{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T19:25:15Z","timestamp":1790623515100,"version":"4.1.0"},"reference-count":45,"publisher":"Springer Science and Business Media LLC","issue":"12","license":[{"start":{"date-parts":[[2016,10,17]],"date-time":"2016-10-17T00:00:00Z","timestamp":1476662400000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Chem Biol"],"published-print":{"date-parts":[[2016,12]]},"DOI":"10.1038\/nchembio.2206","type":"journal-article","created":{"date-parts":[[2016,10,17]],"date-time":"2016-10-17T11:48:23Z","timestamp":1476704903000},"page":"1084-1088","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":119,"title":["A prevalent intraresidue hydrogen bond stabilizes proteins"],"prefix":"10.1038","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2020-2641","authenticated-orcid":false,"given":"Robert W","family":"Newberry","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ronald T","family":"Raines","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2016,10,17]]},"reference":[{"key":"BFnchembio2206_CR1","doi-asserted-by":"publisher","first-page":"1042","DOI":"10.1126\/science.1219021","volume":"338","author":"KA Dill","year":"2012","unstructured":"Dill, K.A. & MacCallum, J.L. The protein-folding problem, 50 years on. Science 338, 1042\u20131046 (2012).","journal-title":"Science"},{"key":"BFnchembio2206_CR2","doi-asserted-by":"publisher","first-page":"7133","DOI":"10.1021\/bi00483a001","volume":"29","author":"KA Dill","year":"1990","unstructured":"Dill, K.A. Dominant forces in protein folding. Biochemistry 29, 7133\u20137155 (1990).","journal-title":"Biochemistry"},{"key":"BFnchembio2206_CR3","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1073\/pnas.37.4.205","volume":"37","author":"L Pauling","year":"1951","unstructured":"Pauling, L., Corey, R.B. & Branson, H.R. The structure of proteins; two hydrogen-bonded helical configurations of the polypeptide chain. Proc. Natl. Acad. Sci. USA 37, 205\u2013211 (1951).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"BFnchembio2206_CR4","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1073\/pnas.37.5.251","volume":"37","author":"L Pauling","year":"1951","unstructured":"Pauling, L. & Corey, R.B. The pleated sheet, a new layer configuration of polypeptide chains. Proc. Natl. Acad. Sci. USA 37, 251\u2013256 (1951).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"BFnchembio2206_CR5","doi-asserted-by":"publisher","first-page":"2577","DOI":"10.1002\/bip.360221211","volume":"22","author":"W Kabsch","year":"1983","unstructured":"Kabsch, W. & Sander, C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577\u20132637 (1983).","journal-title":"Biopolymers"},{"key":"BFnchembio2206_CR6","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1039\/C4RP00057A","volume":"15","author":"AD Clauss","year":"2014","unstructured":"Clauss, A.D. et al. Rabbit-ears hybrids, VSEPR sterics, and other orbital anachronisms. Chem. Educ. Res. Pract. 15, 417\u2013434 (2014).10.1039\/C4RP00057A","journal-title":"Chem. Educ. Res. Pract."},{"key":"BFnchembio2206_CR7","doi-asserted-by":"publisher","first-page":"615","DOI":"10.1038\/nchembio.406","volume":"6","author":"GJ Bartlett","year":"2010","unstructured":"Bartlett, G.J., Choudhary, A., Raines, R.T. & Woolfson, D.N. n\u2192\u03c0* interactions in proteins.\u00a0Nat. Chem. Biol. 6, 615\u2013620 (2010).","journal-title":"\u00a0Nat. Chem. Biol."},{"key":"BFnchembio2206_CR8","doi-asserted-by":"publisher","first-page":"887","DOI":"10.1002\/pro.2896","volume":"25","author":"GJ Bartlett","year":"2016","unstructured":"Bartlett, G.J. & Woolfson, D.N. On the satisfaction of backbone-carbonyl lone pairs of electrons in protein structures. Protein Sci. 25, 887\u2013897 (2016).10.1002\/pro.2896","journal-title":"Protein Sci."},{"key":"BFnchembio2206_CR9","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1002\/bip.1969.360080107","volume":"8","author":"M Avignon","year":"1969","unstructured":"Avignon, M., Huong, P.V., Lascombe, J., Marraud, M. & Neel, J. Etude, par spectroscopie infra-rouge, de la conformation de quelques compos\u00e9s peptidiques mod\u00e8les. Biopolymers 8, 69\u201389 (1969).","journal-title":"Biopolymers"},{"key":"BFnchembio2206_CR10","doi-asserted-by":"publisher","first-page":"2177","DOI":"10.1002\/bip.1973.360120920","volume":"12","author":"AW Burgess","year":"1973","unstructured":"Burgess, A.W. & Scheraga, H.A. Communications to the editor: Stable conformations of dipeptides. Biopolymers 12, 2177\u20132183 (1973).","journal-title":"Biopolymers"},{"key":"BFnchembio2206_CR11","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3109\/10409238009105471","volume":"9","author":"C Toniolo","year":"1980","unstructured":"Toniolo, C. Intramolecularly hydrogen-bonded peptide conformations. CRC Crit. Rev. Biochem. 9, 1\u201344 (1980).","journal-title":"CRC Crit. Rev. Biochem."},{"key":"BFnchembio2206_CR12","doi-asserted-by":"publisher","first-page":"10688","DOI":"10.1063\/1.1521132","volume":"117","author":"BC Dian","year":"2002","unstructured":"Dian, B.C. et al. The infrared and ultraviolet spectra of single conformations of methyl-capped dipeptides: N-acetyl tryptophan amide and N-acetyl tryptophan methyl amide. J. Chem. Phys. 117, 10688\u201310702 (2002).","journal-title":"J. Chem. Phys."},{"key":"BFnchembio2206_CR13","doi-asserted-by":"publisher","first-page":"11675","DOI":"10.1021\/ja048317c","volume":"126","author":"S Blanco","year":"2004","unstructured":"Blanco, S., Lesarri, A., L\u00f3pez, J.C. & Alonso, J.L. The gas-phase structure of alanine. J. Am. Chem. Soc. 126, 11675\u201311683 (2004).10.1021\/ja048317c","journal-title":"J. Am. Chem. Soc."},{"key":"BFnchembio2206_CR14","doi-asserted-by":"publisher","first-page":"3295","DOI":"10.1002\/anie.201510983","volume":"55","author":"AI Gonz\u00e1lez Fl\u00f3rez","year":"2016","unstructured":"Gonz\u00e1lez Fl\u00f3rez, A.I. et al. Charge-induced unzipping of isolated proteins to a defined secondary structure. Angew. Chem. Int. Ed. Engl. 55, 3295\u20133299 (2016).10.1002\/anie.201510983","journal-title":"Angew. Chem. Int. Ed. Engl."},{"key":"BFnchembio2206_CR15","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1021\/ma60055a001","volume":"10","author":"SS Zimmerman","year":"1977","unstructured":"Zimmerman, S.S., Pottle, M.S., N\u00e9methy, G. & Scheraga, H.A. Conformational analysis of the 20 naturally occurring amino acid residues using ECEPP. Macromolecules 10, 1\u20139 (1977).","journal-title":"Macromolecules"},{"key":"BFnchembio2206_CR16","doi-asserted-by":"publisher","first-page":"16132","DOI":"10.1021\/jp053416d","volume":"109","author":"S Scheiner","year":"2005","unstructured":"Scheiner, S. Relative strengths of NH.O and CH.O hydrogen bonds between polypeptide chain segments. J. Phys. Chem. B 109, 16132\u201316141 (2005).10.1021\/jp053416d","journal-title":"J. Phys. Chem. B"},{"key":"BFnchembio2206_CR17","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1002\/1521-3773(20020104)41:1<48::AID-ANIE48>3.0.CO;2-U","volume":"41","author":"T Steiner","year":"2002","unstructured":"Steiner, T. The hydrogen bond in the solid state. Angew. Chem. Int. Ed. Engl. 41, 48\u201376 (2002).","journal-title":"Angew. Chem. Int. Ed. Engl."},{"key":"BFnchembio2206_CR18","doi-asserted-by":"publisher","first-page":"777","DOI":"10.1006\/jmbi.1994.1334","volume":"238","author":"IK McDonald","year":"1994","unstructured":"McDonald, I.K. & Thornton, J.M. Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238, 777\u2013793 (1994).","journal-title":"J. Mol. Biol."},{"key":"BFnchembio2206_CR19","doi-asserted-by":"publisher","first-page":"7384","DOI":"10.1021\/jp953141","volume":"100","author":"RS Rowland","year":"1996","unstructured":"Rowland, R.S. & Taylor, R. Intermolecular nonbonded contact distances in organic crystal structures: comparison with distances expected from van der Waals radii. J. Phys. Chem. 100, 7384\u20137391 (1996).10.1021\/jp953141","journal-title":"J. Phys. Chem."},{"key":"BFnchembio2206_CR20","doi-asserted-by":"publisher","first-page":"899","DOI":"10.1021\/cr00088a005","volume":"88","author":"AE Reed","year":"1988","unstructured":"Reed, A.E., Curtiss, L.A. & Weinhold, F. Intermolecular interactions from a natural bond orbital, donor\u2013acceptor viewpoint. Chem. Rev. 88, 899\u2013926 (1988).","journal-title":"Chem. Rev."},{"key":"BFnchembio2206_CR21","doi-asserted-by":"publisher","first-page":"1188","DOI":"10.1110\/ps.0241903","volume":"12","author":"MP Hinderaker","year":"2003","unstructured":"Hinderaker, M.P. & Raines, R.T. An electronic effect on protein structure. Protein Sci. 12, 1188\u20131194 (2003).","journal-title":"Protein Sci."},{"key":"BFnchembio2206_CR22","doi-asserted-by":"publisher","first-page":"7244","DOI":"10.1021\/ja901188y","volume":"131","author":"A Choudhary","year":"2009","unstructured":"Choudhary, A., Gandla, D., Krow, G.R. & Raines, R.T. Nature of amide carbonyl\u2013carbonyl interactions in proteins. J. Am. Chem. Soc. 131, 7244\u20137246 (2009).","journal-title":"J. Am. Chem. Soc."},{"key":"BFnchembio2206_CR23","doi-asserted-by":"publisher","first-page":"7843","DOI":"10.1021\/ja4033583","volume":"135","author":"RW Newberry","year":"2013","unstructured":"Newberry, R.W., VanVeller, B., Guzei, I.A. & Raines, R.T. n\u2192\u03c0* interactions of amides and thioamides: implications for protein stability. J. Am. Chem. Soc. 135, 7843\u20137846 (2013).10.1021\/ja4033583","journal-title":"J. Am. Chem. Soc."},{"key":"BFnchembio2206_CR24","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1002\/bip.360270302","volume":"27","author":"E Benedetti","year":"1988","unstructured":"Benedetti, E. et al. Structural versatility of peptides from C\u03b1,\u03b1-dialkylated glycines. I. A conformational energy computation and X-ray diffraction study of homo-peptides from C\u03b1,\u03b1-diethylglycine. Biopolymers 27, 357\u2013371 (1988).10.1002\/bip.360270302","journal-title":"Biopolymers"},{"key":"BFnchembio2206_CR25","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1002\/bip.360270303","volume":"27","author":"C Toniolo","year":"1988","unstructured":"Toniolo, C. et al. Structural versatility of peptides from C\u03b1,\u03b1-dialkylated glycines. II. An IR absorption and 1H-NMR study of homo-oligopeptides from C\u03b1,\u03b1-diethylglycine. Biopolymers 27, 373\u2013379 (1988).10.1002\/bip.360270303","journal-title":"Biopolymers"},{"key":"BFnchembio2206_CR26","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1038\/nature02611","volume":"430","author":"S Deechongkit","year":"2004","unstructured":"Deechongkit, S. et al. Context-dependent contributions of backbone hydrogen bonding to \u03b2-sheet folding energetics. Nature 430, 101\u2013105 (2004).","journal-title":"Nature"},{"key":"BFnchembio2206_CR27","doi-asserted-by":"publisher","first-page":"4228","DOI":"10.1021\/ja00063a046","volume":"115","author":"GP Dado","year":"1993","unstructured":"Dado, G.P. & Gellman, S.H. Structural and thermodynamic characterization of temperature-dependent changes in the folding pattern of a synthetic triamide. J. Am. Chem. Soc. 115, 4228\u20134245 (1993).10.1021\/ja00063a046","journal-title":"J. Am. Chem. Soc."},{"key":"BFnchembio2206_CR28","doi-asserted-by":"publisher","first-page":"996","DOI":"10.1002\/pro.2081","volume":"21","author":"JJ Skinner","year":"2012","unstructured":"Skinner, J.J., Lim, W.K., B\u00e9dard, S., Black, B.E. & Englander, S.W. Protein dynamics viewed by hydrogen exchange. Protein Sci. 21, 996\u20131005 (2012).10.1002\/pro.2081","journal-title":"Protein Sci."},{"key":"BFnchembio2206_CR29","doi-asserted-by":"publisher","first-page":"5578","DOI":"10.1073\/pnas.091100898","volume":"98","author":"AG Cochran","year":"2001","unstructured":"Cochran, A.G., Skelton, N.J. & Starovasnik, M.A. Tryptophan zippers: stable, monomeric \u03b2-hairpins. Proc. Natl. Acad. Sci. USA 98, 5578\u20135583 (2001).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"BFnchembio2206_CR30","doi-asserted-by":"publisher","first-page":"15948","DOI":"10.1021\/ja065303t","volume":"128","author":"Y Fu","year":"2006","unstructured":"Fu, Y., Gao, J., Bieschke, J., Dendle, M.A. & Kelly, J.W. Amide-to-E-olefin versus amide-to-ester backbone H-bond perturbations: evaluating the O-O repulsion for extracting H-bond energies. J. Am. Chem. Soc. 128, 15948\u201315949 (2006).","journal-title":"J. Am. Chem. Soc."},{"key":"BFnchembio2206_CR31","doi-asserted-by":"publisher","first-page":"248","DOI":"10.1006\/jmbi.1995.0492","volume":"252","author":"ZS Derewenda","year":"1995","unstructured":"Derewenda, Z.S., Lee, L. & Derewenda, U. The occurrence of C-H...O hydrogen bonds in proteins. J. Mol. Biol. 252, 248\u2013262 (1995).","journal-title":"J. Mol. Biol."},{"key":"BFnchembio2206_CR32","doi-asserted-by":"publisher","first-page":"8026","DOI":"10.1021\/ja301681v","volume":"134","author":"RM Culik","year":"2012","unstructured":"Culik, R.M., Jo, H., DeGrado, W.F. & Gai, F. Using thioamides to site-specifically interrogate the dynamics of hydrogen bond formation in \u03b2-sheet folding. J. Am. Chem. Soc. 134, 8026\u20138029 (2012).10.1021\/ja301681v","journal-title":"J. Am. Chem. Soc."},{"key":"BFnchembio2206_CR33","doi-asserted-by":"publisher","first-page":"9459","DOI":"10.1073\/pnas.96.17.9459","volume":"96","author":"JP Gallivan","year":"1999","unstructured":"Gallivan, J.P. & Dougherty, D.A. Cation-\u03c0 interactions in structural biology. Proc. Natl. Acad. Sci. USA 96, 9459\u20139464 (1999).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"BFnchembio2206_CR34","doi-asserted-by":"publisher","first-page":"1877","DOI":"10.1021\/cr040433a","volume":"106","author":"Z Shi","year":"2006","unstructured":"Shi, Z., Chen, K., Liu, Z. & Kallenbach, N.R. Conformation of the backbone in unfolded proteins. Chem. Rev. 106, 1877\u20131897 (2006).","journal-title":"Chem. Rev."},{"key":"BFnchembio2206_CR35","doi-asserted-by":"publisher","first-page":"2754","DOI":"10.1073\/pnas.052706099","volume":"99","author":"JS Richardson","year":"2002","unstructured":"Richardson, J.S. & Richardson, D.C. Natural \u03b2-sheet proteins use negative design to avoid edge-to-edge aggregation. Proc. Natl. Acad. Sci. USA 99, 2754\u20132759 (2002).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"BFnchembio2206_CR36","doi-asserted-by":"publisher","first-page":"5477","DOI":"10.1021\/ja3088407","volume":"135","author":"P-N Cheng","year":"2013","unstructured":"Cheng, P.-N., Pham, J.D. & Nowick, J.S. The supramolecular chemistry of \u03b2-sheets. J. Am. Chem. Soc. 135, 5477\u20135492 (2013).","journal-title":"J. Am. Chem. Soc."},{"key":"BFnchembio2206_CR37","doi-asserted-by":"publisher","first-page":"453","DOI":"10.1038\/nature05695","volume":"447","author":"MR Sawaya","year":"2007","unstructured":"Sawaya, M.R. et al. Atomic structures of amyloid cross-\u03b2 spines reveal varied steric zippers. Nature 447, 453\u2013457 (2007).","journal-title":"Nature"},{"key":"BFnchembio2206_CR38","doi-asserted-by":"publisher","first-page":"329","DOI":"10.1016\/S0968-0004(99)01445-0","volume":"24","author":"CM Dobson","year":"1999","unstructured":"Dobson, C.M. Protein misfolding, evolution and disease. Trends Biochem. Sci. 24, 329\u2013332 (1999).","journal-title":"Trends Biochem. Sci."},{"key":"BFnchembio2206_CR39","doi-asserted-by":"publisher","first-page":"16338","DOI":"10.1021\/ja066008b","volume":"128","author":"S Ohnishi","year":"2006","unstructured":"Ohnishi, S., Kamikubo, H., Onitsuka, M., Kataoka, M. & Shortle, D. Conformational preference of polyglycine in solution to elongated structure. J. Am. Chem. Soc. 128, 16338\u201316344 (2006).10.1021\/ja066008b","journal-title":"J. Am. Chem. Soc."},{"key":"BFnchembio2206_CR40","doi-asserted-by":"publisher","first-page":"660","DOI":"10.1038\/367660a0","volume":"367","author":"DL Minor Jr.","year":"1994","unstructured":"Minor, D.L. Jr. & Kim, P.S. Measurement of the \u03b2-sheet-forming propensities of amino acids. Nature 367, 660\u2013663 (1994).","journal-title":"Nature"},{"key":"BFnchembio2206_CR41","doi-asserted-by":"publisher","first-page":"1239","DOI":"10.1016\/S0022-2836(03)00021-4","volume":"326","author":"T Kortemme","year":"2003","unstructured":"Kortemme, T., Morozov, A.V. & Baker, D. An orientation-dependent hydrogen bonding potential improves prediction of specificity and structure for proteins and protein-protein complexes. J. Mol. Biol. 326, 1239\u20131259 (2003).","journal-title":"J. Mol. Biol."},{"key":"BFnchembio2206_CR42","doi-asserted-by":"publisher","first-page":"735","DOI":"10.1063\/1.449486","volume":"83","author":"AE Reed","year":"1985","unstructured":"Reed, A.E., Weinstock, R.B. & Weinhold, F. Natural population analysis. J. Chem. Phys. 83, 735\u2013746 (1985).","journal-title":"J. Chem. Phys."},{"key":"BFnchembio2206_CR43","doi-asserted-by":"publisher","first-page":"5661","DOI":"10.1021\/jp9014299","volume":"113","author":"R Huang","year":"2009","unstructured":"Huang, R. et al. Cross-strand coupling and site-specific unfolding thermodynamics of a trpzip \u03b2-hairpin peptide using 13C isotopic labeling and IR spectroscopy. J. Phys. Chem. B 113, 5661\u20135674 (2009).10.1021\/jp9014299","journal-title":"J. Phys. Chem. B"},{"key":"BFnchembio2206_CR44","doi-asserted-by":"publisher","first-page":"1589","DOI":"10.1093\/bioinformatics\/btg224","volume":"19","author":"G Wang","year":"2003","unstructured":"Wang, G. & Dunbrack, R.L. Jr. PISCES: a protein sequence culling server. Bioinformatics 19, 1589\u20131591 (2003).","journal-title":"Bioinformatics"},{"key":"BFnchembio2206_CR45","doi-asserted-by":"publisher","first-page":"212","DOI":"10.1002\/pro.5560050204","volume":"5","author":"EG Hutchinson","year":"1996","unstructured":"Hutchinson, E.G. & Thornton, J.M. PROMOTIF--a program to identify and analyze structural motifs in proteins. Protein Sci. 5, 212\u2013220 (1996).","journal-title":"Protein Sci."}],"container-title":["Nature Chemical Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/nchembio.2206.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/nchembio.2206","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/nchembio.2206.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,18]],"date-time":"2023-05-18T15:43:18Z","timestamp":1684424598000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/nchembio.2206"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,10,17]]},"references-count":45,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2016,12]]}},"alternative-id":["BFnchembio2206"],"URL":"https:\/\/doi.org\/10.1038\/nchembio.2206","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.726854992.793533972","asserted-by":"object"}]},"ISSN":["1552-4450","1552-4469"],"issn-type":[{"value":"1552-4450","type":"print"},{"value":"1552-4469","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,10,17]]},"assertion":[{"value":"12 May 2016","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 August 2016","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 October 2016","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}