11. J. Rösgen, and R. Jackson-Atogi Volume exclusion and H-bonding dominate the thermodynamics and solvation of trimethylamine-N-oxide in aqueous urea J. Am. Chem. Soc. 134 2012 3590 3597
12. C. Tanford Extension of the theory of linked functions to incorporate the effects of protein hydration J. Mol. Biol. 39 1969 539 544
13. S.N. Timasheff The control of protein stability and association by weak interactions with water: how do solvents affect these processes? Annu. Rev. Biophys. Biomol. Struct. 22 1993 67 97
14. J.A. Schellman The thermodynamics of solvent exchange Biopolymers 34 1994 1015 1026
15. E.S. Courtenay, and M.W. Capp M.T. Record Jr. Thermodynamic analysis of interactions between denaturants and protein surface exposed on unfolding: interpretation of urea and guanidinium chloride m-values and their correlation with changes in accessible surface area (ASA) using preferential interaction coefficients and the local-bulk domain model Proteins, Suppl 4 2000 72 85
16. R. Chitra, and P.E. Smith Preferential interactions of cosolvents with hydrophobic solutes J. Phys. Chem. B 105 2001 11513 11522
17. S. Shimizu Estimating hydration changes upon biomolecular reactions from osmotic stress, high pressure, and preferential hydration experiments Proc. Natl. Acad. Sci. USA 101 2004 1195 1199
18. M. Auton, and D.W. Bolen Predicting the energetics of osmolyte-induced protein folding/unfolding Proc. Natl. Acad. Sci. USA 102 2005 15065 15068
19. D. Harries, and J. Rösgen A practical guide on how osmolytes modulate macromolecular properties Methods Cell Biol. 84 2008 679 735
20. M. Auton, D.W. Bolen, and J. Rösgen Structural thermodynamics of protein preferential solvation: osmolyte solvation of proteins, aminoacids, and peptides Proteins 73 2008 802 813
21. E.J. Guinn, and L.M. Pegram M.T. Record Jr. Quantifying why urea is a protein denaturant, whereas glycine betaine is a protein stabilizer Proc. Natl. Acad. Sci. USA 108 2011 16932 16937
22. J. Rösgen, B.M. Pettitt, and D.W. Bolen Protein folding, stability, and solvation structure in osmolyte solutions Biophys. J. 89 2005 2988 2997
23. R.E. MacMillen, and A.K. Lee Australian desert mice: independence of exogenous water Science 158 1967 383 385
24. T. Nakanishi, R.S. Balaban, and M.B. Burg Survey of osmolytes in renal cell lines Am. J. Physiol. 255 1988 C181 C191
25. O. Levillain, M. Schmolke, and W. Guder Influence of dehydratation on glycerophosphorylcholine and choline distribution along the rat nephron Pflügers Arch. 442 2001 218 222
26. E.F. Pettersen, and T.D. Goddard T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
27. Y. Liu, and D.W. Bolen The peptide backbone plays a dominant role in protein stabilization by naturally occurring osmolytes Biochemistry 34 1995 12884 12891
28. W. Zhang, and M.W. Capp M.T. Record Jr. Thermodynamic characterization of interactions of native bovine serum albumin with highly excluded (glycine betaine) and moderately accumulated (urea) solutes by a novel application of vapor pressure osmometry Biochemistry 35 1996 10506 10516
29. E.S. Courtenay, and M.W. Capp M.T. Record Jr. Vapor pressure osmometry studies of osmolyte-protein interactions: implications for the action of osmoprotectants in vivo and for the interpretation of "osmotic stress" experiments in vitro Biochemistry 39 2000 4455 4471
30. J. Hong, and M.W. Capp M.T. Record Preferential interactions in aqueous solutions of urea and KCl Biophys. Chem. 105 2003 517 532
31. J. Gibbs The Scientific Papers of J. Williard Gibbs Volume 1 1993 Ox Bow Press Woodbridge, CT
32. H. Kokubo, and J. Rösgen B.M. Pettitt Molecular basis of the apparent near ideality of urea solutions Biophys. J. 93 2007 3392 3407
33. J. Rösgen Molecular basis of osmolyte effects on protein and metabolites Methods Enzymol. 428 2007 459 486
34. J. Rösgen Molecular crowding and solvation: direct and indirect impact on protein reactions Methods Mol. Biol. 490 2009 195 225
35. E. Matteoli, and L. Lepori Solute solute interactions in water. 2. An analysis through the Kirkwood-Buff integrals for 14 organic solutes J. Chem. Phys. 80 1984 2856 2863
36. D. Lide CRC Handbook of Chemistry and Physics 2004 CRC Press Boca Raton, FL
37. R. Koradi, M. Billeter, and K. Wüthrich MOLMOL: a program for display and analysis of macromolecular structures J. Mol. Graph. 14 1996 51 55 29-32
38. A.W. Schüttelkopf, and D.M. van Aalten PRODRG: a tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr. D Biol. Crystallogr. 60 2004 1355 1363
39. G.J. Kleywegt, and T.A. Jones Databases in protein crystallography Acta Crystallogr. D Biol. Crystallogr. 54 1998 1119 1131
40. S.S. Cho, and G. Reddy D. Thirumalai Entropic stabilization of proteins by TMAO J. Phys. Chem. B 115 2011 13401 13407
41. G. Barone, and P. Cacace V. Elia Excess thermodynamic properties of myo-inositol and polyhydric alcohols in water at 25 C Carbohyd. Res. 119 1983 1 11
42. I.N. Rabinowitz, and J. Kraut The crystal structure of myo-inositol Acta Crystallogr. 17 1964 159 168
43. H. Sutherland, and D. Young The crystal and molecular structure of taurine Acta Crystallogr. 16 1963 897 901
44. S. Abrahamsson, and I. Pascher Crystal and molecular structure of L-α-glycerylphosphorylcholin Acta Crystallogr. 21 1966 79 87
45. C. Romero, and A. Albis J. Sancho Thermodynamic study of the influence of polyols and glucose on the thermal stability of holo-bovine α-lactalbumin J. Therm. Anal. Calorim. 98 2009 1 7
46. M.A. Kabayama, and D. Patterson The thermodynamics of mutarotation of some sugars: II. Theoretical considerations Can. J. Chem. 36 1958 563 573
47. D.T. Warner Some possible relationships of carbohydrates and other biological components with the water structure at 37 Nature 196 1962 1055 1058
48. M.F. Chaplin A proposal for the structuring of water Biophys. Chem. 83 2000 211 221
49. R. Politi, L. Sapir, and D. Harries The impact of polyols on water structure in solution: a computational study J. Phys. Chem. A 113 2009 7548 7555
50. A. Boscaino, and K.J. Naidoo The extent of conformational rigidity determines hydration in nonaromatic hexacyclic systems J. Phys. Chem. B 115 2011 2608 2616
51. W.K. Lim, J. Rösgen, and S.W. Englander Urea, but not guanidinium, destabilizes proteins by forming hydrogen bonds to the peptide group Proc. Natl. Acad. Sci. USA 106 2009 2595 2600
52. P.E. Mason, and G.W. Neilson J.M. Cruickshank The hydration structure of guanidinium and thiocyanate ions: implications for protein stability in aqueous solution Proc. Natl. Acad. Sci. USA 100 2003 4557 4561
53. M.K. Gilson, and K.K. Irikura Symmetry numbers for rigid, flexible, and fluxional molecules: theory and applications J. Phys. Chem. B 114 2010 16304 16317
54. M. Frankel Zur kenntnis der assoziationstendenz von aminosäuren in wässeriger lösung Biochem. Z. 217 1930 378 388
55. A. Buche, P. Colson, and C. Houssier Effect of organic effectors on chromatin solubility, DNA-histone H1 interactions, DNA and histone H1 structures J. Biomol. Struct. Dyn. 11 1993 95 119
56. J.G. Jacobsen, and L.H. Smith Biochemistry and physiology of taurine and taurine derivatives Physiol. Rev. 48 1968 424 511
57. Y. Okaya Refinement of the crystal structure of taurine 2-aminoethylsulfonic acid. An example of computer-controlled experimentation Acta Crystallogr. 21 1966 726 735
58. K. Ohno, Y. Mandai, and H. Matsuura Vibrational spectra and molecular conformation of taurine and its related compounds J. Mol. Struct. 268 1992 41 50
59. J. Rösgen, and R. Jackson-Atogi Correction to volume exclusion and H-bonding dominate the thermodynamics and solvation of trimethylamine-N-oxide in aqueous urea J. Am. Chem. Soc. 134 2012 14263
60. T. Shikata Dielectric relaxation behavior of glycine betaine in aqueous solution J. Phys. Chem. A 106 2002 7664 7670
61. A. Lerbret, and P.E. Mason J.W. Brady Molecular dynamics studies of the conformation of sorbitol Carbohydr. Res. 344 2009 2229 2235
62. A. Schiefner, and J. Breed E. Bremer Cation-pi interactions as determinants for binding of the compatible solutes glycine betaine and proline betaine by the periplasmic ligand-binding protein ProX from Escherichia coli J. Biol. Chem. 279 2004 5588 5596
63. P.H. Yancey, and G.N. Somero Counteraction of urea destabilization of protein structure by methylamine osmoregulatory compounds of elasmobranch fishes Biochem. J. 183 1979 317 323
64. T. Arakawa, and S.N. Timasheff The stabilization of proteins by osmolytes Biophys. J. 47 1985 411 414
65. G.S. Ratnaparkhi, and R. Varadarajan Osmolytes stabilize ribonuclease S by stabilizing its fragments S protein and S peptide to compact folding-competent states J. Biol. Chem. 276 2001 28789 28798
66. J. Hong, and M.W. Capp M.T. Record Jr. Use of urea and glycine betaine to quantify coupled folding and probe the burial of DNA phosphates in lac repressor-lac operator binding Biochemistry 44 2005 16896 16911