A propensity scale for type II polyproline helices (PPII): Aromatic amino acids in proline-rich sequences strongly disfavor PPII due to proline-aromatic interactions

Biochemistry

Volumn 51, Issue 25, 2012, Pages 5041-5051

  Brown, Alaina M ^a   Zondlo, Neal J ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE BOND; AROMATIC AMINO ACID; AROMATIC RESIDUES; BRANCHED AMINO ACIDS; CELLULAR SIGNALING; CIS-TRANS ISOMERISM; HOST-GUEST SYSTEM; POLAR SIDE CHAINS; POLYPROLINE; PROTONATED; SECONDARY STRUCTURE OF PROTEINS; SIDE-CHAINS; TYPE II;

AMIDES; AROMATIC COMPOUNDS; AROMATIZATION; PROTEINS;

AMINO ACIDS;

AROMATIC AMINO ACID; PROLINE; PROTEIN;

AMINO ACID ANALYSIS; AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CHEMICAL BOND; CIS TRANS ISOMERISM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE;

AMINO ACID SEQUENCE; AMINO ACIDS, AROMATIC; ANIMALS; ARABIDOPSIS; CAENORHABDITIS ELEGANS; DROSOPHILA; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PEPTIDES; PROLINE; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STEREOISOMERISM;

EID: 84862835564     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3002924     Document Type: Article

References (119)

1. Adzhubei, A. A. and Sternberg, M. J. E. (1993) Left-Handed Polyproline-II Helices Commonly Occur in Globular-Proteins J. Mol. Biol. 229, 472-493 (Pubitemid 23080393)
2. Stapley, B. J. and Creamer, T. P. (1999) A survey of left-handed polyproline II helices Protein Sci. 8, 587-595 (Pubitemid 29117973)
3. Cubellis, M. V., Caillez, F., Blundell, T. L., and Lovell, S. C. (2005) Properties of polyproline II, a secondary structure element implicated in protein-protein interactions Proteins 58, 880-892 (Pubitemid 40271253)
4. Zarrinpar, A., Bhattacharyya, R. P., and Lim, W. A. (2003) The Structure and Function of Proline Recognition Domains Sci. STKE 2003, re8
5. Rubin, G. M., Yandell, M. D., Wortman, J. R., Miklos, G. L. G., Nelson, C. R., Hariharan, I. K., Fortini, M. E., Li, P. W., Apweiler, R., Fleischmann, W., Cherry, J. M., Henikoff, S., Skupski, M. P., Misra, S., Ashburner, M., Birney, E., Boguski, M. S., Brody, T., Brokstein, P., Celniker, S. E., Chervitz, S. A., Coates, D., Cravchik, A., Gabrielian, A., Galle, R. F., Gelbart, W. M., George, R. A., Goldstein, L. S. B., Gong, F. C., Guan, P., Harris, N. L., Hay, B. A., Hoskins, R. A., Li, J. Y., Li, Z. Y., Hynes, R. O., Jones, S. J. M., Kuehl, P. M., Lemaitre, B., Littleton, J. T., Morrison, D. K., Mungall, C., O'Farrell, P. H., Pickeral, O. K., Shue, C., Vosshall, L. B., Zhang, J., Zhao, Q., Zheng, X. Q. H., Zhong, F., Zhong, W. Y., Gibbs, R., Venter, J. C., Adams, M. D., and Lewis, S. (2000) Comparative Genomics of the Eukaryotes Science 287, 2204-2215 (Pubitemid 30177015)
6. Wright, P. E. and Dyson, H. J. (1999) Intrinsically Unstructured Proteins: Re-assessing the Protein Structure-Function Paradigm J. Mol. Biol. 293, 321-331 (Pubitemid 29516173)
7. Dunker, A. K., Brown, C. J., and Obradovic, Z. (2002) Identification and functions of usefully disordered proteins Adv. Protein Chem. 62, 25-49 (Pubitemid 35204867)
8. Dunker, A. K., Brown, C. J., Lawson, J. D., Iakoucheva, L. M., and Obradovic, Z. (2002) Intrinsic disorder and protein function Biochemistry 41, 6573-6582 (Pubitemid 34547347)
9. Uversky, V. N., Oldfield, C. J., and Dunker, A. K. (2005) Showing your ID: Intrinsic disorder as an ID for recognition, regulation and cell signaling J. Mol. Recognit. 18, 343-384 (Pubitemid 41341287)
10. Rath, A., Davidson, A. R., and Deber, C. M. (2005) The structure of "unstructured" regions in peptides and proteins: Role of the polyproline II helix in protein folding and recognition Biopolymers 80, 179-185 (Pubitemid 40791050)
11. Shi, Z. S., Woody, R. W., and Kallenbach, N. R. (2002) Is polyproline II a major backbone conformation in unfolded proteins? Adv. Protein Chem. 62, 163-240 (Pubitemid 35204871)
12. Mezei, M., Fleming, P. J., Srinivasan, R., and Rose, G. D. (2004) Polyproline II helix is the preferred conformation for unfolded polyalanine in water Proteins 55, 502-507 (Pubitemid 38620075)
13. Grdadolnik, J., Mohacek-Grosev, V., Baldwin, R. L., and Avbelj, F. (2011) Populations of the three major backbone conformations in 19 amino acid dipeptides Proc. Natl. Acad. Sci. U.S.A. 108, 1794-1798
14. Shi, Z. S., Olson, C. A., Rose, G. D., Baldwin, R. L., and Kallenbach, N. R. (2002) Polyproline II structure in a sequence of seven alanine residues Proc. Natl. Acad. Sci. U.S.A. 99, 9190-9195 (Pubitemid 34764589)
15. Ding, L., Chen, K., Santini, P. A., Shi, Z., and Kallenbach, N. R. (2003) The Pentapeptide GGAGG Has PII Conformation J. Am. Chem. Soc. 125, 8092-8093 (Pubitemid 36828561)
16. Chen, K., Liu, Z. G., and Kallenbach, N. R. (2004) The polyproline II conformation in short alanine peptides is noncooperative Proc. Natl. Acad. Sci. U.S.A. 101, 15352-15357 (Pubitemid 39441545)
17. Ramakrishnan, V., Ranbhor, R., and Durani, S. (2004) Existence of specific "folds" in polyproline II ensembles of an "unfolded" alanine peptide detected by molecular dynamics J. Am. Chem. Soc. 126, 16332-16333 (Pubitemid 40081925)
18. Gokce, I., Woody, R. W., Anderluh, G., and Lakey, J. H. (2005) Single peptide bonds exhibit poly(pro)II ("random coil") circular dichroism spectra J. Am. Chem. Soc. 127, 9700-9701 (Pubitemid 40981530)
19. Eker, F., Griebenow, K., Cao, X. L., Nafie, L. A., and Schweitzer-Stenner, R. (2004) Preferred peptide backbone conformations in the unfolded state revealed by the structure analysis of alanine-based (AXA) tripeptides in aqueous solution Proc. Natl. Acad. Sci. U.S.A. 101, 10054-10059 (Pubitemid 38891193)
20. Hagarman, A., Measey, T. J., Mathieu, D., Schwalbe, H., and Schweitzer-Stenner, R. (2010) Intrinsic Propensities of Amino Acid Residues in GxG Peptides Inferred from Amide I′ Band Profiles and NMR Scalar Coupling Constants J. Am. Chem. Soc. 132, 540-551
21. Neidigh, J. W., Fesinmeyer, R. M., and Andersen, N. H. (2002) Designing a 20-residue protein Nat. Struct. Biol. 9, 425-430 (Pubitemid 34568786)
22. Zondlo, N. J. and Schepartz, A. (1999) Highly specific DNA recognition by a designed miniature protein J. Am. Chem. Soc. 121, 6938-6939 (Pubitemid 29374495)
23. Arora, P. S., Ansari, A. Z., Best, T. P., Ptashne, M., and Dervan, P. B. (2002) Design of Artificial Transcriptional Activators with Rigid Poly- l -proline Linkers J. Am. Chem. Soc. 124, 13067-13071 (Pubitemid 35247118)
24. Tremmel, P. and Geyer, A. (2002) An Oligomeric Ser-Pro Dipeptide Mimetic Assuming the Polyproline II Helix Conformation J. Am. Chem. Soc. 124, 8548-8549 (Pubitemid 34791022)
25. Golemi-Kotra, D., Mahaffty, R., Footer, M. J., Holtzman, J. H., Pollard, T. D., Theriot, J. A., and Schepartz, A. (2004) High Affinity, Paralog-Specific Recognition of the Mena EVH1 Domain by a Miniature Protein J. Am. Chem. Soc. 126, 4-5 (Pubitemid 38090312)
26. Daniels, D. S. and Schepartz, A. (2007) Intrinsically cell-permeable miniature proteins based on a minimal cationic PPII motif J. Am. Chem. Soc. 129, 14578-14579 (Pubitemid 350207870)
27. Schimmel, P. R. and Flory, P. J. (1967) Conformational Energy and Configurational Statistics of Poly- l -Proline Proc. Natl. Acad. Sci. U.S.A. 58, 52-59
28. Schimmel, P. R. and Flory, P. J. (1968) Confromational energies and configurational statistics of copolypeptides containing l -proline J. Mol. Biol. 34, 105-120
29. Crespo, L., Sanclimens, G., Montaner, B., Pérez-Tomás, R., Royo, M., Pons, M., Albericio, F., and Giralt, E. (2002) Peptide Dendrimers Based on Polyproline Helices J. Am. Chem. Soc. 124, 8876-8883 (Pubitemid 34809633)
30. Schuler, B., Lipman, E. A., Steinbach, P. J., Kumke, M., and Eaton, W. A. (2005) Polyproline and the "spectroscopic ruler" revisited with single-molecule fluorescence Proc. Natl. Acad. Sci. U.S.A. 102, 2754-2759 (Pubitemid 40299865)
31. Fillon, Y. A., Anderson, J. P., and Chmielewski, J. (2005) Cell penetrating agents based on a polyproline helix scaffold J. Am. Chem. Soc. 127, 11798-11803 (Pubitemid 41208765)
32. Kumin, M., Sonntag, L. S., and Wennemers, H. (2007) Azidoproline containing helices: Stabilization of the polyproline II structure by a functionalizable group J. Am. Chem. Soc. 129, 466-467 (Pubitemid 46147728)
33. Erdmann, R. S. and Wennemers, H. (2010) Functionalizable Collagen Model Peptides J. Am. Chem. Soc. 132, 13957-13959
34. Owens, N. W., Stetefeld, J., Lattova, E., and Schweizer, F. (2010) Contiguous O-Galactosylation of 4(R)-Hydroxy- l -proline Residues Forms Very Stable Polyproline II Helices J. Am. Chem. Soc. 132, 5036-5042
35. Stryer, L. and Haugland, R. P. (1967) Energy transfer: A spectroscopic ruler Proc. Natl. Acad. Sci. U.S.A. 58, 719-726
36. Sahoo, H., Roccatano, D., Hennig, A., and Nau, W. M. (2007) A 10-Å Spectroscopic Ruler Applied to Short Polyprolines J. Am. Chem. Soc. 129, 9762-9772 (Pubitemid 47237490)
37. Best, R. B., Merchant, K. A., Gopich, I. V., Schuler, B., Bax, A., and Eaton, W. A. (2007) Effect of flexibility and cis residues in single-molecule FRET studies of polyproline Proc. Natl. Acad. Sci. U.S.A. 104, 18964-18969
38. Durocher, D., Taylor, I. A., Sarbassova, D., Haire, L. F., Westcott, S. L., Jackson, S. P., Smerdon, S. J., and Yaffe, M. B. (2000) The molecular basis of FHA domain: Phosphopeptide binding specificity and implications for phospho-dependent signaling mechanisms Mol. Cell 6, 1169-1182
39. Creamer, T. P. (1998) Left-handed polyproline II helix formation is (very) locally driven Proteins 33, 218-226 (Pubitemid 28457974)
40. Persikov, A. V., Ramshaw, J. A. M., Kirkpatrick, A., and Brodsky, B. (2000) Amino acid propensities for the collagen triple-helix Biochemistry 39, 14960-14967
41. Kelly, M. A., Chellgren, B. W., Rucker, A. L., Troutman, J. M., Fried, M. G., Miller, A. F., and Creamer, T. P. (2001) Host-guest study of left-handed polyproline II helix formation Biochemistry 40, 14376-14383 (Pubitemid 33111719)
42. Rucker, A. L., Pager, C. T., Campbell, M. N., Qualls, J. E., and Creamer, T. P. (2003) Host-Guest Scale of Left-Handed Polyproline II Helix Formation Proteins 53, 68-75 (Pubitemid 37059545)
43. Vila, J. A., Baldoni, H. A., Ripolli, D. R., Ghosh, A., and Scheraga, H. A. (2004) Polyproline II Helix Conformation in a Proline-Rich Environment: A Theoretical Study Biophys. J. 86, 731-742 (Pubitemid 38209521)
44. Jha, A. K., Colubri, A., Zaman, M. H., Koide, S., Sosnick, T. R., and Freed, K. F. (2005) Helix, sheet, and polyproline II frequencies and strong nearest neighbor effects in a restricted coil library Biochemistry 44, 9691-9702 (Pubitemid 40994363)
45. Chen, K., Liu, Z. G., Zhou, C. H., Shi, Z. S., and Kallenbach, N. R. (2005) Neighbor effect on PPII conformation in alanine peptides J. Am. Chem. Soc. 127, 10146-10147 (Pubitemid 41045462)
46. Shi, Z., Chen, K., Liu, Z., Ng, A., Bracken, W. C., and Kallenbach, N. R. (2005) Polyproline II propensities from GGXGG peptides reveal an anticorrelation with β-sheet scales Proc. Natl. Acad. Sci. U.S.A. 102, 17964-17968 (Pubitemid 41798485)
47. Woody, R. W. (1994) Contributions of Tryptophan Side-chains to the Far-Ultraviolet Circular-Dichroism of Proteins Eur. Biophys. J. 23, 253-262 (Pubitemid 24331689)
48. Sreerama, N., Manning, M. C., Powers, M. E., Zhang, J. X., Goldenberg, D. P., and Woody, R. W. (1999) Tyrosine, phenylalanine, and disulfide contributions to the circular dichroism of proteins: Circular dichroism spectra of wild-type and mutant bovine pancreatic trypsin inhibitor Biochemistry 38, 10814-10822
49. Manning, M. C. and Woody, R. W. (1989) Theoretical study of the contribution of aromatic side chains to the circular dichroism of basic bovine pancreatic trypsin inhibitor Biochemistry 28, 8609-8613 (Pubitemid 19269056)
50. Helbecque, N. and Loucheux-Lefebvre, M. H. (1982) Critical chain length for polyproline-II structure formation in H-Gly-(Pro)n-OH Int. J. Pept. Protein Res. 19, 94-101
51. Saha, I. and Shamala, N. (2012) Investigating Diproline Segments in Proteins: Occurrences, Conformation and Classification Biopolymers 97, 54-64
52. Sreerama, N. and Woody, R. W. (1994) Poly(Pro)II Helices in Globular Proteins: Identification and Circular Dichroic Anaysis Biochemistry 33, 10022-10025 (Pubitemid 24286080)
53. Woody, R. W. (2009) Circular Dichroism Spectrum of Peptides in the Poly(Pro)II Conformation J. Am. Chem. Soc. 131, 8234-8245
54. Whittington, S. J. and Creamer, T. P. (2003) Salt bridges do not stabilize polyproline II helices Biochemistry 42, 14690-14695 (Pubitemid 37532016)
55. 2O on polyproline II helical structure J. Am. Chem. Soc. 126, 14734-14735 (Pubitemid 39532150)
56. Whittington, S. J., Chellgren, B. W., Hermann, V. M., and Creamer, T. P. (2005) Urea promotes polyproline II helix formation: Implications for protein denatured states Biochemistry 44, 6269-6275 (Pubitemid 40570720)
57. Wallimann, P., Kennedy, R. J., Miller, J. S., Shalongo, W., and Kemp, D. S. (2003) Dual Wavelength Parametric Test of Two-State Models for Circular Dichroism Spectra of Helical Peptides: Anomalous Dichroic Properties of Alanine-Rich Peptides J. Am. Chem. Soc. 125, 1203-1220 (Pubitemid 36159832)
58. 15N-enriched Proteins J. Am. Chem. Soc. 115, 7772-7777
59. Manning, M. C. and Woody, R. W. (1991) Theoretical CD Studies of Polypeptide Helices: Examination of Important Electronic and Geometric Factors Biopolymers 31, 569-586
60. Creamer, T. P. and Campbell, M. N. (2002) Determinants of the polyproline II helix from modeling studies Adv. Protein Chem. 62, 263-282 (Pubitemid 35204873)
61. Lyu, P. C., Sherman, J. C., Chen, A., and Kallenbach, N. R. (1991) α-Helix Stabilization by Natural and Unnatural Amino-Acids with Alkyl Side-Chains Proc. Natl. Acad. Sci. U.S.A. 88, 5317-5320 (Pubitemid 21914735)
62. Cornish, V. W., Kaplan, M. I., Veenstra, D. L., Kollman, P. A., and Schultz, P. G. (1994) Stabilizing and Destabilizing Effects of Placing β-Branched Amino Acids in Protein α-Helices Biochemistry 33, 12022-12031 (Pubitemid 24328016)
63. Mendel, D., Ellman, J. A., Chang, Z., Veenstra, D. L., Kollman, P. A., and Schultz, P. G. (1992) Probing Protein Stability with Unnatural Amino Acids Science 256, 1798-1802
64. Bielska, A. A. and Zondlo, N. J. (2006) Hyperphosphorylation of tau induces local polyproline II helix Biochemistry 45, 5527-5537 (Pubitemid 43673183)
65. Hagarman, A., Mathieu, D., Toal, S., Measey, T. J., Schwalbe, H., and Schweitzer-Stenner, R. (2011) Amino Acids with Hydrogen-Bonding Side Chains have an Intrinsic Tendency to Sample Various Turn Conformations in Aqueous Solution Chem.-Eur. J. 17, 6789-6797
66. Creamer, T. P. and Rose, G. D. (1992) Side-Chain Entropy Opposes α-Helix Formation but Rationalizes Experimentally Determined Helix-Forming Propensities Proc. Natl. Acad. Sci. U.S.A. 89, 5937-5941
67. Chellgren, B. W. and Creamer, T. P. (2006) Side-Chain Entropy Effects on Protein Secondary Structure Formation Proteins 62, 411-420 (Pubitemid 43054361)
68. Vijayakumar, M., Qian, H., and Zhou, H. X. (1999) Hydrogen bonds between short polar side chains and peptide backbone: Prevalence in proteins and effects on helix-forming propensities Proteins 34, 497-507 (Pubitemid 29129700)
69. Eswar, N. and Ramakrishnan, C. (2000) Deterministic features of side-chain main-chain hydrogen bonds in globular protein structures Protein Eng. 13, 227-238 (Pubitemid 30258956)
70. Gronert, S. and O'Hair, R. A. J. (1995) Ab Initio Studies of Amino Acid Conformations. 1. The Conformers of Alanine, Serine, and Cysteine J. Am. Chem. Soc. 117, 2071-2081
71. Iakoucheva, L. M., Radivojac, P., Brown, C. J., O'Connor, T. R., Sikes, J. G., Obradovic, Z., and Dunker, A. K. (2004) The importance of intrinsic disorder for protein phosphorylation Nucleic Acids Res. 32, 1037-1049 (Pubitemid 38854704)
72. Dyson, H. J., Rance, M., Houghten, R. A., Lerner, R. A., and Wright, P. E. (1988) Folding of Immunogenic Peptide-Fragments of Proteins in Water Solution. 1. Sequence Requirements for the Formation of a Reverse Turn J. Mol. Biol. 201, 161-200
73. Yao, J., Dyson, H. J., and Wright, P. E. (1994) 3-Dimensional Structure of a Type-VI turn in a Linear Peptide in Water Solution: Evidence for Stacking of Aromatic Rings as a Major Stabilizing Factor J. Mol. Biol. 243, 754-766
74. Yao, J., Feher, V. A., Espejo, B. F., Reymond, M. T., Wright, P. E., and Dyson, H. J. (1994) Stabilization of a Type-VI Turn in a Family of Linear Peptides in Water Solution J. Mol. Biol. 243, 736-753 (Pubitemid 24341715)
75. Kemmink, J. and Creighton, T. E. (1995) The Physical Properties of Local Interactions of Tyrosine Residues in Peptides and Unfolded Proteins J. Mol. Biol. 245, 251-260
76. Reimer, U., Scherer, G., Drewello, M., Kruber, S., Schutkowski, M., and Fischer, G. (1998) Side-chain effects on peptidyl-prolyl cis/trans isomerization J. Mol. Biol. 279, 449-460 (Pubitemid 28263982)
77. Wu, W.-J. and Raleigh, D. P. (1998) Local Control of Peptide Conformation: Stabilization of cis Proline Peptide Bonds by Aromatic Proline Interactions Biopolymers 45, 381-394
78. i +2 Amide Bond: Implications for Type VI β-turn Formation Biopolymers 84, 192-204
79. Thomas, K. M., Naduthambi, D., and Zondlo, N. J. (2006) Electronic control of amide cis-trans isomerism via the aromatic-prolyl interaction J. Am. Chem. Soc. 128, 2216-2217
80. Forbes, C. R. and Zondlo, N. J. (2012) Synthesis of Thiophenylalanine- Containing Peptides via Cu(I)-mediated Cross-Coupling Org. Lett. 14, 464-467
81. Nardi, F., Kemmink, J., Sattler, M., and Wade, R. C. (2000) The cisproline(i-1)-aromatic(i) interaction: Folding of the Ala-cisPro-Tyr peptide characterized by NMR and theoretical approaches J. Biomol. NMR 17, 63-77 (Pubitemid 30434839)
82. Toth, G., Murphy, R. F., and Lovas, S. (2001) Stabilization of local structures by π-CH and aromatic-backbone amide interactions involving prolyl and aromatic residues Protein Eng. 14, 543-547 (Pubitemid 32959478)
83. n-Tyr-OH peptides Biopolymers 33, 781-795 (Pubitemid 23141419)
84. Stewart, D. E., Sarkar, A., and Wampler, J. E. (1990) Occurrence and role of cis peptide-bonds in protein structures J. Mol. Biol. 214, 253-260 (Pubitemid 20231222)
85. Wu, C. H., Huang, H., Arminski, L., Castro-Alvear, J., Chen, Y., Hu, Z.-Z., Ledley, R. S., Lewis, K. C., Mewes, H.-W., Orcutt, B. C., Suzek, B. E., Tsugita, A., Vinayaka, C. R., Yeh, L.-S. L., Zhang, J., and Barker, W. C. (2002) The Protein Information Resource: An integrated public resource of functional annotation of proteins Nucleic Acids Res. 30, 35-37 (Pubitemid 34679497)
86. Echols, N., Harrison, P., Balasubramanian, S., Luscombe, N. M., Bertone, P., Zhang, Z., and Gerstein, M. (2002) Comprehensive analysis of amino acid and nucleotide composition of eukaryotic genomes, comparing genes and pseudogenes Nucleic Acids Res. 30, 2515-2523 (Pubitemid 34619005)
87. http://pir.georgetown.edu/.
88. Dasgupta, B., Chakrabarti, P., and Basu, G. (2007) Enhanced stability of cis Pro-Pro peptide bond in Pro-Pro-Phe sequence motif FEBS Lett. 581, 4529-4532 (Pubitemid 47376697)
89. Wright, P. E., Dyson, H. J., and Lerner, R. A. (1988) Conformation of Peptide-Fragments of Proteins in Aqueous-Solution: Implications for Initiation of Protein Folding Biochemistry 27, 7167-7175
90. Pal, D. and Chakrabarti, P. (1999) Cis Peptide Bonds in Proteins: Residues Involved, Their Conformations, Interactions and Locations J. Mol. Biol. 294, 271-288
91. Halab, L. and Lubell, W. D. (2002) Effect of sequence on peptide geometry in 5-tert-butylprolyl type VI β-turn mimics J. Am. Chem. Soc. 124, 2474-2484 (Pubitemid 34251761)
92. Thomas, K. M., Naduthambi, D., Tririya, G., and Zondlo, N. J. (2005) Proline Editing: A Divergent Strategy for the Synthesis of Conformationally Diverse Peptides Org. Lett. 7, 2397-2400 (Pubitemid 40847645)
93. Ting, D., Wang, G., Shapovalov, M., Mitra, R., Jordan, M. I., and Dunbrack, R. L. (2010) Neighbor-Dependent Ramachandran Probability Distributions of Amino Acids Developed from a Hierarchical Dirichlet Process Model PLoS Comput. Biol. 6 e1000763
94. Bretscher, L. E., Jenkins, C. L., Taylor, K. M., DeRider, M. L., and Raines, R. T. (2001) Conformational Stability of Collagen Relies on a Stereoelectronic Effect J. Am. Chem. Soc. 123, 777-778 (Pubitemid 32106035)
95. Hinderaker, M. P. and Raines, R. T. (2003) An electronic effect on protein structure Protein Sci. 12, 1188-1194 (Pubitemid 36597505)
96. Hodges, J. A. and Raines, R. T. (2006) Energetics of an n → π* interaction that impacts protein structure Org. Lett. 8, 4695-4697 (Pubitemid 44629438)
97. Horng, J. C. and Raines, R. T. (2006) Stereoelectronic effects on polyproline conformation Protein Sci. 15, 74-83 (Pubitemid 43004235)
98. Bartlett, G. J., Choudhary, A., Raines, R. T., and Woolfson, D. N. (2010) n → π* interactions in proteins Nat. Chem. Biol. 6, 615-620
99. Zondlo, N. J. (2010) Fold Globally, Bond Locally Nat. Chem. Biol. 6, 567-568
100. Lovell, S. C., Word, J. M., Richardson, J. S., and Richardson, D. C. (2000) The Penultimate Rotamer Library Proteins 40, 389-408 (Pubitemid 30624447)
101. Bienkiewicz, E. A., Moon Woody, A.-Y., and Woody, R. W. (2000) Conformation of the RNA Polymerase II C-Terminal Domain: Circular Dichroism of Long and Short Fragments J. Mol. Biol. 297, 119-133
102. Verdecia, M. A., Bowman, M. E., Lu, K. P., Hunter, T., and Noel, J. P. (2000) Structural basis for phosphoserine-proline recognition by group IV WW domains Nat. Struct. Biol. 7, 639-643 (Pubitemid 30636673)
103. Yaffe, M. B. and Eila, A. E. H. (2001) Phosphoserine/threonine-binding domains Curr. Opin. Cell Biol. 13, 131-138 (Pubitemid 32209212)
104. Manke, I. A., Lowery, D. M., Nguyen, A., and Yaffe, M. B. (2003) BRCT repeats as phosphopeptide-binding modules involved in protein targeting Science 302, 636-639 (Pubitemid 37310918)
105. Pe'er, I., Felder, C. E., Man, O., Silman, I., Sussman, J. L., and Beckmann, J. S. (2004) Proteomic Signatures: Amino Acid and Oligopeptide Compositions Differ Among Phyla Proteins 54, 20-40 (Pubitemid 38036912)
106. Jenkins, C. L. and Raines, R. T. (2002) Insights on the conformational stability of collagen Nat. Prod. Rep. 19, 49-59 (Pubitemid 34140332)
107. Kraulis, P. J. (1991) MOLSCRIPT: A Program to Produce Both Detailed and Schematic Plots of Protein Structures J. Appl. Crystallogr. 24, 946-950
108. Wu, Y. H., Ko, T. P., Guo, S. M., Hu, S. M., Chuang, L. M., and Wang, A. H. J. (2008) Structural Basis for Catalytic and Inhibitory Mechanisms of Human Prostaglandin Reductase PTGR2 Structure 16, 1714-1723
109. Iwasaki, W., Miyatake, H., and Miki, K. (2005) Crystal Structure of the Small Form of Glucose-Inhibited Divisional Protein A from Thermus thermophilus HB8 Proteins 61, 1121-1126 (Pubitemid 41753182)
110. Kemmink, J. and Creighton, T. E. (1993) Local Conformations of Peptides Representing the Entire Sequence of Bovine Pancreatic Trypsin Inhibitor and Their Roles in Folding J. Mol. Biol. 234, 861-878 (Pubitemid 24007806)
111. n-Tyr Biopolymers 16, 277-288 (Pubitemid 8046954)
112. Wierzchowski, K. L., Majcher, K., and Poznanski, J. (1995) CD Investigations on Conformation of H-X-(Pro)(N)-Y-OH Peptides (X = Trp, Tyr, Y = Tyr, Met) Models for Intramolecular Long-Range Energy-Transfer Acta Biochim. Pol. 42, 259-268
113. n-Tyr-OH, n = 3-5, Series of Peptides J. Phys. Chem. B 103, 10316-10324 (Pubitemid 129614085)
114. Doose, S., Neuweiler, H., Barsch, H., and Sauer, M. (2007) Probing polyproline structure and dynamics by photoinduced electron transfer provides evidence for deviations from a regular polyproline type II helix Proc. Natl. Acad. Sci. U.S.A. 104, 17400-17405 (Pubitemid 350219850)
115. Li, S. S. C. (2005) Specificity and versatility of SH3 and other proline-recognition domains: Structural basis and implications for cellular signal transduction Biochem. J. 390, 641-653
116. Koide, S. and Sidhu, S. S. (2009) The Importance of Being Tyrosine: Lessons in Molecular Recognition from Minimalist Synthetic Binding Proteins ACS Chem. Biol. 4, 325-334
117. Meyer, E. A., Castellano, R. K., and Diederich, F. (2003) Interactions with Aromatic Rings in Chemical and Biological Recognition Angew. Chem., Int. Ed. 42, 1210-1250 (Pubitemid 36410287)
118. Salonen, L. M., Ellermann, M., and Diederich, F. (2011) Aromatic Rings in Chemical and Biological Recognition: Energetics and Structures Angew. Chem., Int. Ed. 50, 4808-4842
119. Chen, J. K., Lane, W. S., Brauer, A. W., Tanaka, A., and Schreiber, S. L. (1993) Biased Combinatorial Libraries: Novel Ligands for the SH3 Domain of Phosphatidylinositol 3-Kinase J. Am. Chem. Soc. 115, 12591-12592 (Pubitemid 24078366)