Stability and stabilization of proteins: The ribonuclease a example

Protein Folding

Volumn , Issue , 2011, Pages 83-118

  Arnold, Ulrich ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84863490527     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (227)

1. Sumner, J. B. (1926). The isolation and crystallization of the enzyme urease: preliminary paper. J. Biol. Chem., 69, 435-441.
2. Cech, T. R. (1990). Nobel lecture. Self-splicing and enzymatic activity of an intervening sequence RNA from Tetrahymena. Biosci. Rep., 10, 239-261.
3. Altman, S. (1990). Nobel lecture. Enzymatic cleavage of RNA by RNA. Biosci. Rep., 10, 317-337.
4. Richards, F. M. (1997). Protein stability: still an unsolved problem. Cell. Mol. Life Sci., 53, 790-802.
5. Frauenfelder, H., Sligar, S. G. & Wolynes, P. G. (1991). The energy landscapes and motions of proteins. Science, 254, 1598-1603.
6. Anfinsen, C. B. (1973). Principles that govern the folding of protein chains. Science, 181, 223-230.
7. Govindarajan, S., Recabarren, R. & Goldstein, R. A. (1999). Estimating the total number of protein folds. Proteins, 35, 408-414.
8. Mirny, L. A., Abkevich, V. I. & Shakhnovich, E. I. (1998). How evolution makes proteins fold quickly. Proc. Natl. Acad. Sci. U. S. A., 95, 4976-4981.
9. Rackovsky, S. (1993). On the nature of the protein folding code. Proc. Natl. Acad. Sci. U. S. A., 90, 644-648.
10. Vieille, C. & Zeikus, G. J. (2001). Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol. Mol. Biol. Rev., 65, 1-43.
11. Eijsink, V. G., Bjork, A., Gåseidnes, S., Sirevag, R., Synstad, B., van den Burg, B. & Vriend, G. (2004). Rational engineering of enzyme stability. J. Biotechnol., 113, 105-120.
12. Schellman, J. A. (2002). Fifty years of solvent denaturation. Biophys. Chem., 96, 91-101.
13. Santoro, M. M. & Bolen, D. W. (1988). Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry, 27, 8063-8068.
14. Clarke, J. & Fersht, A. R. (1993). Engineered disulfide bonds as probes of the folding pathway of barnase: increasing the stability of proteins against the rate of denaturation. Biochemistry, 32, 4322-4329.
15. Pace, C. N., Hebert, E. J., Shaw, K. L., Schell, D., Both, V., Krajcikova, D., Sevcik, J., Wilson, K. S., Dauter, Z., Hartley, R. W. & Grimsley, G. R. (1998). Conformational stability and thermodynamics of folding of ribonucleases Sa, Sa2 and Sa3. J. Mol. Biol., 279, 271-286.
16. Lumry, R. & Biltonen, R. (1966). Validity of the "two-state" hypothesis for conformational transitions of proteins. Biopolymers, 4, 917-944.
17. Pace, C. N. & Laurents, D. V. (1989). A new method for determining the heat capacity change for protein folding. Biochemistry, 28, 2520-2525.
18. Makhatadze, G. I. & Privalov, P. L. (1990). Heat capacity of proteins. I. Partial molar heat capacity of individual amino acid residues in aqueous solution: hydration effect. J. Mol. Biol., 213, 375-384.
19. Privalov, P. L. (1979). Stability of proteins: small globular proteins. Adv. Protein Chem., 33, 167-241.
20. Greene, R. F., Jr. & Pace, C. N. (1974). Urea and guanidine hydrochloride denaturation of ribonuclease, lysozyme, alpha-chymotrypsin, and beta-lactoglobulin. J. Biol. Chem., 249, 5388-5393.
21. Tanford, C. (1970). Protein denaturation. C. Theoretical models for the mechanism of denaturation. Adv. Protein Chem., 24, 1-95.
22. Schellman, J. A. (1994). The thermodynamics of solvent exchange. Biopolymers, 34, 1015-1026.
23. Bieri, O. & Kiefhaber, T. (2000). Kinetic models in protein folding, in: ed. Pain, R. H., Mechanisms of protein folding, p. 34-64, New York, Oxford University Press Inc.
24. Clark, P. L. (2004). Protein folding in the cell: reshaping the folding funnel. Trends Biochem. Sci., 29, 527-534.
25. Cheung, M. S., Klimov, D. & Thirumalai, D. (2005). Molecular crowding enhances native state stability and refolding rates of globular proteins. Proc. Natl. Acad. Sci. U. S. A., 102, 4753-4758.
26. Ebbinghaus, S., Dhar, A., McDonald, J. D. & Gruebele, M. (2010). Protein folding stability and dynamics imaged in a living cell. Nat. Methods, 7, 319-323.
27. Truhlar, S. M. & Agard, D. A. (2005). The folding landscape of an α-lytic protease variant reveals the role of a conserved β-hairpin in the development of kinetic stability. Proteins, 61, 105-114.
28. Evans, P. A., Dobson, C. M., Kautz, R. A., Hatfull, G. & Fox, R. O. (1987). Proline isomerism in staphylococcal nuclease characterized by NMR and site-directed mutagenesis. Nature, 329, 266-268.
29. Kuwajima, K., Okayama, N., Yamamoto, K., Ishihara, T. & Sugai, S. (1991). The Pro117 to glycine mutation of staphylococcal nuclease simplifies the unfolding-folding kinetics. FEBS Lett., 290, 135-138.
30. Dill, K. A. & Chan, H. S. (1997). From Levinthal to pathways to funnels. Nat. Struct. Biol., 4, 10-19.
31. Oliveberg, M., Tan, Y. J. & Fersht, A. R. (1995). Negative activation enthalpies in the kinetics of protein folding. Proc. Natl. Acad. Sci. U. S. A., 92, 8926-8929.
32. Daggett, V. (2002). Molecular dynamics simulations of the protein unfolding/folding reaction. Acc. Chem. Res., 35, 422-429.
33. Jackson, S. E. (1998). How do small single-domain proteins fold? Fold. Des., 3, R81-91.
34. Jackson, S. E. & Fersht, A. R. (1991). Folding of chymotrypsin inhibitor 2. 1. Evidence for a two-state transition. Biochemistry, 30, 10428-10435.
35. Parker, M. J. & Marqusee, S. (1999). The cooperativity of burst phase reactions explored. J. Mol. Biol., 293, 1195-1210.
36. Kiefhaber, T. & Schmid, F. X. (1992). Kinetic coupling between protein folding and prolyl isomerization. II. Folding of ribonuclease A and ribonuclease T1. J. Mol. Biol., 224, 231-240.
37. Brandts, J. F., Halvorson, H. R. & Brennan, M. (1975). Consideration of the possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues. Biochemistry, 14, 4953-4963.
38. Grathwohl, C. & Wüthrich, K. (1981). NMR studies of the rates of proline cis-trans isomerization in oligopeptides. Biopolymers, 20, 2623-2633.
39. Stewart, D. E., Sarkar, A. & Wampler, J. E. (1990). Occurrence and role of cis peptide bonds in protein structures. J. Mol. Biol., 214, 253-260.
40. Weiss, M. S., Jabs, A. & Hilgenfeld, R. (1998). Peptide bonds revisited. Nat. Struct. Biol., 5, 676.
41. Reimer, U., Scherer, G., Drewello, M., Kruber, S., Schutkowski, M. & Fischer, G. (1998). Side-chain effects on peptidyl-prolyl cis/trans isomerisation. J. Mol. Biol., 279, 449-460.
42. Balbach, J. & Schmid, F. X. (2000). Proline isomerization and its catalysis in protein folding, in: ed. Pain, R. H., Mechanisms of protein folding, p. 212-249, New York, Oxford University Press Inc.
43. Schultz, D. A. & Baldwin, R. L. (1992). Cis proline mutants of ribonuclease A. I. Thermal stability. Protein Sci., 1, 910-916.
44. Mutter, M., Wohr, T., Gioria, S. & Keller, M. (1999). Pseudo-prolines: induction of cis/trans-conformational interconversion by decreased transition state barriers. Biopolymers, 51, 121-128.
45. An, S. S. A., Cathy, C. C., Peng, J. L., Li, Y. J., Rothwarf, D. M., Welker, E., Thannhauser, T. W., Zhang, L. S., Tam, J. P. & Scheraga, H. A. (1999). Retention of the cis proline conformation in tripeptide fragments of bovine pancreatic ribonuclease A containing a non-natural proline analogue, 5, 5-dimethylproline. J. Am. Chem. Soc., 121, 11558-11566.
46. Renner, C., Alefelder, S., Bae, J. H., Budisa, N., Huber, R. & Moroder, L. (2001). Fluoroprolines as Tools for Protein Design and Engineering. Angew. Chem. Int. Ed. Engl., 40, 923-925.
47. Arnold, U., Hinderaker, M. P., Köditz, J., Golbik, R., Ulbrich-Hofmann, R. & Raines, R. T. (2003). Protein prosthesis: a nonnatural residue accelerates folding and increases stability. J. Am. Chem. Soc., 125, 7500-7501.
48. Levitt, M. (1981). Effect of proline residues on protein folding. J. Mol. Biol., 145, 251-263.
49. Fischer, G., Bang, H. & Mech, C. (1984). [Determination of enzymatic catalysis for the cis-trans-isomerization of peptide binding in proline-containing peptides]. Biomed. Biochim. Acta, 43, 1101-1111.
50. Schiene, C. & Fischer, G. (2000). Enzymes that catalyse the restructuring of proteins. Curr. Opin. Struct. Biol., 10, 40-45.
51. Schmid, F. X. (1983). Mechanism of folding of ribonuclease A. Slow refolding is a sequential reaction via structural intermediates. Biochemistry, 22, 4690-4696.
52. Chen, B. L., Baase, W. A. & Schellman, J. A. (1989). Low-temperature unfolding of a mutant of phage T4 lysozyme. 2. Kinetic investigations. Biochemistry, 28, 691-699.
53. Gahl, R. F. & Scheraga, H. A. (2009). Oxidative folding pathway of onconase, a ribonuclease homologue: insight into oxidative folding mechanisms from a study of two homologues. Biochemistry, 48, 2740-2751.
54. Shakhnovich, E., Abkevich, V. & Ptitsyn, O. (1996). Conserved residues and the mechanism of protein folding. Nature, 379, 96-98.
55. Collinet, B., Garcia, P., Minard, P. & Desmadril, M. (2001). Role of loops in the folding and stability of yeast phosphoglycerate kinase. Eur. J. Biochem., 268, 5107-5118.
56. Schellenberger, A. & Ulbrich, R. (1989). Protein stabilization by blocking the native unfolding nucleus. Biomed. Biochim. Acta, 48, 63-67.
57. Ulbrich-Hofmann, R., Golbik, R. & Damerau, W. (1993). Fixation of the unfolding region-a hypothesis of enzyme stabilization, in: eds. van den Tweel, W. J. J., Harder, A., and Buitelaar, R. M., Stability and stabilization of enzymes, p. 497-504, Amsterdam, Elsevier.
58. Ulbrich-Hofmann, R., Arnold, U. & Mansfeld, J. (1999). The concept of the unfolding region for approaching the mechanisms of enzyme stabilization. J. Mol. Catal. B, 7, 125-131.
59. Siddiqui, K. S., Rangarajan, M., Hartley, B. S., Kitmitto, A., Panico, M., Blench, I. P. & Morris, H. R. (1993). Arthrobacter D-xylose isomerase: partial proteolysis with thermolysin. Biochem. J., 289, 201-208.
60. Eijsink, V. G., Veltman, O. R., Aukema, W., Vriend, G. & Venema, G. (1995). Structural determinants of the stability of thermolysin-like proteinases. Nat. Struct. Biol., 2, 374-379.
61. Gåseidnes, S., Synstad, B., Jia, X., Kjellesvik, H., Vriend, G. & Eijsink, V. G. (2003). Stabilization of a chitinase from Serratia marcescens by Gly→Ala and Xxx→Pro mutations. Protein Eng., 16, 841-846.
62. Fersht, A. R., Matouschek, A. & Serrano, L. (1992). The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. J. Mol. Biol., 224, 771-782.
63. Fersht, A. R. & Sato, S. (2004). Phi-value analysis and the nature of protein-folding transition states. Proc. Natl. Acad. Sci. U. S. A., 101, 7976-7981.
64. Matouschek, A., Kellis, J. T., Jr., Serrano, L. & Fersht, A. R. (1989). Mapping the transition state and pathway of protein folding by protein engineering. Nature, 340, 122-126.
65. Köditz, J., Ulbrich-Hofmann, R. & Arnold, U. (2004). Probing the unfolding region of ribonuclease A by site-directed mutagenesis. Eur. J. Biochem., 271, 4147-4156.
66. Pecher, P. & Arnold, U. (2009). The effect of additional disulfide bonds on the stability and folding of ribonuclease A. Biophys. Chem., 141, 21-28.
67. Fersht, A. R. (1999). Kinetics of protein folding-a guide to enzyme catalysis and protein folding, in, Structure and mechanism in protein science, p. 540-572, NewYork, W. H. Freeman and Company.
68. Krebs, H., Rudolph, R. & Jaenicke, R. (1979). Influence of coenzyme on the refolding and reassociation in vitro of glyceraldehyde-3-phosphate dehydrogenase from yeast. Eur. J. Biochem., 100, 359-364.
69. Relimpio, A., Iriarte, A., Chlebowski, J. F. & Martinez-Carrion, M. (1981). Differential scanning calorimetry of cytoplasmic aspartate transaminase. J. Biol. Chem., 256, 4478-4488.
70. Pantoliano, M. W. (1992). Proteins designed for challenging environments and catalysis in organic solvents. Curr. Opin. Struct. Biol., 2, 559-568.
71. Shareghi, B. & Moosavi-Movahedi, A. A. (1996). Kinetics and thermodynamics studies on the interaction of D-amino acid oxidase and sodium n-dodecyl sulphate in the presence and absence of flavin adenine dinucleotide. Int. J. Biol. Macromol., 19, 9-13.
72. Forsgren, N., Lamont, R. J. & Persson, K. Two intramolecular isopeptide bonds are identified in the crystal structure of the Streptococcus gordonii SspB C-terminal domain. J. Mol. Biol., 397, 740-751.
73. Diwan, M. & Park, T. G. (2001). Pegylation enhances protein stability during encapsulation in PLGA microspheres. J. Control. Release, 73, 233-244.
74. Blomhoff, H. K. & Christensen, T. B. (1983). Effect of dextran and dextran modifications on the thermal and proteolytic stability of conjugated bovine testis beta-galactosidase and human serum albumin. Biochim. Biophys. Acta, 743, 401-407.
75. Solá, R. J. & Griebenow, K. Glycosylation of therapeutic proteins: an effective strategy to optimize efficacy. BioDrugs, 24, 9-21.
76. Marfey, P. S., Uziel, M. & Little, J. (1965). Reaction of bovine pancreatic ribonuclease a with 1, 5-difluoro-2, 4-dinitrobenzene. II. Structure of an intramolecularly bridged derivative. J. Biol. Chem., 240, 3270-3275.
77. Lin, S. H., Konishi, Y., Denton, M. E. & Scheraga, H. A. (1984). Influence of an extrinsic cross-link on the folding pathway of ribonuclease A. Conformational and thermodynamic analysis of cross-linked (lysine7-lysine41)-ribonuclease A. Biochemistry, 23, 5504-5512.
78. Reiner, R., Siebeneick, H.-U., Christensen, I. & Döring, H. (1977). Chemical modification of enzymes II. Conformational stability of cross-linked bovine pancreatic ribonuclease. J. Mol. Catal., 2, 119-128.
79. Sheldon, R. A. (2007). Cross-linked enzyme aggregates (CLEAs): stable and recyclable biocatalysts. Biochem. Soc. Trans., 35, 1583-1587.
80. Ulbrich, R., Schellenberger, A. & Damerau, W. (1986). Studies on the thermal inactivation of immobilized enzymes. Biotechnol. Bioeng., 28, 511-522.
81. Hickey, A. M., Marle, L., McCreedy, T., Watts, P., Greenway, G. M. & Littlechild, J. A. (2007). Immobilization of thermophilic enzymes in miniaturized flow reactors. Biochem. Soc. Trans., 35, 1621-1623.
82. Gianfreda, L. & Scarfi, M. R. (1991). Enzyme stabilization: state of the art. Mol. Cell. Biochem., 100, 97-12.
83. Vermuë, M. H. & Tramper, J. (1995). Biocatalysis in non-conventional media: Medium engineering aspects. Pure & Appl. Chem., 67, 345-373.
84. Illanes, A. (1999). Stability of biocatalysts. Electron. J. Biotechn., 2, 1-9.
85. Faria, T. Q., Mingote, A., Siopa, F., Ventura, R., Maycock, C. & Santos, H. (2008). Design of new enzyme stabilizers inspired by glycosides of hyperthermophilic microorganisms. Carbohydr. Res., 343, 3025-3033.
86. Urfer, R. & Kirschner, K. (1992). The importance of surface loops for stabilizing an eightfold beta alpha barrel protein. Protein Sci., 1, 31-45.
87. Gu, H., Kim, D. & Baker, D. (1997). Contrasting roles for symmetrically disposed beta-turns in the folding of a small protein. J. Mol. Biol., 274, 588-596.
88. Leszczynski, J. F. & Rose, G. D. (1986). Loops in globular proteins: a novel category of secondary structure. Science, 234, 849-855.
89. Fetrow, J. S. (1995). Omega loops: nonregular secondary structures significant in protein function and stability. FASEB J., 9, 708-717.
90. Arnold, U., Köditz, J., Markert, Y. & Ulbrich-Hofmann, R. (2005). Local fluctuations vs. global unfolding of proteins investigated by limited proteolysis. Biocatal. Biotransfor., 23, 159-167.
91. Price, N. C. & Johnson, C. M. (1990). Proteinases as probes of conformation of soluble proteins, in: ed. Beynon, R. J., Bond, J. S., Proteolytic Enzymes: A practical approach, p. 163-180, Oxford, IRL Press.
92. Hubbard, S. J., Eisenmenger, F. & Thornton, J. M. (1994). Modeling studies of the change in conformation required for cleavage of limited proteolytic sites. Protein Sci., 3, 757-768.
93. Arnold, U., Rücknagel, K. P., Schierhorn, A. & Ulbrich-Hofmann, R. (1996). Thermal unfolding and proteolytic susceptibility of ribonuclease A. Eur. J. Biochem., 237, 862-869.
94. Hubbard, S. J. (1998). The structural aspects of limited proteolysis of native proteins. Biochim. Biophys. Acta, 1382, 191-206.
95. Park, C. & Marqusee, S. (2004). Probing the high energy states in proteins by proteolysis. J. Mol. Biol., 343, 1467-1476.
96. Klee, W. A. (1967). Intermediate stages in the thermally induced transconformation reactions of bovine pancreatic ribonuclease A. Biochemistry, 6, 3736-3742.
97. Winchester, B. G., Mathias, A. P. & Rabin, B. R. (1970). Study of the thermal denaturation of ribonuclease A by differential thermal analysis and susceptibility to proteolysis. Biochem. J., 117, 299-307.
98. Arnold, U. & Ulbrich-Hofmann, R. (1997). Kinetic and thermodynamic thermal stabilities of ribonuclease A and ribonuclease B. Biochemistry, 36, 2166-2172.
99. Wang, L., Chen, R. X. & Kallenbach, N. R. (1998). Proteolysis as a probe of thermal unfolding of cytochrome c. Proteins, 30, 435-441.
100. Arnold, U. & Ulbrich-Hofmann, R. (2000). Differences in the denaturation behavior of ribonuclease A induced by temperature and guanidine hydrochloride. J. Protein Chem., 19, 345-352.
101. Fontana, A., de Laureto, P. P., Spolaore, B., Frare, E., Picotti, P. & Zambonin, M. (2004). Probing protein structure by limited proteolysis. Acta Biochim. Pol., 51, 299-321.
102. Matheson, R. R., Jr. & Scheraga, H. A. (1979). Steps in the pathway of the thermal unfolding of ribonuclease A. A nonspecific photochemical surface-labeling study. Biochemistry, 18, 2437-2445.
103. Kintses, B., Simon, Z., Gyimesi, M., Tóth, J., Jelinek, B., Niedetzky, C., Kovács, M. & Málnási-Csizmadia, A. (2006). Enzyme kinetics above denaturation temperature: a temperature-jump/stopped-flow apparatus. Biophys. J., 91, 4605-4610.
104. Torrent, J., Marchal, S., Ribó, M., Vilanova, M., Georges, C., Dupont, Y. & Lange, R. (2008). Distinct unfolding and refolding pathways of ribonuclease a revealed by heating and cooling temperature jumps. Biophys. J., 94, 4056-4065.
105. Ooi, T., Rupley, J. A. & Scheraga, H. A. (1963). Structural Studies of Ribonuclease. VIII. Tryptic Hydrolysis of Ribonuclease a at Elevated Temperatures. Biochemistry, 2, 432-437.
106. Matthyssens, G. E., Simons, G. & Kanarek, L. (1972). Study of the thermal-denaturation mechanism of hen egg-white lysozyme through proteolytic degradation. Eur. J. Biochem., 26, 449-454.
107. Imoto, T., Yamada, H. & Ueda, T. (1986). Unfolding rates of globular proteins determined by kinetics of proteolysis. J. Mol. Biol., 190, 647-649.
108. Tams, J. W. & Welinder, K. G. (1996). Unfolding and refolding of Coprinus cinereus peroxidase at high pH, in urea, and at high temperature. Effect of organic and ionic additives on these processes. Biochemistry, 35, 7573-7579.
109. Arnold, U., Schierhorn, A. & Ulbrich-hofmann, R. (1999). Modification of the unfolding region in bovine pancreatic ribonuclease and its influence on the thermal stability and proteolytic fragmentation. Eur. J. Biochem., 259, 470-475.
110. Arnold, U. & Ulbrich-Hofmann, R. (2001). Proteolytic degradation of ribonuclease A in the pretransition region of thermally and urea-induced unfolding. Eur. J. Biochem., 268, 93-97.
111. Arnold, U. (2009). Incorporation of non-natural modules into proteins: structural features beyond the genetic code. Biotechnol. Lett., 31, 1129-1139.
112. Raines, R. T. (1998). Ribonuclease A. Chem. Rev., 98, 1045-1066.
113. Marshall, G. R., Feng, J. A. & Kuster, D. J. (2008). Back to the future: ribonuclease A. Biopolymers, 90, 259-277.
114. Dubos, R. J. & Thompson, R. H. S. (1938). The decomposition of yeast nucleic acid by a heat-resistant enzyme. J. Biol. Chem., 124, 501-510.
115. Kunitz, M. (1940). Crystalline Ribonuclease. J. Gen. Physiol., 24, 15-32.
116. Kunitz, M. & McDonald, M. R. (1953). Ribonuclease, in: ed. Snell, E. E., Biochemical Preparations, p. 9-19, New York, John Wiley & Sons.
117. Jones, W. (1920). The action of boiled pancreas extract on yeast nucleic acid. Am. J. Physiol., 52, 203-207.
118. Harrington, W. F. & Schellman, J. A. (1956). Evidence for the instability of hydrogen-bonded peptide structures in water, based on studies of ribonuclease and oxidized ribonuclease. C. R. Trav. Lab. Carlsberg Chim., 30, 21-43.
119. Hirs, C. H., Moore, S. & Stein, W. H. (1960). The sequence of the amino acid residues in performic acid-oxidized ribonuclease. J. Biol. Chem., 235, 633-647.
120. Smyth, D. G., Stein, W. H. & Moore, S. (1963). The sequence of amino acid residues in bovine pancreatic ribonuclease: revisions and confirmations. J. Biol. Chem., 238, 227-234.
121. Kartha, G., Bello, J. & Harker, D. (1967). Tertiary structure of ribonuclease. Nature, 213, 862-865.
122. Saunders, M., Wishnia, A. & Kirkwood, J. G. (1957). The nuclear magnetic resonance spectrum of ribonuclease. J. Am. Chem. Soc., 79, 3289-3290.
123. Udgaonkar, J. B. & Baldwin, R. L. (1988). NMR evidence for an early framework intermediate on the folding pathway of ribonuclease A. Nature, 335, 694-699.
124. Evans, T. C., Jr., Benner, J. & Xu, M. Q. (1998). Semisynthesis of cytotoxic proteins using a modified protein splicing element. Protein Sci., 7, 2256-2264.
125. Beintema, J. J., Breukelman, H. J., Carsana, A. & Furia, A. (1997). Evolution of vertebrate ribonucleases: Ribonuclease A superfamily, in: eds. D'Alessio, G., and Riordan, J. F., Ribonucleases: Structures and functions, p. 245-269, New York, Academic Press.
126. Beintema, J. J. & Kleineidam, R. G. (1998). The ribonuclease A superfamily: general discussion. Cell. Mol. Life Sci., 54, 825-832.
127. Bennett, M. J., Choe, S. & Eisenberg, D. (1994). Domain swapping: entangling alliances between proteins. Proc. Natl. Acad. Sci. U. S. A., 91, 3127-3131.
128. Libonati, M., Gotte, G. & Vottariello, F. (2008). A novel biological actions acquired by ribonuclease through oligomerization. Curr. Pharm. Biotechnol., 9, 200-209.
129. Raines, R. T. (1999). Ribonuclease A: from model system to cancer chemotherapeutic, in: eds. Frey, P. A., and Northrop, D. B., Enzymatic Mechanisms, p. 235-249, Washington, DC, IOS Press.
130. Arnold, U. & Ulbrich-Hofmann, R. (2006). Natural and engineered ribonucleases as potential cancer therapeutics. Biotechnol. Lett., 28, 1615-1622.
131. Arnold, U. (2008). Aspects of the cytotoxic action of ribonucleases. Curr. Pharm. Biotechnol., 9, 161-168.
132. Pace, C. N., Laurents, D. V. & Thomson, J. A. (1990). pH dependence of the urea and guanidine hydrochloride denaturation of ribonuclease A and ribonuclease T1. Biochemistry, 29, 2564-2572.
133. Klink, T. A., Woycechowsky, K. J., Taylor, K. M. & Raines, R. T. (2000). Contribution of disulfide bonds to the conformational stability and catalytic activity of ribonuclease A. Eur. J. Biochem., 267, 566-572.
134. Ramos, C. H. & Baldwin, R. L. (2002). Sulfate anion stabilization of native ribonuclease A both by anion binding and by the Hofmeister effect. Protein Sci., 11, 1771-1778.
135. Stelea, S. D., Pancoska, P., Benight, A. S. & Keiderling, T. A. (2001). Thermal unfolding of ribonuclease A in phosphate at neutral pH: deviations from the two-state model. Protein Sci., 10, 970-978.
136. Köditz, J., Arnold, U. & Ulbrich-Hofmann, R. (2002). Dissecting the effect of trifluoroethanol on ribonuclease A. Subtle structural changes detected by nonspecific proteases. Eur. J. Biochem., 269, 3831-3837.
137. Takeda, K., Sasa, K., Nagao, M. & Batra, P. P. (1988). Secondary structural changes of non-reduced and reduced ribonuclease A in solutions of urea, guanidine hydrochloride and sodium dodecyl sulfate. Biochim. Biophys. Acta, 957, 340-344.
138. Ahmad, F. (1984). Free energy changes in denaturation of ribonuclease A by mixed denaturants. Effects of combinations of guanidine hydrochloride and one of the denaturants lithium bromide, lithium chloride, and sodium bromide. J. Biol. Chem., 259, 4183-4186.
139. Sagar, A. J. & Pandit, M. W. (1983). Denaturation studies on bovine pancreatic ribonuclease. Effect of trichloroacetic acid. Biochim. Biophys. Acta, 743, 303-309.
140. Ribó, M., Benito, A., Torrent, J., Lange, R. & Vilanova, M. (2006). Pressure as a tool to study protein-unfolding/refolding processes: the case of ribonuclease A. Biochim. Biophys. Acta, 1764, 461-469.
141. Pace, C. N., Grimsley, G. R., Thomas, S. T. & Makhatadze, G. I. (1999). Heat capacity change for ribonuclease A folding. Protein Sci., 8, 1500-1504.
142. Benz, F. W. & Roberts, G. C. (1973). NMR Studies of the unfolding of ribonuclease by guanidine hydrochloride. Evidence for intermediate states. FEBS Lett., 29, 263-266.
143. Chen, M. C. & Lord, R. C. (1976). Laser Raman spectroscopic studies of the thermal unfolding of ribonuclease A. Biochemistry, 15, 1889-1897.
144. Burgess, A.W. & Scheraga, H. A. (1975). A hypothesis for the pathway of the thermally-induced unfolding of bovine pancreatic ribonuclease. J. Theor. Biol., 53, 403-420.
145. Plummer, T. H., Jr. & Hirs, C. H. (1963). The isolation of ribonuclease B, a glycoprotein, from bovine pancreatic juice. J. Biol. Chem., 238, 1396-1401.
146. Ardelt, W., Mikulski, S. M. & Shogen, K. (1991). Amino acid sequence of an anti-tumor protein from Rana pipiens oocytes and early embryos. Homology to pancreatic ribonucleases. J. Biol. Chem., 266, 245-251.
147. Puett, D. (1973). Conformational studies on a glycosylated bovine pancreatic ribonuclease. J. Biol. Chem., 248, 3566-3572.
148. Joao, H. C. & Dwek, R. A. (1993). Effects of glycosylation on protein structure and dynamics in ribonuclease B and some of its individual glycoforms. Eur. J. Biochem., 218, 239-244.
149. Fu, D., Chen, L. & O'Neill, R. A. (1994). A detailed structural characterization of ribonuclease B oligosaccharides by 1H NMR spectroscopy and mass spectrometry. Carbohydr. Res., 261, 173-186.
150. Woods, R. J., Edge, C. J. & Dwek, R. A. (1994). Protein surface oligosaccharides and protein function. Nat. Struct. Biol., 1, 499-501.
151. Leland, P. A., Staniszewski, K. E., Kim, B. & Raines, R. T. (2000). A synapomorphic disulfide bond is critical for the conformational stability and cytotoxicity of an amphibian ribonuclease. FEBS Lett., 477, 203-207.
152. Arnold, U., Schulenburg, C., Schmidt, D. & Ulbrich-Hofmann, R. (2006). Contribution of structural peculiarities of onconase to its high stability and folding kinetics. Biochemistry, 45, 3580-3587.
153. Anfinsen, C.B., Haber, E., Sela, M. & White, F. H., Jr. (1961). The kinetics of formation of native ribonuclease during oxidation of the reduced polypeptide chain. Proc. Natl. Acad. Sci. U. S. A., 47, 1309-1314.
154. Tsong, T. Y., Baldwin, R. L. & Elson, E. L. (1972). Properties of the refolding and unfolding reactions of ribonuclease A. Proc. Natl. Acad. Sci. U. S. A., 69, 1809-1812.
155. Garel, J. R. & Baldwin, R. L. (1973). Both the fast and slow refolding reactions of ribonuclease A yield native enzyme. Proc. Natl. Acad. Sci. U. S. A., 70, 3347-3351.
156. Schmid, F. X. & Blaschek, H. (1981). A native-like intermediate on the ribonuclease A folding pathway. 2. Comparison of its properties to native ribonuclease A. Eur. J. Biochem., 114, 111-117.
157. Nall, B. T., Garel, J. R. & Baldwin, R. L. (1978). Test of the extended two-state model for the kinetic intermediates observed in the folding transition of ribonuclease A. J. Mol. Biol., 118, 317-330.
158. Schmid, F. X. & Baldwin, R. L. (1978). Acid catalysis of the formation of the slow-folding species of RNase A: evidence that the reaction is proline isomerization. Proc. Natl. Acad. Sci. U. S. A., 75, 4764-4768.
159. Fischer, G.& Bang, H. (1985). The refolding of urea-denatured ribonuclease A is catalyzed by peptidyl-prolyl cis-trans isomerase. Biochim. Biophys. Acta, 828, 39-42.
160. Cook, K. H., Schmid, F. X. & Baldwin, R. L. (1979). Role of proline isomerization in folding of ribonuclease A at low temperatures. Proc. Natl. Acad. Sci. U. S. A., 76, 6157-6161.
161. Schmid, F. X. (1981). A native-like intermediate on the ribonuclease A folding pathway. 1. Detection by tyrosine fluorescence changes. Eur. J. Biochem., 114, 105-109.
162. Blum, A. D., Smallcombe, S. H. & Baldwin, R. L. (1978). Nuclear magnetic resonance evidence for a structural intermediate at an early stage in the refolding of ribonuclease A. J. Mol. Biol., 118, 305-316.
163. Kim, P. S. & Baldwin, R. L. (1980). Structural intermediates trapped during the folding of ribonuclease A by amide proton exchange. Biochemistry, 19, 6124-6129.
164. Udgaonkar, J. B. & Baldwin, R. L. (1995). Nature of the early folding intermediate of ribonuclease A. Biochemistry, 34, 4088-4096.
165. Laurents, D.V., Bruix, M., Jamin, M. & Baldwin, R. L. (1998). A pulse-chase-competition experiment to determine if a folding intermediate is on or off-pathway: application to ribonuclease A. J. Mol. Biol., 283, 669-678.
166. Kiefhaber, T. & Baldwin, R. L. (1995). Kinetics of hydrogen bond breakage in the process of unfolding of ribonuclease A measured by pulsed hydrogen exchange. Proc. Natl. Acad. Sci. U. S. A., 92, 2657-2661.
167. Noronha, M., Lima, J. C., Paci, E., Santos, H. & Maçanita, A. L. (2007). Tracking local conformational changes of ribonuclease A using picosecond time-resolved fluorescence of the six tyrosine residues. Biophys. J., 92, 4401-4414.
168. Schmid, F. X., Grafl, R., Wrba, A. & Beintema, J. J. (1986). Role of proline peptide bond isomerization in unfolding and refolding of ribonuclease. Proc. Natl. Acad. Sci. U. S. A., 83, 872-876.
169. Juminaga, D., Wedemeyer, W. J. & Scheraga, H. A. (1998). Proline isomerization in bovine pancreatic ribonuclease A. 1. Unfolding conditions. Biochemistry, 37, 11614-11620.
170. Kiefhaber, T., Labhardt, A. M. & Baldwin, R. L. (1995). Direct NMR evidence for an intermediate preceding the rate-limiting step in the unfolding of ribonuclease A. Nature, 375, 513-515.
171. Wlodawer, A., Bott, R. & Sjolin, L. (1982). The refined crystal structure of ribonuclease A at 2.0 Å resolution. J. Biol. Chem., 257, 1325-1332.
172. Houry, W. A., Rothwarf, D. M. & Scheraga, H. A. (1994). A very fast phase in the refolding of disulfide-intact ribonuclease A: implications for the refolding and unfolding pathways. Biochemistry, 33, 2516-2530.
173. Houry, W. A. & Scheraga, H. A. (1996). Nature of the unfolded state of ribonuclease A: effect of cis-trans X-Pro peptide bond isomerization. Biochemistry, 35, 11719-11733.
174. Wedemeyer, W. J., Welker, E. & Scheraga, H. A. (2002). Proline cis-trans isomerization and protein folding. Biochemistry, 41, 14637-14644.
175. Schultz, D.A., Schmid, F. X. & Baldwin, R. L. (1992). Cis proline mutants of ribonuclease A. II. Elimination of the slow-folding forms by mutation. Protein Sci., 1, 917-924.
176. Dodge, R. W. & Scheraga, H. A. (1996). Folding and unfolding kinetics of the proline-to-alanine mutants of bovine pancreatic ribonuclease A. Biochemistry, 35, 1548-1559.
177. Schultz, L. W., Hargraves, S. R., Klink, T. A. & Raines, R. T. (1998). Structure and stability of the P93G variant of ribonuclease A. Protein Sci., 7, 1620-1625.
178. Xiong, Y., Juminaga, D., Swapna, G. V., Wedemeyer, W. J., Scheraga, H. A. & Montelione, G. T. (2000). Solution NMR evidence for a cis Tyr-Ala peptide group in the structure of [Pro93Ala] bovine pancreatic ribonuclease A. Protein Sci., 9, 421-426.
179. Schultz, D.A., Friedman, A. M., White, M. A. & Fox, R. O. (2005). The crystal structure of the cis-proline to glycine variant (P114G) of ribonuclease A. Protein Sci., 14, 2862-2870.
180. Muir, T. W., Sondhi, D. & Cole, P. A. (1998). Expressed protein ligation: a general method for protein engineering. Proc. Natl. Acad. Sci. U. S. A., 95, 6705-6710.
181. Dawson, P. E., Muir, T. W., Clark-Lewis, I. & Kent, S. B. (1994). Synthesis of proteins by native chemical ligation. Science, 266, 776-779.
182. Mayo, S. L. & Baldwin, R. L. (1993). Guanidinium chloride induction of partial unfolding in amide proton exchange in RNase A. Science, 262, 873-876.
183. Neira, J. L., Sevilla, P., Menéndez, M., Bruix, M. & Rico, M. (1999). Hydrogen exchange in ribonuclease A and ribonuclease S: evidence for residual structure in the unfolded state under native conditions. J. Mol. Biol., 285, 627-643.
184. Qu, Y. & Bolen, D. W. (2003). Hydrogen exchange kinetics of RNase A and the urea: TMAO paradigm. Biochemistry, 42, 5837-5849.
185. Kim, K. S., Fuchs, J. A. & Woodward, C. K. (1993). Hydrogen exchange identifies native-state motional domains important in protein folding. Biochemistry, 32, 9600-9608.
186. Mullins, L. S., Pace, C. N. & Raushel, F. M. (1997). Conformational stability of ribonuclease T1 determined by hydrogen-deuterium exchange. Protein Sci., 6, 1387-1395.
187. Matheson, R. R. J. & Scheraga, H. A. (1978). A method for predicting nucleation sites for protein folding based on hydrophobic contacts. Macromolecules, 11, 819-829.
188. Clarke, J., Hounslow, A. M., Bycroft, M. & Fersht, A. R. (1993). Local breathing and global unfolding in hydrogen exchange of barnase and its relationship to protein folding pathways. Proc. Natl. Acad. Sci. U. S. A., 90, 9837-9841.
189. Itzhaki, L. S., Neira, J. L. & Fersht, A. R. (1997). Hydrogen exchange in chymotrypsin inhibitor 2 probed by denaturants and temperature. J. Mol. Biol., 270, 89-98.
190. Udgaonkar, J. B. & Baldwin, R. L. (1990). Early folding intermediate of ribonuclease A. Proc. Natl. Acad. Sci. U. S. A., 87, 8197-8201.
191. Houry, W. A. & Scheraga, H. A. (1996). Structure of a hydrophobically collapsed intermediate on the conformational folding pathway of ribonuclease A probed by hydrogen-deuterium exchange. Biochemistry, 35, 11734-11746.
192. Merkley, E. D., Bernard, B. & Daggett, V. (2008). Conformational changes below the Tm: molecular dynamics studies of the thermal pretransition of ribonuclease A. Biochemistry, 47, 880-892.
193. Loh, S. N., Rohl, C. A., Kiefhaber, T. & Baldwin, R. L. (1996). A general two-process model describes the hydrogen exchange behavior of RNase A in unfolding conditions. Proc. Natl. Acad. Sci. U. S. A., 93, 1982-1987.
194. Benz, F. W. & Roberts, G. C. (1975). Nuclear magnetic resonance studies of the unfolding of pancreatic ribonuclease. II. Unfolding by urea and guanidine hydrochloride. J. Mol. Biol., 91, 367-387.
195. Rupley, J. A. & Scheraga, H. A. (1963). Structural Studies of Ribonuclease. VII. Chymotryptic Hydrolysis of Ribonuclease A at Elevated Temperatures. Biochemistry, 2, 421-431.
196. Juneja, J. & Udgaonkar, J. B. (2002). Characterization of the unfolding of ribonuclease a by a pulsed hydrogen exchange study: evidence for competing pathways for unfolding. Biochemistry, 41, 2641-2654.
197. Grafl, R., Lang, K., Vogl, H. & Schmid, F. X. (1987). The mechanism of folding of pancreatic ribonucleases is independent of the presence of covalently linked carbohydrate. J. Biol. Chem., 262, 10624-10629.
198. Schulenburg, C., Martinez-Senac, M. d. M., Löw, C., Golbik, R., Ulbrich-Hofman, R. & Arnold, U. (2007). Identification of three phases in onconase refolding. FEBS J., 274, 5826-5833.
199. Schulenburg, C., Löw, C., Weininger, U., Mrestani-Klaus, C., Hofmann, H., Balbach, J., Ulbrich-Hofmann, R. & Arnold, U. (2009). The folding pathway of onconase is directed by a conserved intermediate. Biochemistry, 48, 8449-8457.
200. Schulenburg, C., Weininger, U., Neumann, P., Meiselbach, H., Stubbs, M. T., Sticht, H., Balbach, J., Ulbrich-Hofmann, R. & Arnold, U. (2010). Impact of the C-terminal disulfide bond on the folding and stability of onconase. ChemBioChem, 11, 978-986.
201. Kolbanovskaya, E., Sathyanarayana, B. K., Wlodawer, A. & Karpeisky, M. (1992). Intramolecular interactions in pancreatic ribonucleases. Protein Sci., 1, 1050-1060.
202. Vilà, R., Benito, A., Ribó, M. & Vilanova, M. (2009). Mapping the stability clusters in bovine pancreatic ribonuclease A. Biopolymers, 91, 1038-1047.
203. Marfey, P. S., Nowak, H., Uziel, M. & Yphantis, D. A. (1965). Reaction of bovine pancreatic ribonuclease a with 1, 5-difluoro-2, 4-dinitrobenzene. I. Preparation of monomeric intramolecularly bridged derivatives. J. Biol. Chem., 240, 3264-3269.
204. Lin, S. H., Konishi, Y., Nall, B. T. & Scheraga, H. A. (1985). Influence of an extrinsic cross-link on the folding pathway of ribonuclease A. Kinetics of folding-unfolding. Biochemistry, 24, 2680-2686.
205. Reiner, R., Siebeneick, H.-U., Christensen, I. & Lukas, H. (1975/76). Chemical modification of enzymes II. Two-step cross-linking of bovine pancreatic ribonuclease. J. Mol. Catal., 1, 3-12.
206. Quirk, D. J., Park, C., Thompson, J. E. & Raines, R. T. (1998). His...Asp catalytic dyad of ribonuclease A: conformational stability of the wild-type, D121N, D121A, and H119A enzymes. Biochemistry, 37, 17958-17964.
207. Rutkoski, T. J., Kurten, E. L., Mitchell, J. C. & Raines, R. T. (2005). Disruption of shape-complementarity markers to create cytotoxic variants of ribonuclease A. J. Mol. Biol., 354, 41-54.
208. Chatani, E., Nonomura, K., Hayashi, R., Balny, C. & Lange, R. (2002). Comparison of heat-and pressure-induced unfolding of ribonuclease a: the critical role of Phe46 which appears to belong to a new hydrophobic chain-folding initiation site. Biochemistry, 41, 4567-4574.
209. Kadonosono, T., Chatani, E., Hayashi, R., Moriyama, H. & Ueki, T. (2003). Minimization of cavity size ensures protein stability and folding: structures of Phe46-replaced bovine pancreatic RNase A. Biochemistry, 42, 10651-10658.
210. Markert, Y., Köditz, J., Mansfeld, J., Arnold, U. & Ulbrich-Hofmann, R. (2001). Increased proteolytic resistance of ribonuclease A by protein engineering. Protein Eng., 14, 791-796.
211. Markert, Y., Köditz, J., Ulbrich-Hofmann, R. & Arnold, U. (2003). Proline versus charge concept for protein stabilization against proteolytic attack. Protein Eng., 16, 1041-1046.
212. Font, J., Benito, A., Lange, R., Ribó, M. & Vilanova, M. (2006). The contribution of the residues from the main hydrophobic core of ribonuclease A to its pressure-folding transition state. Protein Sci., 15, 1000-1009.
213. Klink, T. A. & Raines, R. T. (2000). Conformational stability is a determinant of ribonuclease A cytotoxicity. J. Biol. Chem., 275, 17463-17467.
214. Pradeep, L., Kurinov, I., Ealick, S. E. & Scheraga, H. A. (2007). Implementation of a k/k(0) method to identify long-range structure in transition states during conformational folding/unfolding of proteins. Structure, 15, 1178-1189.
215. Thornton, J. M. (1981). Disulphide bridges in globular proteins. J. Mol. Biol., 151, 261-287.
216. Rico, M., Santoro, J., Bermejo, F. J., Herranz, J., Nieto, J. L., Gallego, E. & Jiménez, M. A. (1986). Thermodynamic parameters for the helix-coil thermal transition of ribonuclease-S-peptide and derivatives from 1H-NMR data. Biopolymers, 25, 1031-1053.
217. Fisher, B. M., Ha, J. H. & Raines, R. T. (1998). Coulombic forces in protein-RNA interactions: binding and cleavage by ribonuclease A and variants at Lys7, Arg10, and Lys66. Biochemistry, 37, 12121-12132.
218. Haigis, M. C., Kurten, E. L., Abel, R. L. & Raines, R. T. (2002). KFERQ sequence in ribonuclease A-mediated cytotoxicity. J. Biol. Chem., 277, 11576-11581.
219. Park, C. & Raines, R. T. (2000). Dimer formation by a "monomeric" protein. Protein Sci., 9, 2026-2033.
220. Catanzano, F., Graziano, G., Cafaro, V., D'Alessio, G., Di Donato, A. & Barone, G. (1997). From ribonuclease A toward bovine seminal ribonuclease: a step by step thermodynamic analysis. Biochemistry, 36, 14403-14408.
221. Juminaga, D., Wedemeyer, W. J., Garduno-Juarez, R., McDonald, M. A. & Scheraga, H. A. (1997). Tyrosyl interactions in the folding and unfolding of bovine pancreatic ribonuclease A: a study of tyrosine-to-phenylalanine mutants. Biochemistry, 36, 10131-10145.
222. Fisher, B. M., Grilley, J. E. & Raines, R. T. (1998). A new remote subsite in ribonuclease A. J. Biol. Chem., 273, 34134-34138.
223. delCardayré, S. B. & Raines, R. T. (1995). A residue to residue hydrogen bond mediates the nucleotide specificity of ribonuclease A. J. Mol. Biol., 252, 328-336.
224. Fuchs, S. M., Rutkoski, T. J., Kung, V. M., Groeschl, R. T. & Raines, R. T. (2007). Increasing the potency of a cytotoxin with an arginine graft. Protein Eng. Des. Sel., 20, 505-509.
225. Catanzano, F., Graziano, G., Capasso, S. & Barone, G. (1997). Thermodynamic analysis of the effect of selective monodeamidation at asparagine 67 in ribonuclease A. Protein Sci., 6, 1682-1693.
226. Chatani, E., Tanimizu, N., Ueno, H. & Hayashi, R. (2001). Structural and functional changes in bovine pancreatic ribonuclease a by the replacement of Phe120 with other hydrophobic residues. J. Biochem., 129, 917-922.
227. Fujii, T., Ueno, H. & Hayashi, R. (2002). Significance of the four carboxyl terminal amino acid residues of bovine pancreatic ribonuclease A for structural folding. J. Biochem., 131, 193-200.