A chemical method for investigating disulfide-coupled peptide and protein folding

FEBS Journal

Volumn 279, Issue 13, 2012, Pages 2283-2295

  Okumura, Masaki ^a,b   Shimamoto, Shigeru ^a   Hidaka, Yuji ^a  

^a KINKI UNIVERSITY   (Japan)

^b KWANSEI GAKUIN UNIVERSITY   (Japan)

Author keywords

Additive; Chemical ligation; Disulfide; Folding; Glutathione; Heat stable enterotoxin; Regioselective; Selenocysteine; Topological isomer; Uroguanylin

Indexed keywords

GLUTATHIONE; RECOMBINANT PROTEIN; SYNTHETIC PEPTIDE; THIOL;

BIOTECHNOLOGY; CHEMICAL ANALYSIS; DISULFIDE BOND; ISOMERIZATION; NATIVE CHEMICAL LIGATION; OXIDATION; OXIDATION REDUCTION REACTION; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; SHORT SURVEY; THERMODYNAMICS;

ANIMALS; DISULFIDES; HUMANS; PEPTIDE FRAGMENTS; PROTEIN FOLDING; PROTEINS;

EID: 84862564239     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08596.x     Document Type: Short Survey

References (74)

1. Creighton TE (1988) Disulphide bonds and protein stability. BioEssays 8, 57-63.
2. Pace CN, Grimsley GR, Thomson JA & Barnett BJ (1988) Conformational stability and activity of ribonuclease T1 with zero, one, and two intact disulfide bonds. J Biol Chem 263, 11820-11825.
3. Ryle AP & Anfinsen CB (1957) Studies on the disulfide bridges in ribonuclease. Biochim Biophys Acta 24, 633-635.
4. Weissman JS & Kim PS (1991) Reexamination of the folding of BPTI: predominance of native intermediates. Science 253, 1386-1393.
5. Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181, 223-230.
6. Dawson PE, Muir TW, Clark-Lewis I & Kent SB (1994) Synthesis of proteins by native chemical ligation. Science 266, 776-779.
7. Evans TC Jr, Benner J & Xu MQ (1998) Semisynthesis of cytotoxic proteins using a modified protein splicing element. Protein Sci 7, 2256-2264.
8. Muir TW (2003) Semisynthesis of proteins by expressed protein ligation. Annu Rev Biochem 72, 249-289.
9. Moroder L, Besse D, Musiol HJ, Rudolph-Bohner S & Siedler F (1996) Oxidative folding of cystine-rich peptides vs regioselective cysteine pairing strategies. Biopolymers 40, 207-234.
10. Sato Y & Inaba K (2012) Disulfide bond formation network in the three biological kingdoms, bacteria, fungi and mammals. FEBS J 279, 2262-2271.
11. Sies H (1999) Glutathione and its role in cellular functions. Free Radic Biol Med 27, 916-921.
12. Narayan M (2012) Disulfide bonds: protein folding and subcellular protein trafficking. FEBS J 279, 2272-2282.
13. Okumura M, Saiki M, Yamaguchi H & Hidaka Y (2011) Acceleration of disulfide-coupled protein folding using glutathione derivatives. FEBS J 278, 1137-1144.
14. Camarero JA & Muir TW (2001) Native chemical ligation of polypeptides. Curr Protoc Protein Sci 1, 18.4.1-18.4.21.
15. Muralidharan V & Muir TW (2006) Protein ligation: an enabling technology for the biophysical analysis of proteins. Nat Methods 3, 429-438.
16. Tolbert TJ & Wong CH (2002) New methods for proteomic research: preparation of proteins with N-terminal cysteines for labeling and conjugation. Angew Chem Int Ed Engl 41, 2171-2174.
17. Hirel PH, Schmitter MJ, Dessen P, Fayat G & Blanquet S (1989) Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the sidechain length of the penultimate amino acid. Proc Natl Acad Sci USA 86, 8247-8251.
18. Erlanson DA, Chytil M & Verdine GL (1996) The leucine zipper domain controls the orientation of AP-1 in the NFAT·AP-1·DNA complex. Chem Biol 3, 981-991.
19. Camarero JA, Shekhtman A, Campbell EA, Chlenov M, Gruber TM, Bryant DA, Darst SA, Cowburn D & Muir TW (2002) Autoregulation of a bacterial r factor explored by using segmental isotopic labeling and NMR. Proc Natl Acad Sci USA 99, 8536-8541.
20. Valiyaveetil FI, MacKinnon R & Muir TW (2002) Semisynthesis and folding of the potassium channel KcsA. J Am Chem Soc 124, 9113-9120.
21. Evans TC Jr, Benner J & Xu MQ (1999) The in vitro ligation of bacterially expressed proteins using an intein from Methanobacterium thermoautotrophicum. J Biol Chem 274, 3923-3926.
22. Pentelute BL, Mandal K, Gates ZP, Sawaya MR, Yeates TO & Kent SB (2010) Total chemical synthesis and X-ray structure of kaliotoxin by racemic protein crystallography. Chem Commun (Camb) 46, 8174-8176.
23. Bang D & Kent SB (2004) A one-pot total synthesis of crambin. Angew Chem Int Ed Engl 43, 2534-2538.
24. Bang D, Pentelute BL & Kent SB (2006) Kinetically controlled ligation for the convergent chemical synthesis of proteins. Angew Chem Int Ed Engl 45, 3985-3988.
25. Ollivier N, Vicogne J, Vallin A, Drobecq H, Desmet R, El Mahdi O, Leclercq B, Goormachtigh G, Fafeur V & Melnyk O (2012) A one-pot three-segment ligation strategy for protein chemical synthesis. Angew Chem Int Ed Engl 51, 209-213.
26. Vogel EM & Imperiali B (2007) Semisynthesis of unnatural amino acid mutants of paxillin: protein probes for cell migration studies. Protein Sci 16, 550-556.
27. Katayama H, Hojo H, Ohira T, Ishii A, Nozaki T, Goto K, Nakahara Y, Takahashi T, Hasegawa Y, Nagasawa H et al. (2010) Correct disulfide pairing is required for the biological activity of crustacean androgenic gland hormone (AGH): synthetic studies of AGH. Biochemistry 49, 1798-1807.
28. Wang Q, Parrish AR & Wang L (2009) Expanding the genetic code for biological studies. Chem Biol 16, 323-336.
29. Mandal K & Kent SB (2011) Total chemical synthesis of biologically active vascular endothelial growth factor. Angew Chem Int Ed Engl 50, 8029-8033.
30. Kamber B, Hartmann A, Eisler K, Riniker B, Rink H, Sieber P & Rittel W (1980) The synthesis of cystine peptides by iodine oxidation of S-trityl-cysteine and S-acetamidomethyl-cysteine peptides. Helv Chim Acta 63, 899-915.
31. Shimonishi Y, Hidaka Y, Koizumi M, Hane M, Aimoto S, Takeda T, Miwatani T & Takeda Y (1987) Mode of disulfide bond formation of a heat-stable enterotoxin (STh) produced by a human strain of enterotoxigenic Escherichia coli. FEBS Lett 215, 165-170.
32. Akaji K, Fujino K, Tatsumi T & Kiso Y (1993) Total synthesis of human insulin by regioselective disulfide formation using the silyl chloride sulfoxide method. J Am Chem Soc 115, 11384-11392.
33. Tam JP, Deng XC & Wang RJ (1999) Solvent assistance in regiospecific disulfide formation in dimethylsulfoxide. Lett Pept Sci 6, 265-273.
34. Royo M, Alsina J, Giralt E, Slomcyznska U & Albericio F (1995) S-phenylacetamidomethyl (Phacm): an orthogonal cysteine protecting group for Boc and Fmoc solid-phase peptide synthesis strategies. J Chem Soc, Perkin Trans 1 1, 1095-1102.
35. Bock A, Forchhammer K, Heider J, Leinfelder W, Sawers G, Veprek B & Zinoni F (1991) Selenocysteine: the 21st amino acid. Mol Microbiol 5, 515-520.
36. Armishaw CJ, Daly NL, Nevin ST, Adams DJ, Craik DJ & Alewood PF (2006) a-selenoconotoxins, a new class of potent a7 neuronal nicotinic receptor antagonists. J Biol Chem 281, 14136-14143.
37. Beld J, Woycechowsky KJ & Hilvert D (2007) Selenoglutathione: efficient oxidative protein folding by a diselenide. Biochemistry 46, 5382-5390.
38. Gray WR, Rivier JE, Galyean R, Cruz LJ & Olivera BM (1983) Conotoxin MI. Disulfide bonding and conformational states. J Biol Chem 258, 12247-12251.
39. Chino N, Kubo S, Kitani T, Yoshida T, Tanabe R, Kobayashi Y, Nakazato M, Kangawa K & Kimura T (1998) Topological isomers of human uroguanylin: interconversion between biologically active and inactive isomers. FEBS Lett 421, 27-31.
40. Hidaka Y, Ohno M, Hemmasi B, Hill O, Forssmann WG & Shimonishi Y (1998) In vitro disulfide-coupled folding of guanylyl cyclase-activating peptide and its precursor protein. Biochemistry 37, 8498-8507.
41. Schulz A, Escher S, Marx UC, Meyer M, Rosch P, Forssmann WG & Adermann K (1998) Carboxy-terminal extension stabilizes the topological stereoisomers of guanylin. J Pept Res 52, 518-525.
42. Hidaka Y, Kubota H, Yoshimura S, Ito H, Takeda Y & Shimonishi Y (1988) Disulfide linkages in a heat-stable enterotoxin (STp) produced by a porcine strain of enterotoxigenic Escherichia coli. Bull Chem Soc Jpn 61, 1265-1271.
43. Ozaki H, Sato T, Kubota H, Hata Y, Katsube Y & Shimonishi Y (1991) Molecular structure of the toxin domain of heat-stable enterotoxin produced by a pathogenic strain of Escherichia coli. A putative binding site for a binding protein on rat intestinal epithelial cell membranes. J Biol Chem 266, 5934-5941.
44. Schulz A, Marx UC, Tidten N, Lauber T, Hidaka Y & Adermann K (2005) Side chain contributions to the interconversion of the topological isomers of guanylinlike peptides. J Pept Sci 11, 319-330.
45. Marx UC, Klodt J, Meyer M, Gerlach H, Rosch P, Forssmann WG & Adermann K (1998) One peptide, two topologies: structure and interconversion dynamics of human uroguanylin isomers. J Pept Res 52, 229-240.
46. Hidaka Y, Shimono C, Ohno M, Okumura N, Adermann K, Forssmann WG & Shimonishi Y (2000) Dual function of the propeptide of prouroguanylin in the folding of the mature peptide: disulfide-coupled folding and dimerization. J Biol Chem 275, 25155-25162.
47. Moss NG, Riguera DA, Solinga RM, Kessler MM, Zimmer DP, Arendshorst WJ, Currie MG & Goy MF (2009) The natriuretic peptide uroguanylin elicits physiologic actions through 2 distinct topoisomers. Hypertension 53, 867-876.
48. Buczek P, Buczek O & Bulaj G (2005) Total chemical synthesis and oxidative folding of δ-conotoxin PVIA containing an N-terminal propeptide. Biopolymers 80, 50-57.
49. Inouye M, Fu X & Shinde U (2001) Substrate-induced activation of a trapped IMC-mediated protein folding intermediate. Nat Struct Biol 8, 321-325.
50. Woycechowsky KJ & Raines RT (2003) The CXC motif: a functional mimic of protein disulfide isomerase. Biochemistry 42, 5387-5394.
51. Gough JD & Lees WJ (2005) Effects of redox buffer properties on the folding of a disulfide-containing protein: dependence upon pH, thiol pKa, and thiol concentration. J Biotechnol 115, 279-290.
52. Salamanca S, Li L, Vendrell J, Aviles FX & Chang JY (2003) Major kinetic traps for the oxidative folding of leech carboxypeptidase inhibitor. Biochemistry 42, 6754-6761.
53. Buchner J & Rudolph R (1991) Renaturation, purification and characterization of recombinant Fab-fragments produced in Escherichia coli. Biotechnology (NY) 9, 157-162.
54. Chambers I, Frampton J, Goldfarb P, Affara N, McBain W & Harrison PR (1986) The structure of the mouse glutathione peroxidase gene: the selenocysteine in the active site is encoded by the 'termination' codon, TGA. EMBO J 5, 1221-1227.
55. Lindley H (1960) A study of the kinetics of the reaction between thiol compounds and choloracetamide. Biochem J 74, 577-584.
56. Edsall JT & Wyman J (1958) Biophysical Chemistry. Academic Press Inc., New York.
57. Friedman M, Cavins JF & Wall JS (1965) Relative nucleophilic reactivities of amino groups and mercaptide ions in addition reactions with a,b-unsaturated compounds. J Am Chem Soc 87, 3672-3682.
58. Huber RE & Criddle RS (1967) Comparison of the chemical properties of selenocysteine and selenocystine with their sulfur analogs. Arch Biochem Biophys 122, 164-173.
59. Vuillard L, Rabilloud T, Leberman R, Berthet-Colominas C & Cusack S (1994) A new additive for protein crystallization. FEBS Lett 353, 294-296.
60. Bhuyan AK (2002) Protein stabilization by urea and guanidine hydrochloride. Biochemistry 41, 13386-13394.
61. Baynes BM, Wang DI & Trout BL (2005) Role of arginine in the stabilization of proteins against aggregation. Biochemistry 44, 4919-4925.
62. Creighton TE (1992) Folding pathway determined using disulfide bonds. In Protein Folding (Creighton TE ed), pp. 301-352. WH Freeman, New York.
63. Smith DC & Hider RC (1988) Thiol exchange catalysed refolding of small proteins utilizing solid-phase supports. Biophys Chem 31, 21-28.
64. Reddy K RC, Lilie H, Rudolph R & Lange C (2005) l-Arginine increases the solubility of unfolded species of hen egg white lysozyme. Protein Sci 14, 926-935.
65. Chen J, Liu Y, Li X, Wang Y, Ding H, Ma G & Su Z (2009) Cooperative effects of urea and l-arginine on protein refolding. Protein Expr Purif 66, 82-90.
66. Tsumoto K, Shinoki K, Kondo H, Uchikawa M, Juji T & Kumagai I (1998) Highly efficient recovery of functional single-chain Fv fragments from inclusion bodies overexpressed in Escherichia coli by controlled introduction of oxidizing reagent-application to a human single-chain Fv fragment. J Immunol Methods 219, 119-129.
67. Lange C, Patil G & Rudolph R (2005) Ionic liquids as refolding additives: N'-alkyl and N'-(x-hydroxyalkyl) N-methylimidazolium chlorides. Protein Sci 14, 2693-2701.
68. Hamada H & Shiraki K (2007) l-argininamide improves the refolding more effectively than l-arginine. J Biotechnol 130, 153-160.
69. Ito L, Shiraki K, Makino M, Hasegawa K & Kumasaka T (2011) Glycine amide shielding on the aromatic surfaces of lysozyme: implication for suppression of protein aggregation. FEBS Lett 585, 555-560.
70. Luo P & Baldwin RL (1997) Mechanism of helix induction by trifluoroethanol: a framework for extrapolating the helix-forming properties of peptides from trifluoroethanol ? water mixtures back to water. Biochemistry 36, 8413-8421.
71. Kentsis A & Sosnick TR (1998) Trifluoroethanol promotes helix formation by destabilizing backbone exposure: desolvation rather than native hydrogen bonding defines the kinetic pathway of dimeric coiled coil folding. Biochemistry 37, 14613-14622.
72. Siligardi G, Drake AF, Mascagni P, Neri P, Lozzi L, Niccolai N & Gibbons WA (1987) Resolution of conformation equilibria in linear peptides by circular dichroism in cryogenic solvents. Biochem Biophys Res Commun 143, 1005-1011.
73. Cann JR, London RE, Unkefer CJ, Vavrek RJ & Stewart JM (1987) CD-n.m.r. study of the solution conformation of bradykinin analogs containing a-aminoisobutyric acid. Int J Pept Protein Res 29, 486-496.
74. Dubey VK, Shah A, Jagannadham MV & Kayastha AM (2006) Effect of organic solvents on the molten globule state of procerain: β-sheet to α-helix switchover in presence of trifluoroethanol. Protein Pept Lett 13, 545-547.