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. 1996 Oct;5(10):1973–1983. doi: 10.1002/pro.5560051003

Protein secondary structural types are differentially coded on messenger RNA.

T A Thanaraj 1, P Argos 1
PMCID: PMC2143259  PMID: 8897597

Abstract

Tricodon regions on messenger RNAs corresponding to a set of proteins from Escherichia coli were scrutinized for their translation speed. The fractional frequency values of the individual codons as they occur in mRNAs of highly expressed genes from Escherichia coli were taken as an indicative measure of the translation speed. The tricodons were classified by the sum of the frequency values of the constituent codons. Examination of the conformation of the encoded amino acid residues in the corresponding protein tertiary structures revealed a correlation between codon usage in mRNA and topological features of the encoded proteins. Alpha helices on proteins tend to be preferentially coded by translationally fast mRNA regions while the slow segments often code for beta strands and coil regions. Fast regions correspondingly avoid coding for beta strands and coil regions while the slow regions similarly move away from encoding alpha helices. Structural and mechanistic aspects of the ribosome peptide channel support the relevance of sequence fragment translation and subsequent conformation. A discussion is presented relating the observation to the reported kinetic data on the formation and stabilization of protein secondary structural types during protein folding. The observed absence of such strong positive selection for codons in non-highly expressed genes is compatible with existing theories that mutation pressure may well dominate codon selection in non-highly expressed genes.

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Selected References

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  1. Andersson S. G., Kurland C. G. Codon preferences in free-living microorganisms. Microbiol Rev. 1990 Jun;54(2):198–210. doi: 10.1128/mr.54.2.198-210.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anfinsen C. B. Principles that govern the folding of protein chains. Science. 1973 Jul 20;181(4096):223–230. doi: 10.1126/science.181.4096.223. [DOI] [PubMed] [Google Scholar]
  3. Baldwin R. L. Intermediates in protein folding reactions and the mechanism of protein folding. Annu Rev Biochem. 1975;44:453–475. doi: 10.1146/annurev.bi.44.070175.002321. [DOI] [PubMed] [Google Scholar]
  4. Bernstein F. C., Koetzle T. F., Williams G. J., Meyer E. F., Jr, Brice M. D., Rodgers J. R., Kennard O., Shimanouchi T., Tasumi M. The Protein Data Bank: a computer-based archival file for macromolecular structures. J Mol Biol. 1977 May 25;112(3):535–542. doi: 10.1016/s0022-2836(77)80200-3. [DOI] [PubMed] [Google Scholar]
  5. Blobel G., Sabatini D. D. Controlled proteolysis of nascent polypeptides in rat liver cell fractions. I. Location of the polypeptides within ribosomes. J Cell Biol. 1970 Apr;45(1):130–145. doi: 10.1083/jcb.45.1.130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bonekamp F., Andersen H. D., Christensen T., Jensen K. F. Codon-defined ribosomal pausing in Escherichia coli detected by using the pyrE attenuator to probe the coupling between transcription and translation. Nucleic Acids Res. 1985 Jun 11;13(11):4113–4123. doi: 10.1093/nar/13.11.4113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Briggs M. S., Roder H. Early hydrogen-bonding events in the folding reaction of ubiquitin. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2017–2021. doi: 10.1073/pnas.89.6.2017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brimacombe R. The structure of ribosomal RNA: a three-dimensional jigsaw puzzle. Eur J Biochem. 1995 Jun 1;230(2):365–383. [PubMed] [Google Scholar]
  9. Buck M., Radford S. E., Dobson C. M. A partially folded state of hen egg white lysozyme in trifluoroethanol: structural characterization and implications for protein folding. Biochemistry. 1993 Jan 19;32(2):669–678. doi: 10.1021/bi00053a036. [DOI] [PubMed] [Google Scholar]
  10. Buck M., Radford S. E., Dobson C. M. Amide hydrogen exchange in a highly denatured state. Hen egg-white lysozyme in urea. J Mol Biol. 1994 Apr 1;237(3):247–254. doi: 10.1006/jmbi.1994.1228. [DOI] [PubMed] [Google Scholar]
  11. Candelas G. C., Ortiz A., Ortiz N. Features of the cell-free translation of a spider fibroin mRNA. Biochem Cell Biol. 1989 Feb-Mar;67(2-3):173–176. doi: 10.1139/o89-026. [DOI] [PubMed] [Google Scholar]
  12. Carlsson U., Jonsson B. H. Folding of beta-sheet proteins. Curr Opin Struct Biol. 1995 Aug;5(4):482–487. doi: 10.1016/0959-440x(95)80032-8. [DOI] [PubMed] [Google Scholar]
  13. Chaney W. G., Morris A. J. Nonuniform size distribution of nascent peptides. The effect of messenger RNA structure upon the rate of translation. Arch Biochem Biophys. 1979 Apr 15;194(1):283–291. doi: 10.1016/0003-9861(79)90620-9. [DOI] [PubMed] [Google Scholar]
  14. Chyan C. L., Wormald C., Dobson C. M., Evans P. A., Baum J. Structure and stability of the molten globule state of guinea-pig alpha-lactalbumin: a hydrogen exchange study. Biochemistry. 1993 Jun 1;32(21):5681–5691. doi: 10.1021/bi00072a025. [DOI] [PubMed] [Google Scholar]
  15. Colloc'h N., Etchebest C., Thoreau E., Henrissat B., Mornon J. P. Comparison of three algorithms for the assignment of secondary structure in proteins: the advantages of a consensus assignment. Protein Eng. 1993 Jun;6(4):377–382. doi: 10.1093/protein/6.4.377. [DOI] [PubMed] [Google Scholar]
  16. Deana A., Ehrlich R., Reiss C. Synonymous codon selection controls in vivo turnover and amount of mRNA in Escherichia coli bla and ompA genes. J Bacteriol. 1996 May;178(9):2718–2720. doi: 10.1128/jb.178.9.2718-2720.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dobson C. M., Evans P. A., Radford S. E. Understanding how proteins fold: the lysozyme story so far. Trends Biochem Sci. 1994 Jan;19(1):31–37. doi: 10.1016/0968-0004(94)90171-6. [DOI] [PubMed] [Google Scholar]
  18. Doniach S., Bascle J., Garel T., Orland H. Partially folded states of proteins: characterization by X-ray scattering. J Mol Biol. 1995 Dec 15;254(5):960–967. doi: 10.1006/jmbi.1995.0668. [DOI] [PubMed] [Google Scholar]
  19. Farrow N. A., Zhang O., Forman-Kay J. D., Kay L. E. Comparison of the backbone dynamics of a folded and an unfolded SH3 domain existing in equilibrium in aqueous buffer. Biochemistry. 1995 Jan 24;34(3):868–878. doi: 10.1021/bi00003a021. [DOI] [PubMed] [Google Scholar]
  20. Feng Y., Sligar S. G., Wand A. J. Solution structure of apocytochrome b562. Nat Struct Biol. 1994 Jan;1(1):30–35. doi: 10.1038/nsb0194-30. [DOI] [PubMed] [Google Scholar]
  21. Finkelstein A. V. Rate of beta-structure formation in polypeptides. Proteins. 1991;9(1):23–27. doi: 10.1002/prot.340090104. [DOI] [PubMed] [Google Scholar]
  22. Frank J., Zhu J., Penczek P., Li Y., Srivastava S., Verschoor A., Radermacher M., Grassucci R., Lata R. K., Agrawal R. K. A model of protein synthesis based on cryo-electron microscopy of the E. coli ribosome. Nature. 1995 Aug 3;376(6539):441–444. doi: 10.1038/376441a0. [DOI] [PubMed] [Google Scholar]
  23. Friguet B., Djavadi-Ohaniance L., King J., Goldberg M. E. In vitro and ribosome-bound folding intermediates of P22 tailspike protein detected with monoclonal antibodies. J Biol Chem. 1994 Jun 3;269(22):15945–15949. [PubMed] [Google Scholar]
  24. Harms E., Umbarger H. E. Role of codon choice in the leader region of the ilvGMEDA operon of Serratia marcescens. J Bacteriol. 1987 Dec;169(12):5668–5677. doi: 10.1128/jb.169.12.5668-5677.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hartl F. U., Hlodan R., Langer T. Molecular chaperones in protein folding: the art of avoiding sticky situations. Trends Biochem Sci. 1994 Jan;19(1):20–25. doi: 10.1016/0968-0004(94)90169-4. [DOI] [PubMed] [Google Scholar]
  26. Hunt J. F., Weaver A. J., Landry S. J., Gierasch L., Deisenhofer J. The crystal structure of the GroES co-chaperonin at 2.8 A resolution. Nature. 1996 Jan 4;379(6560):37–45. doi: 10.1038/379037a0. [DOI] [PubMed] [Google Scholar]
  27. Ikemura T. Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol. 1985 Jan;2(1):13–34. doi: 10.1093/oxfordjournals.molbev.a040335. [DOI] [PubMed] [Google Scholar]
  28. Ikemura T., Ozeki H. Codon usage and transfer RNA contents: organism-specific codon-choice patterns in reference to the isoacceptor contents. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 2):1087–1097. doi: 10.1101/sqb.1983.047.01.123. [DOI] [PubMed] [Google Scholar]
  29. Jacobs M. D., Fox R. O. Staphylococcal nuclease folding intermediate characterized by hydrogen exchange and NMR spectroscopy. Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):449–453. doi: 10.1073/pnas.91.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 1983 Dec;22(12):2577–2637. doi: 10.1002/bip.360221211. [DOI] [PubMed] [Google Scholar]
  31. Komar A. A., Jaenicke R. Kinetics of translation of gamma B crystallin and its circularly permutated variant in an in vitro cell-free system: possible relations to codon distribution and protein folding. FEBS Lett. 1995 Dec 4;376(3):195–198. doi: 10.1016/0014-5793(95)01275-0. [DOI] [PubMed] [Google Scholar]
  32. Krasheninnikov I. A., Komar A. A., Adzhubei I. A. Rol' vyrozhdennosti koda v opredelenii puti kotransliatsionnogo svorachivaniia belka. Biokhimiia. 1989 Feb;54(2):187–200. [PubMed] [Google Scholar]
  33. Kudlicki W., Kitaoka Y., Odom O. W., Kramer G., Hardesty B. Elongation and folding of nascent ricin chains as peptidyl-tRNA on ribosomes: the effect of amino acid deletions on these processes. J Mol Biol. 1995 Sep 15;252(2):203–212. doi: 10.1006/jmbi.1995.0488. [DOI] [PubMed] [Google Scholar]
  34. Kudlicki W., Odom O. W., Kramer G., Hardesty B. Chaperone-dependent folding and activation of ribosome-bound nascent rhodanese. Analysis by fluorescence. J Mol Biol. 1994 Dec 2;244(3):319–331. doi: 10.1006/jmbi.1994.1732. [DOI] [PubMed] [Google Scholar]
  35. Kypr J. A part of codon bias in genes protects protein spatial structures from destabilization by random single point mutations. Biochem Biophys Res Commun. 1986 Sep 30;139(3):1094–1097. doi: 10.1016/s0006-291x(86)80289-3. [DOI] [PubMed] [Google Scholar]
  36. Liljenström H., von Heijne G. Translation rate modification by preferential codon usage: intragenic position effects. J Theor Biol. 1987 Jan 7;124(1):43–55. doi: 10.1016/s0022-5193(87)80251-5. [DOI] [PubMed] [Google Scholar]
  37. Lim V. I., Spirin A. S. Stereochemical analysis of ribosomal transpeptidation. Conformation of nascent peptide. J Mol Biol. 1986 Apr 20;188(4):565–574. doi: 10.1016/s0022-2836(86)80006-7. [DOI] [PubMed] [Google Scholar]
  38. Lipman D. J., Wilbur W. J. Contextual constraints on synonymous codon choice. J Mol Biol. 1983 Jan 25;163(3):363–376. doi: 10.1016/0022-2836(83)90063-3. [DOI] [PubMed] [Google Scholar]
  39. Liu Z. P., Rizo J., Gierasch L. M. Equilibrium folding studies of cellular retinoic acid binding protein, a predominantly beta-sheet protein. Biochemistry. 1994 Jan 11;33(1):134–142. doi: 10.1021/bi00167a017. [DOI] [PubMed] [Google Scholar]
  40. Lobry J. R., Gautier C. Hydrophobicity, expressivity and aromaticity are the major trends of amino-acid usage in 999 Escherichia coli chromosome-encoded genes. Nucleic Acids Res. 1994 Aug 11;22(15):3174–3180. doi: 10.1093/nar/22.15.3174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Logan T. M., Thériault Y., Fesik S. W. Structural characterization of the FK506 binding protein unfolded in urea and guanidine hydrochloride. J Mol Biol. 1994 Feb 18;236(2):637–648. doi: 10.1006/jmbi.1994.1173. [DOI] [PubMed] [Google Scholar]
  42. Mullins L. S., Pace C. N., Raushel F. M. Investigation of ribonuclease T1 folding intermediates by hydrogen-deuterium amide exchange-two-dimensional NMR spectroscopy. Biochemistry. 1993 Jun 22;32(24):6152–6156. doi: 10.1021/bi00075a006. [DOI] [PubMed] [Google Scholar]
  43. Narayana S. V., Argos P. Residue contacts in protein structures and implications for protein folding. Int J Pept Protein Res. 1984 Jul;24(1):25–39. doi: 10.1111/j.1399-3011.1984.tb00924.x. [DOI] [PubMed] [Google Scholar]
  44. Phillips D. C. The three-dimensional structure of an enzyme molecule. Sci Am. 1966 Nov;215(5):78–90. doi: 10.1038/scientificamerican1166-78. [DOI] [PubMed] [Google Scholar]
  45. Ptitsyn O. B. How the molten globule became. Trends Biochem Sci. 1995 Sep;20(9):376–379. doi: 10.1016/s0968-0004(00)89081-7. [DOI] [PubMed] [Google Scholar]
  46. Purvis I. J., Bettany A. J., Santiago T. C., Coggins J. R., Duncan K., Eason R., Brown A. J. The efficiency of folding of some proteins is increased by controlled rates of translation in vivo. A hypothesis. J Mol Biol. 1987 Jan 20;193(2):413–417. doi: 10.1016/0022-2836(87)90230-0. [DOI] [PubMed] [Google Scholar]
  47. Redfield C., Smith R. A., Dobson C. M. Structural characterization of a highly-ordered 'molten globule' at low pH. Nat Struct Biol. 1994 Jan;1(1):23–29. doi: 10.1038/nsb0194-23. [DOI] [PubMed] [Google Scholar]
  48. Rice C. M., Fuchs R., Higgins D. G., Stoehr P. J., Cameron G. N. The EMBL data library. Nucleic Acids Res. 1993 Jul 1;21(13):2967–2971. doi: 10.1093/nar/21.13.2967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Roder H., Elöve G. A., Englander S. W. Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR. Nature. 1988 Oct 20;335(6192):700–704. doi: 10.1038/335700a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Sharp P. M., Li W. H. Codon usage in regulatory genes in Escherichia coli does not reflect selection for 'rare' codons. Nucleic Acids Res. 1986 Oct 10;14(19):7737–7749. doi: 10.1093/nar/14.19.7737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Sharp P. M., Li W. H. The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 1987 Feb 11;15(3):1281–1295. doi: 10.1093/nar/15.3.1281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Sharp P. M., Stenico M., Peden J. F., Lloyd A. T. Codon usage: mutational bias, translational selection, or both? Biochem Soc Trans. 1993 Nov;21(4):835–841. doi: 10.1042/bst0210835. [DOI] [PubMed] [Google Scholar]
  53. Sharp P. M., Tuohy T. M., Mosurski K. R. Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Res. 1986 Jul 11;14(13):5125–5143. doi: 10.1093/nar/14.13.5125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Shiraki K., Nishikawa K., Goto Y. Trifluoroethanol-induced stabilization of the alpha-helical structure of beta-lactoglobulin: implication for non-hierarchical protein folding. J Mol Biol. 1995 Jan 13;245(2):180–194. doi: 10.1006/jmbi.1994.0015. [DOI] [PubMed] [Google Scholar]
  55. Shpaer E. G. Constraints on codon context in Escherichia coli genes. Their possible role in modulating the efficiency of translation. J Mol Biol. 1986 Apr 20;188(4):555–564. doi: 10.1016/s0022-2836(86)80005-5. [DOI] [PubMed] [Google Scholar]
  56. Sosnick T. R., Mayne L., Hiller R., Englander S. W. The barriers in protein folding. Nat Struct Biol. 1994 Mar;1(3):149–156. doi: 10.1038/nsb0394-149. [DOI] [PubMed] [Google Scholar]
  57. Stade K., Jünke N., Brimacombe R. Mapping the path of the nascent peptide chain through the 23S RNA in the 50S ribosomal subunit. Nucleic Acids Res. 1995 Jul 11;23(13):2371–2380. doi: 10.1093/nar/23.13.2371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Stark H., Mueller F., Orlova E. V., Schatz M., Dube P., Erdemir T., Zemlin F., Brimacombe R., van Heel M. The 70S Escherichia coli ribosome at 23 A resolution: fitting the ribosomal RNA. Structure. 1995 Aug 15;3(8):815–821. doi: 10.1016/s0969-2126(01)00216-7. [DOI] [PubMed] [Google Scholar]
  59. Sørensen M. A., Kurland C. G., Pedersen S. Codon usage determines translation rate in Escherichia coli. J Mol Biol. 1989 May 20;207(2):365–377. doi: 10.1016/0022-2836(89)90260-x. [DOI] [PubMed] [Google Scholar]
  60. Sørensen M. A., Pedersen S. Absolute in vivo translation rates of individual codons in Escherichia coli. The two glutamic acid codons GAA and GAG are translated with a threefold difference in rate. J Mol Biol. 1991 Nov 20;222(2):265–280. doi: 10.1016/0022-2836(91)90211-n. [DOI] [PubMed] [Google Scholar]
  61. Taylor F. J., Coates D. The code within the codons. Biosystems. 1989;22(3):177–187. doi: 10.1016/0303-2647(89)90059-2. [DOI] [PubMed] [Google Scholar]
  62. Tokatlidis K., Friguet B., Deville-Bonne D., Baleux F., Fedorov A. N., Navon A., Djavadi-Ohaniance L., Goldberg M. E. Nascent chains: folding and chaperone interaction during elongation on ribosomes. Philos Trans R Soc Lond B Biol Sci. 1995 Apr 29;348(1323):89–95. doi: 10.1098/rstb.1995.0049. [DOI] [PubMed] [Google Scholar]
  63. Trifonov E. N. The multiple codes of nucleotide sequences. Bull Math Biol. 1989;51(4):417–432. doi: 10.1007/BF02460081. [DOI] [PubMed] [Google Scholar]
  64. Tsalkova T., Zardeneta G., Kudlicki W., Kramer G., Horowitz P. M., Hardesty B. GroEL and GroES increase the specific enzymatic activity of newly-synthesized rhodanese if present during in vitro transcription/translation. Biochemistry. 1993 Apr 6;32(13):3377–3380. doi: 10.1021/bi00064a022. [DOI] [PubMed] [Google Scholar]
  65. Tu C., Tzeng T. H., Bruenn J. A. Ribosomal movement impeded at a pseudoknot required for frameshifting. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8636–8640. doi: 10.1073/pnas.89.18.8636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Udgaonkar J. B., Baldwin R. L. Early folding intermediate of ribonuclease A. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8197–8201. doi: 10.1073/pnas.87.21.8197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Varenne S., Baty D., Verheij H., Shire D., Lazdunski C. The maximum rate of gene expression is dependent on the downstream context of unfavourable codons. Biochimie. 1989 Nov-Dec;71(11-12):1221–1229. doi: 10.1016/0300-9084(89)90027-8. [DOI] [PubMed] [Google Scholar]
  68. Volkenstein M. V. The genetic coding of protein structure. Biochim Biophys Acta. 1966 May 19;119(2):421–424. doi: 10.1016/0005-2787(66)90204-8. [DOI] [PubMed] [Google Scholar]
  69. Walther D., Argos P. Intrahelical side chain-side chain contacts: the consequences of restricted rotameric states and implications for helix engineering and design. Protein Eng. 1996 Jun;9(6):471–478. doi: 10.1093/protein/9.6.471. [DOI] [PubMed] [Google Scholar]
  70. Wiedmann B., Sakai H., Davis T. A., Wiedmann M. A protein complex required for signal-sequence-specific sorting and translocation. Nature. 1994 Aug 11;370(6489):434–440. doi: 10.1038/370434a0. [DOI] [PubMed] [Google Scholar]
  71. Williams S., Causgrove T. P., Gilmanshin R., Fang K. S., Callender R. H., Woodruff W. H., Dyer R. B. Fast events in protein folding: helix melting and formation in a small peptide. Biochemistry. 1996 Jan 23;35(3):691–697. doi: 10.1021/bi952217p. [DOI] [PubMed] [Google Scholar]
  72. Woese C. R., Dugre D. H., Saxinger W. C., Dugre S. A. The molecular basis for the genetic code. Proc Natl Acad Sci U S A. 1966 Apr;55(4):966–974. doi: 10.1073/pnas.55.4.966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Yamao F., Andachi Y., Muto A., Ikemura T., Osawa S. Levels of tRNAs in bacterial cells as affected by amino acid usage in proteins. Nucleic Acids Res. 1991 Nov 25;19(22):6119–6122. doi: 10.1093/nar/19.22.6119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Yang A. S., Honig B. Free energy determinants of secondary structure formation: II. Antiparallel beta-sheets. J Mol Biol. 1995 Sep 22;252(3):366–376. doi: 10.1006/jmbi.1995.0503. [DOI] [PubMed] [Google Scholar]
  75. Yarus M., Folley L. S. Sense codons are found in specific contexts. J Mol Biol. 1985 Apr 20;182(4):529–540. doi: 10.1016/0022-2836(85)90239-6. [DOI] [PubMed] [Google Scholar]
  76. Yonath A. Approaching atomic resolution in crystallography of ribosomes. Annu Rev Biophys Biomol Struct. 1992;21:77–93. doi: 10.1146/annurev.bb.21.060192.000453. [DOI] [PubMed] [Google Scholar]
  77. Zhang S., Goldman E., Zubay G. Clustering of low usage codons and ribosome movement. J Theor Biol. 1994 Oct 21;170(4):339–354. doi: 10.1006/jtbi.1994.1196. [DOI] [PubMed] [Google Scholar]
  78. de Prat Gay G., Ruiz-Sanz J., Neira J. L., Corrales F. J., Otzen D. E., Ladurner A. G., Fersht A. R. Conformational pathway of the polypeptide chain of chymotrypsin inhibitor-2 growing from its N terminus in vitro. Parallels with the protein folding pathway. J Mol Biol. 1995 Dec 15;254(5):968–979. doi: 10.1006/jmbi.1995.0669. [DOI] [PubMed] [Google Scholar]

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