Small molecule pharmacological chaperones: From thermodynamic stabilization to pharmaceutical drugs

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1764, Issue 11, 2006, Pages 1677-1687

  Arakawa, Tsutomu ^a   Ejima, Daisuke ^b   Kita, Yoshiko ^a   Tsumoto, Kouhei ^c  

^a ALLIANCE PROTEIN LABORATORIES   (United States)

^b AJINOMOTO CO INC   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Chemical chaperone; Osmolyte; Pharmacological chaperone; Stabilization

Indexed keywords

1 DEOXYGALACTONORIJIMYCIN; ALPHA GALACTOSIDASE; CHAPERONE; ENZYME INHIBITOR; GLYCEROL; MUTANT PROTEIN; N (NONYL)DEOXYNOJIRIMYCIN; QUINOLIZIDINE DERIVATIVE; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; CELL DEATH; CONFORMATIONAL TRANSITION; DIABETES MELLITUS; FABRY DISEASE; GAUCHER DISEASE; GENE MUTATION; HUMAN; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW; TEMPERATURE DEPENDENCE; THERMODYNAMICS; VIRUS INFECTION;

PHARMACEUTICAL PREPARATIONS; PROTEIN FOLDING; PROTEINS; THERMODYNAMICS;

EID: 33846020543     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2006.08.012     Document Type: Review

References (134)

1. Alberch J., Perez-Navarro E., and Canals J.M. Neurotrophic factors in Huntington's disease. Prog. Brain Res. 146 (2004) 195-229
2. Johnston T.H., and Brotchie J.M. Drugs in development for Parkinson's disease. Curr. Opin. Investig. Drugs 5 (2004) 720-726
3. Sellal F., Nieoullon A., Michel G., Michel B.F., Lacomblez L., Greerts H., Delini-Stula A., Bentue-Ferrer D., Bordet R., and Allain H. Pharmacology of Alzheimer's disease: where do we go from here?. Therapie 60 (2005) 89-107
4. Kelly J.W. The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways. Curr. Opin. Struct. Biol. 8 (1998) 101-106
5. Lomas D.A., and Carrell R.W. Serpinopathies and the conformational dementias. Nat. Rev., Genet. 3 (2002) 759-768
6. Stefani M., and Dobson C.M. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. 81 (2003) 678-699
7. Stefani M. Protein misfolding and aggregation: new examples in medicine and biology of the dark side of the protein world. Biochim. Biophys. Acta 1739 (2004) 5-25
8. Weksler M.E., Gouras G., Relkin N.R., and Szabo P. The immune system, amyloid-beta peptide, and Alzheimer's disease. Immunol. Rev. 205 (2005) 244-256
9. Zimmermann M., Borroni B., Cattabeni F., Padovani F., and Di Luca M. Cholinesterase inhibitors influence APP metabolism in Alzheimer disease patients. Neurobiol. Dis. 19 (2005) 237-242
10. Brenneman D.E., Spong C.Y., and Gozes I. Protective peptides derived from novel glial proteins. Biochem. Soc. Trans. 28 (2000) 452-455
11. Hashimoto Y., Niikura T., Tajima H., Yasukawa T., Sudo H., Ito Y., Kita Y., Kawasumi M., Kouyama K., Doyu M., Sobue G., Koide T., Tsuji S., Lang J., Kurokawa K., and Nishimoto I. A rescue factor abolishing neuronal cell death by a wide spectrum of familial Alzheimer's disease genes and Abeta. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 6336-6341
12. Sponne I., Fifre A., Koziel V., Kriem B., Oster T., and Pillot T. Humanin rescues cortical neurons from prion-peptide-induced apoptosis. Mol. Cell. Neurosci. 25 (2004) 95-102
13. Chiba T., Hashimoto Y., Tajima H., Yamada M., Kato R., Niikura T., Terashita K., Schulman H., Aiso S., Kita Y., Matsuoka M., and Nishimoto I. Humanin antagonists: mutants that interfere with dimerization inhibit neuroprotection by Humanin. J. Neurosci. Res. 78 (2004) 542-552
14. Thomas P.J., Qu B.H., and Pedersen P.L. Defective protein folding as a basis of human disease. Trends Biosci. 20 (1995) 456-459
15. Welch W.J., and Brown C.R. Influence of molecular and chemical chaperones on protein folding. Cell Stress Chaperones 1 (1996) 109-115
16. Yancey P.H., Clark M.E., Hand S.C., Bowlus R.D., and Somero G.N. Living with water stress: evolution of osmolyte systems. Science 217 (1982) 1214-1222
17. Yancey P.H. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208 (2005) 819-2830
18. Borowitzka L.J., and Brown A.D. The salt relations of marine and halophilic species of the unicellular green alga, Dunaliella. The role of glycerol as a compatible solute. Arch. Microbiol. 96 (1974) 37-52
19. Borowitzka L.J. Transport Processes, Iono- and Osmoregulation. In: Gilles R., and Gilles_baillien M. (Eds) (1985), Springer-Verlag, Berlin 437-453
20. Bowlus R.D., and Somero G.N. Solute compatibility with enzyme function and structure rationales for the selection of osmotic agents and end-products of anaerobic metabolism in marine invertebrates. J. Exp. Zool. 288 (1979) 137-151
21. Arakawa T., and Timasheff S.N. Preferential interactions of proteins with solvent components in aqueous amino acid solutions. Arch. Biochem. Biophys. 224 (1983) 169-177
22. Arakawa T., and Timasheff S.N. The mechanism of action of Na glutamate, lysine HCl, and piperazine-N,N′-bis(2-ethanesulfonic acid) in the stabilization of tubulin and microtubule formation. J. Biol. Chem. 259 (1984) 4979-4986
23. Arakawa T., and Timasheff S.N. The stabilization of proteins by osmolytes. Biophys. J. 47 (1985) 411-414
24. Bai C.X., Biwersi J., Verkman A.S., and Matthay M.A. A mouse model to test the in vivo efficacy of chemical chaperones. J. Pharmacol. Toxicol. Methods 40 (1998) 39-45
25. Fischer H., Fukuda N., Barbry P., Illek B., Sartori C., and Matthay M.A. Partial restoration of defective chloride conductance in DeltaF508 CF mice by trimethylamine oxide. Am. J. Physiol.: Lung Cell. Mol. Physiol. 281 (2001) L52-L57
26. Morello J.P., Petaja-Repo U.E., Bichet D.G., and Bouvier M. Pharmacological chaperones: a new twist on receptor folding. Trends Pharmacol. Sci. 21 (2000) 466-469
27. Cohen F.E., and Kelly J.W. Therapeutic approaches to protein-misfolding diseases. Nature 426 (2003) 905-909
28. Conn P.M., Leanos-Miranda A., and Janovick J.A. Protein origami: therapeutic rescue of misfolded gene products. Mol. Interv. 2 (2002) 308-316
29. Ventosa A., Nieto J.J., and Oren A. Biology of moderately halophilic aerobic bacteria. Microbiol. Mol. Biol. Rev. 62 (1998) 504-544
30. Lanyi J.K. Salt-dependent properties of proteins from extremely halophilic bacteria. Bacteriol. Rev. 38 (1974) 272-290
31. Pundak S., Aloni H., and Eisenberg H. Structure and activity of malate dehydrogenase from the extreme halophilic bacteria of the Dead Sea. 2. Inactivation, dissociation and unfolding at NaCl concentrations below 2 M. Salt, salt concentration and temperature dependence of enzyme stability. Eur. J. Biochem. 118 (1981) 471-477
32. Mevarech M., Frolow F., and Gloss L.M. Halophilic enzymes: proteins with a grain of salt. Biophys. Chemist. 86 (2000) 155-164
33. Zaccai G., and Eisenberg H. Halophilic proteins and the influence of solvent on protein stabilization. Trends Biochem. Science 15 (1990) 333-337
34. Madern D., Ebel C., and Zaccai G. Halophilic adaptation of enzymes. Extremophiles 4 (2000) 91-98
35. Kita Y., Arakawa T., Lin T.-Y., and Tmasheff S.N. Contribution of the surface free energy perturbation to protein-solvent interactions. Biochemistry 33 (1994) 15178-15189
36. Lin T.-Y., and Timasheff S.N. On the role of surface tension in the stabilization of globular proteins. Protein Sci. 5 (1996) 372-381
37. Tsumoto K., Umetsu M., Kumagai I., Ejima D., Philo J.S., and Arakawa T. Role of arginine in protein refolding, solubilization, and purification. Biotechnol. Prog. 20 (2004) 1301-1308
38. Ishibashi M., Tsumoto K., Tokunaga M., Ejima D., Kita Y., and Arakawa T. Is arginine a protein-denaturant?. Protein Expression Purif. 42 (2005) 1-6
39. Lee J.C., and Timasheff S.N. Partial specific volumes and interactions with solvent components of proteins in guanidine hydrochloride. Biochemistry 13 (1974) 257-265
40. Prakash V., Loucheux C., Scheufele S., Gorbunoff M.J., and Timasheff S.N. Interactions of proteins with solvent components in 8 M urea. Arch. Biochem. Biophys. 210 (1981) 455-464
41. Timasheff S.N., and Xie G. Preferential interactions of urea with lysozyme and their linkage to protein denaturation. Biophys. Chemist. 105 (2003) 421-448
42. Hand S.C., and Somero G.N. Urea and methylamine effects on rabbit muscle phosphofructokinase. Catalytic stability and aggregation state as a function of pH and temperature. J. Biol. Chem. 257 (1982) 734-741
43. Gerlsma S.Y., and Stuur E.R. The effect of polyhydric and monohydric alcohols on the heat-induced reversible denaturation of lysozyme and ribonuclease. Int. J. Pept. Protein Res. 4 (1972) 377-383
44. Back J.F., Oakenfull D., and Smith M.B. Increased thermal stability of proteins in the presence of sugars and polyols. Biochemistry 18 (1979) 5191-5199
45. Gekko K., and Koga S. Increased thermal stability of collagen in the presence of sugars and polyols. J. Biochem. 94 (1983) 199-208
46. Frigon R.P., and Lee J.C. The stabilization of calf-brain microtubule protein by sucrose. Arch. Biochem. Biophys. 153 (1972) 587-589
47. Shelanski M.L., Gaskin F., and Cantor C.R. Microtubule assembly in the absence of added nucleotides. Proc. Natl. Acad. Sci. U. S. A. 70 (1973) 765-768
48. Lee J.C., Frigon R.P., and Timasheff S.N. Structural stability of calf brain microtubule protein. Ann. N.Y. Acad Sci. 253 (1975) 284-291
49. Lee J.C., and Timasheff S.N. The stabilization of proteins by sucrose. J. Biol. Chem. 256 (1981) 7193-7201
50. Gekko K., and Timasheff S.N. Thermodynamic and kinetic examination of protein stabilization by glycerol. Biochemistry 20 (1981) 4667-4676
51. Na G.C., and Timasheff S.N. Interaction of calf brain tubulin with glycerol. J. Mol. Biol. 151 (1981) 165-178
52. Arakawa T., and Timasheff S.N. Stabilization of protein structure by sugars. Biochemistry 21 (1982) 6536-6544
53. Inoue H., and Timasheff S.N. Preferential and absolute interactions of solvent components with proteins in mixed solvent systems. Biopolymers 11 (1972) 737-743
54. Timasheff S.N., and Inoue H. Preferential binding of solvent components to proteins in mixed water-organic solvent systems. Biochemistry 7 (1968) 2502-2513
55. Lee J.C., Gekko K., and Timasheff S.N. Measurements of preferential solvent interactions by densimetric techniques. Methods Enzymol. 61 (1979) 26-49
56. Casassa E.F., and Eisenberg H. Thermodynamic analysis of multicomponent solutions. Adv. Protein Chem. 19 (1964) 287-395
57. Arakawa T., and Timasheff S.N. Preferential interactions of proteins with salts in concentrated solutions. Biochemistry 21 (1982) 6545-6552
58. Bull H.B., and Breese K. Binding of water and electrolytes to proteins. An equilibrium dialysis study. Biopolymers 15 (1976) 1573-1583
59. Arakawa T., and Timasheff S.N. Protein stabilization and destabilization by guanidinium salts. Biochemistry 23 (1984) 5924-5929
60. Diamant S., Eliahu N., Rosenthal D., and Goloubinoff P. Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J. Biol. Chem. 276 (2001) 39586-39591
61. Narhi L., Wood S.L., Steavenson S., Jiang Y., Wu G.M., Anafi D., Kaufman S.A., Martin F., Sitney K., Denis P., Louis J.C., Wypych J., Biere A.L., and Citron M. Both familial Parkinson's disease mutations accelerate alpha-synuclein aggregation. J. Biol. Chem. 274 (1999) 9843-9846
62. Kaufman R.J. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13 (1999) 1211-1233
63. Harding H.P., Calfon M., Urano F., Novoa I., and Ron D. Transcriptional and translational control in the Mammalian unfolded protein response. Annu. Rev. Cell Dev. Biol. 18 (2002) 575-599
64. Riordan J.R., Rommens J.M., Kerem B.-S., Alon N., Rozmahel R., Grzelczak Z., Zielenski J., Lok S., Plavsic N., Chou J.-L., Drumm M.L., Iannuzzi M.C., Collins F.S., and Tsui L.-C. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245 (1989) 1066-1073
65. Cheng S.H., Gregory R.J., Marshall J., Paul S., Souza D.W., White G.A., O'Riordan C.R., and Smith A.E. Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63 (1990) 827-834
66. Kopito R.R. Biosynthesis and degradation of CFTR. Physiol. Rev. 79 (1999) S167-S173
67. Kerem B.-S., Rommens J.M., Buchanan J.A., Markiewicz D., Cox T.K., Chakravarti A., Buchwald M., and Tsui L.-C. Identification of the cystic fibrosis gene: genetic analysis. Science 245 (1989) 1073-1080
68. Yang Y., Janich S., Cohn J.A., and Wilson J.M. The common variant of cystic fibrosis transmembrane conductance regulator is recognized by hsp70 and degraded in a pre-Golgi nonlysosomal compartment. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 9480-9484
69. Pind S., Riordan J.R., and Williams D.B. Participation of the endoplasmic reticulum chaperone calnexin (p88, IP90) in the biogenesis of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 269 (1994) 12784-12788
70. Li C., Ramjeesingh M., Reyes E., Jensen T., Chang X., Rommens J.M., and Bear C.E. The cystic fibrosis mutation (delta F508) does not influence the chloride channel activity of CFTR. Nat. Genet. 3 (1993) 311-316
71. Denning G.M., Anderson M.P., Amara J.F., Marshall J., Smith A.E., and Welsh M.J. Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358 (1992) 761-764
72. Brown C.R., Hong-Brown L.Q., Biwersi J., Verkman A.S., and Welch W.J. Chemical chaperones correct the mutant phenotype of the delta F508 cystic fibrosis transmembrane conductance regulator protein. Cell Stress Chaperones 1 (1996) 117-125
73. Sato S., Ward C.L., Krouse M.E., Wine J.J., and Kopito R.R. Glycerol reverses the misfolding phenotype of the most common cystic fibrosis mutation. J. Biol. Chem. 271 (1996) 635-638
74. Michalovitz D., Halevy O., and Oren M. Conditional inhibition of transformation and of cell proliferation by a temperature-sensitive mutant of p53. Cell 62 (1990) 671-680
75. Martinez J., Georgoff I., Martinez J., and Levine A.J. Cellular localization and cell cycle regulation by a temperature-sensitive p53 protein. Genes Dev. 5 (1991) 151-159
76. Brown C.R., Hong-Brown L.Q., and Welch W.J. Correcting temperature-sensitive protein folding defects. J. Clin. Invest. 99 (1997) 1432-1444
77. Ohnishi T., Ohnishi K., Wang X., Takahashi A., and Okaichi K. Restoration of mutant TP53 to normal TP53 function by glycerol as a chemical chaperone. Radiat. Res. 151 (1999) 498-500
78. Ohnishi T., Matsumoto H., Wang X., Takahashi A., Tamamoto T., and Ohnishi K. Restoration by glycerol of p53-dependent apoptosis in cells bearing the mutant p53 gene. Int. J. Radiat. Biol. 75 (1999) 1095-1098
79. Tamarappoo B.K., Yang B., and Verkman A.S. Misfolding of mutant aquaporin-2 water channels in nephrogenic diabetes insipidus. J. Biol. Chem. 274 (1999) 34825-34831
80. Maroney A.C., Qureshi S.A., Foster D.A., and Brugge J.S. Cloning and characterization of a thermolabile v-src gene for use in reversible transformation of mammalian cells. Oncogene 7 (1992) 1207-1214
81. Nishizawa M., Mayer B.J., Takeya T., Yamamoto T., Toyoshima K., Hanafusa H., and Kawai S.J. Two independent mutations are required for temperature-sensitive cell transformation by a Rous sarcoma virus temperature-sensitive mutant. Virology 56 (1985) 743-749
82. Hawthorne D.C., and Friss J. Osmotic-remedial mutants. a new classification for nutritional mutants in yeast. Genetics 50 (1964) 829-839
83. Higgins C.F. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8 (1992) 67-113
84. Gottesman M.M., and Pastan I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem. 62 (1993) 385-427
85. Kuchler K., and Thorner J. Functional expression of human mdr1 in the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 2302-2305
86. Figler R.A., Omote H., Nakamoto R.K., and Al-Shawa M.K. Use of chemical chaperones in the yeast Saccharomyces cerevisiae to enhance heterologous membrane protein expression: high-yield expression and purification of human P-glycoprotein. Arch. Biochem. Biophys. 376 (2000) 34-46
87. Loo T.W., and Clark D.M. Correction of defective protein kinesis of human P-glycoprotein mutants by substrates and modulators. J. Biol. Chem. 272 (1997) 709-712
88. Illek B., and Fischer H. Flavonoids stimulate Cl conductance of human airway epithelium in vitro and in vivo. Am. J. Physiol., Lung Cell. Mol. Physiol. 275 (1998) L902-L910
89. Jensen T.J., Loo M.A., Pind S., Williams D.B., Goldberg A.L., and Riordan J.R. Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83 (1995) 129-135
90. Loo T.W., and Clarke D.M. Prolonged association of temperature-sensitive mutants of human P-glycoprotein with calnexin during biogenesis. J. Biol. Chem. 269 (1994) 28683-28689
91. Morello J.P., and Bichet D.G. Nephrogenic diabetes insipidus. Annu. Rev. Physiol. 63 (2001) 607-630
92. Carrell R.W., and Lomas D.A. Conformational disease. Lancet 350 (1997) 134-138
93. Kopito R.R., and Ron D. Conformational disease. Nat. Cell Biol. 2 (2000) E207-E209
94. Selkoe D.J. Folding proteins in fatal ways. Nature 426 (2003) 900-904
95. Sitia R., and Braakman I. Quality control in the endoplasmic reticulum protein factory. Nature 426 (2003) 891-894
96. Soto C. Unfolding the role of protein misfolding in neurodegenerative diseases. Nat. Rev., Neurosci. 4 (2003) 49-60
97. Cheng S.H., Gregory R.J., Marshall J., Paul S., Souza D.W., White G.A., O'Riordan C.R., and Smith A.E. Cell 63 (1990) 827-834
98. Aridor M., and Balch W.E. Integration of endoplasmic reticulum signaling in health and disease. Nat. Med. 5 (1999) 745-751
99. Boyce M., Bryant K.F., Jousse C., Long K., Harding H.P., Scheuner D., Kaufman R.J., Ma D., Coen D.M., Ron D., and Yuan J. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307 (2005) 935-939
100. Loo T.W., and Clarke D.M. P-glycoprotein. Associations between domains and between domains and molecular chaperones. J. Biol. Chem. 270 (1995) 21839-21844
101. Kim B.E., Smith K., Meagher C.K., and Petris M.J. A conditional mutation affecting localization of the Menkes disease copper ATPase. Suppression by copper supplementation. J. Biol. Chem. 277 (2002) 44079-44084
102. Loo T.W., and Clarke D.M. Determining the structure and mechanism of the human multidrug resistance P-glycoprotein using cysteine-scanning mutagenesis and thiol-modification techniques. Biochim. Biophys. Acta 1461 (1999) 315-325
103. Morello J.P., Salahpour A., Laperriere A., Bernier V., Arthus M.F., Lonergan M., Petaja-Repo U., Angers S., Morin D., Bichet D.G., and Bouvier M. Pharmacological chaperones rescue cell-surface expression and function of misfolded V2 vasopressin receptor mutants. J. Clin. Invest. 105 (2000) 887-895
104. Ishii S., Kase R., Okumiya T., Sakuraba H., and Suzuki Y. Aggregation of the inactive form of human alpha-galactosidase in the endoplasmic reticulum. Biochem. Biophys. Res. Commun. 220 (1996) 812-815
105. Fan J.Q., Ishii S., Asano N., and Suzuki Y. Accelerated transport and maturation of lysosomal alpha-galactosidase A in Fabry lymphoblasts by an enzyme inhibitor. Nat. Med. 5 (1999) 112-115
106. Frustaci A., Chimenti C., Ricci R., Natale L., Russo M.A., Pieroni M., Eng C.M., and Desnick R.J. Improvement in cardiac function in the cardiac variant of Fabry's disease with galactose-infusion therapy. N. Engl. Med. 345 (2001) 25-32
107. Lee K., Jin X., Zhang K., Copertino L., Andrews L., Baker-Malcolm J., Geagan L., Qiu H., Seiger K., Barngrover D., McPherson J.M., and Edmunds T. biochemical and pharmacological comparison of enzyme replacement therapies for the glycolipid storage disorder Fabry disease. Glycobiology 13 (2003) 305-313
108. Tominaga L., Ogawa Y., Taniguchi M., Ohno K., Matsuda J., Oshima A., Suzuki Y., and Nanba E. Galactonojirimycin derivatives restore mutant human beta-galactosidase activities expressed in fibroblasts from enzyme-deficient knockout mouse. Brain Develop. 23 (2001) 284-287
109. Matsuda J., Suzuki O., Oshima A., Yamamoto Y., Noguchi A., Takimoto K., Itoh M., Matsuzaki Y., Yasuda Y., Ogawa S., Sakata Y., Nanba E., Higaki K., Ogawa Y., Tominaga L., Ohno K., Iwasaki H., Watanabe H., Brady R.O., and Suzuki Y. Emical chaperone therapy for brain pathology in G(M1)-gangliosidosis. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15912-15917
110. de Fost M., Aerts J.M., and Hollak C.E. Gaucher disease: from fundamental research to effective therapeutic interventions. Neth. J. Med. 61 (2003) 3-8
111. Dormer R.L., Derand R., McNeilly C.M., Mettey Y., Bulteau-Pignoux L., Metaye T., Vierfond J.M., Gray M.A., Galietta L.J., Morris M.R., Pereira M.M., Doull I.J., Becq F., and McPherson M.A. Correction of delF508-CFTR activity with benzo(c)quinolizinium compounds through facilitation of its processing in cystic fibrosis airway cells. J. Cell Sci. 114 (2001) 4073-4081
112. Galietta L.J., Springsteel M.F., Eda M., Niedzinski E.J., By K., Haddadin M.J., Kurth M.J., Nantz M.H., and Verkman A.S. Novel CFTR chloride channel activators identified by screening of combinatorial libraries based on flavone and benzoquinolizinium lead compounds. J. Biol. Chem. 276 (2001) 19723-19728
113. Barth S., Huhn M., Matthew B., Klimka A., Galinski E.A., and Engert A. Compatible-solute-supported periplasmic expression of functional recombinant proteins under stress conditions. Appl. Environ. Microbiol. 66 (2000) 1572-1579
114. Beck F.X., and Neuhofer W. Response of renal medullary cells to osmotic stress. Contrib. Nephrol. 148 (2005) 21-34
115. Bourot S., Sire O., Trautwetter A., Touze T., Wu L.F., Blanco C., and Bernard T. Glycine betaine-assisted protein folding in a lysA mutant of Escherichia coli. J. Biol. Chem. 275 (2000) 1050-1056
116. Macario A.J.L., and de Macario E.C. Sick chaperones, cellular stress, and disease. N. Engl. J. Med. 353 (2005) 1489-1501
117. Kregel K.C. Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J. Appl. Physiol. 92 (2002) 2177-2186
118. Prohaszka Z., and Fuest G. Immunological aspects of heat-shock proteins-The optimum stress of life. Mol. Immunol. 41 (2004) 29-44
119. Sun Y., and MacRae T.H. The small heat shock proteins and their role in human disease. FEBS J. 272 (2005) 2613-2627
120. Wemekamp-Kamphuis H.H., Sleator R.D., Wouters J.A., Hill C., and Abee T. Molecular and physiological analysis of the role of osmolyte transporters BetL, Gbu, and OpuC in growth of Listeria monocytogenes at low temperatures. Appl. Environ. Microbiol. 70 (2004) 2912-2918
121. Nemethy G., and Scheraga H.A. J. Chem. Phys. 41 (1964) 680-689
122. Hamaguchi K. Structure of muramidase (lysozyme). 8. Effect of dimethyl sulfoxide on the stability of muramidase. J. Biochem. 56 (1964) 441-449
123. Porubcan R.S., Watters K.L., and McFarland J.T. A laser Raman study of lysozyme denaturation. Arch. Biochem. Biophys. 186 (1978) 255-264
124. Jacob S.N., Rosenbaum E.E., and Wood D.C. Dimethyl Sulfoxide vol.1 (1971), Marcel Dekker, New York
125. Maurel P. Relevance of dielectric constant and solvent hydrophobicity to the organic solvent effect in enzymology. J. Biol. Chem. 253 (1978) 1677-1683
126. Miegel A., Sano K.I., Yamamoto K., Maeda K., Maeda Y., Taniguchi H., Yao M., and Wakatsuki S. Production and crystallization of lobster muscle tropomyosin expressed in Sf9 cells. FEBS Lett. 394 (1996) 201-205
127. Himes R.H., Burton P.R., and Gaito J.M. Dimethyl sulfoxide-induced self-assembly of tubulin lacking associated proteins. J. Biol. Chem. 252 (1977) 6222-6228
128. Himes R.H., Burton P.R., Kersey R.N., and Pierson G.B. Brain tubulin polymerization in the absence of "microtubule-associated proteins". Proc. Natl. Acad. Sci. U. S. A. 73 (1976) 4397-4399
129. Hamel E., Lin C.M., Kenney S., and Skehan P. Highly variable effects of beryllium and beryllium fluoride on tubulin polymerization under different reaction conditions: comparison of assembly reactions dependent on microtubule-associated proteins, glycerol, dimethyl sulfoxide, and glutamate. Arch. Biochem. Biophys. 286 (1991) 57-69
130. He M.M., Smith A.S., Oslob J.D., Flanagan W.M., Braisted A.C., Whitty A., Cancilla M.T., Wang J., Lugovskoy A.A., Yoburn J.C., Fung A.D., Farrington G., Eldredge J.K., Day E.S., Cruz L.A., Cachero T.G., Miller S.K., Friedman J.E., Choong I.C., and Cunningham B.C. Small-molecule inhibition of TNF-alpha. Science 310 (2005) 1022-1025
131. Schramm V.L., and Hochstein L.I. Stabilization of allosteric adenosine monophosphate nucleosidase by inorganic salts, substrate, and essential activator. Biochemistry 10 (1971) 3411-3417
132. Pace C.N., and McGrath T. Substrate stabilization of lysozyme to thermal and guanidine hydrochloride denaturation. J. Biol. Chem. 255 (1980) 3862-3865
133. Imoto T. Engineering of lysozyme. EXS 75 (1996) 163-181
134. Kakavonos R., Hopwood J.J., Lang D., Meikle P.J., and Brooks D.A. Stabilizing normal and mis-sense variant alpha-glucosidase. FEBS Lett 580 (2006) 4365-4370