Rational design strategies for developing synthetic inhibitors of helical protein interfaces

Topics in Medicinal Chemistry

Volumn 8, Issue , 2012, Pages 197-230

  Mahon, Andrew B ^a   Miller, Stephen E ^a   Joy, Stephen T ^a   Arora, Paramjit S ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

Helix mimetics; Inhibitors; Protein protein interactions

Indexed keywords

A 385358; CARBOHYDRATE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; DNA; ENFUVIRTIDE; HUMAN IMMUNODEFICIENCY VIRUS FUSION INHIBITOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NOTCH RECEPTOR; PEPTOID; PROTEIN BAD; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN BID; PROTEIN INHIBITOR; PROTEIN MDM2; PROTEIN P300; PROTEIN P53; RAS PROTEIN; RNA; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; COMPLEX FORMATION; DRUG DESIGN; HYDROGEN BOND; IN VITRO STUDY; INHIBITION KINETICS; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

EID: 84864049238     PISSN: 18622461     EISSN: 1862247X     Source Type: Book Series    
DOI: 10.1007/978-3-642-28965-1_6     Document Type: Article

References (157)

1. Ryan DP, Matthews JM (2005) Protein-protein interactions in human disease. Curr Opin Struct Biol 15:441-446
2. Arkin MR, Wells JA (2004) Small-molecule inhibitors of protein-protein interactions: progressing towards the dream. Nat Rev Drug Discov 3:301-317
3. Hajduk PJ, Greer J (2007) A decade of fragment-based drug design: strategic advances and lessons learned. Nat Rev Drug Discov 6:211-219
4. Lo Conte L, Chothia C, Janin J (1999) The atomic structure of protein-protein recognition sites. J Mol Biol 285:2177-2198
5. Overington JP, Al-Lazikani B, Hopkins AL (2006) How many drug targets are there? Nat Rev Drug Discov 5:993-996
6. Vitkup D, Melamud E, Moult J, Sander C (2001) Completeness in structural genomics. Nat Struct Biol 8:559-566
7. Vassilev L, Fry D (eds) (2011) Small molecule inhibitors of protein-protein interactions, vol 348, Current topics in microbiology and immunology. Springer, Heidelberg/Dordecht/ London/New York
8. Berg T (2008) Inhibition of transcription factors with small organic molecules. Curr Opin Chem Biol 12:464-471
9. Shangary S, Wang S (2008) Targeting the MDM2-p53 interaction for cancer therapy. Clin Cancer Res 14:5318-5324
10. Vassilev LT, Vu BT, Graves B et al (2004) In vivo activation of the p53 pathway by smallmolecule antagonists of MDM2. Science 303:844-848
11. Chene P (2003) Inhibiting the p53-MDM2 interaction: an important target for cancer therapy. Nat Rev Cancer 3:102-109
12. Kussie PH, Gorina S, Marechal V et al (1996) Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science 274:948-953
13. Oltersdorf T, Elmore SW, Shoemaker AR et al (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435:677-681
14. Sattler M, Liang H, Nettesheim D et al (1997) Structure of Bcl-x(L)-Bak peptide complex: recognition between regulators of apoptosis. Science 275:983-986
15. Shoemaker AR, Oleksijew A, Bauch J et al (2006) A small-molecule inhibitor of Bcl-XL potentiates the activity of cytotoxic drugs in vitro and in vivo. Cancer Res 66:8731-8739
16. Wendt MD, Shen W, Kunzer A et al (2006) Discovery and structure-activity relationship of antagonists of B-cell lymphoma 2 family proteins with chemopotentiation activity in vitro and in vivo. J Med Chem 49:1165-1181
17. Wang Y, Coulombe R, Cameron DR et al (2004) Crystal structure of the E2 transactivation domain of human papillomavirus type 11 bound to a protein interaction inhibitor. J Biol Chem 279:6976-6985
18. Cheng RP, DeGrado WF (2001) De novo design of a monomeric helical beta-peptide stabilized by electrostatic interactions. J Am Chem Soc 123:5162-5163
19. Liu Z, Sun C, Olejniczak ET et al (2000) Structural basis for binding of Smac/DIABLO to the XIAP BIR3 domain. Nature 408:1004-1008
20. Oost TK, Sun C, Armstrong RC et al (2004) Discovery of potent antagonists of the antiapoptotic protein XIAP for the treatment of cancer. J Med Chem 47:4417-4426
21. Sun H, Nikolovska-Coleska Z, Yang C-Y et al (2004) Structure-based design of potent, conformationally constrained Smac mimetics. J Am Chem Soc 126:16686-16687
22. Glattli A, Daura X, Bindschadler P et al (2005) On the influence of charged side chains on the folding-unfolding equilibrium of beta-peptides: a molecular dynamics simulation study. Chemistry 11:7276-7293
23. Berg T, Cohen SB, Desharnais J et al (2002) Small-molecule antagonists of Myc/Max dimerization inhibit Myc-induced transformation of chicken embryo fibroblasts. Proc Natl Acad Sci USA 99:3830-3835
24. Kiessling A, Sperl B, Hollis A et al (2006) Selective inhibition of c-Myc/Max dimerization and DNA binding by small molecules. Chem Biol 13:745-751
25. Bogan AA, Thorn KS (1998) Anatomy of hot spots in protein interfaces. J Mol Biol 280:1-9
26. Moreira IS, Fernandes PA, Ramos MJ (2007) Hot spots-a review of the protein-protein interface determinant amino-acid residues. Proteins 68:803-812
27. Clackson T, Wells JA (1995) A hot-spot of binding-energy in a hormone-receptor interface. Science 267:383-386
28. Keskin Z, Gursoy A, Ma B, Nussinov R (2008) Principles of protein-protein interactions: what are the preferred ways for proteins to interact? Chem Rev 108:1225-1244
29. Guharoy M, Chakrabarti P (2007) Secondary structure based analysis and classification of biological interfaces: identification of binding motifs in protein-protein interactions. Bioinformatics 23:1909-1918
30. Jones S, Thornton JM (1995) Protein-protein interactions - a review of protein dimer structures. Prog Biophys Mol Biol 63:31-65
31. Goodman CM, Choi S, Shandler S, DeGrado WF (2007) Foldamers as versatile frameworks for the design and evolution of function. Nat Chem Biol 3:252-262
32. Horne WS, Johnson LM, Ketas TJ et al (2009) Structural and biological mimicry of protein surface recognition by a/b-peptide foldamers. Proc Natl Acad Sci USA 106:14751-14756
33. Henchey LK, Porter JR, Ghosh I, Arora PS (2010) High specificity in protein recognition by hydrogen-bond-surrogate a-helices: selective inhibition of the p53/MDM2 complex. Chembiochem 11:2104-2107
34. Ko E, Liu J, Burgess K (2011) Minimalist and universal peptidomimetics. Chem Soc Rev 40:4411-4421
35. Wang D, Lu M, Arora PS (2008) Inhibition of HIV-1 fusion by hydrogen-bond-surrogatebased a helices. Angew Chem Int Ed 47:1879-1882
36. Moellering RE, Cornejo M, Davis TN et al (2009) Direct inhibition of NOTCH transcription factor complex. Nature 462:182-190
37. Walensky LD, Kung AL, Escher I et al (2004) Activation of apoptosis in vivo by a hydrocarbon-stabled BH3 helix. Science 305:1466-1470
38. Harrison RS, Shepherd NE, Hoang HN et al (2010) Downsizing human, bacterial, and viral proteins to short water-stable a helices that maintain biological potency. Proc Natl Acad Sci USA 107:11686-11691
39. Smith BA, Daniels DS, Coplin AE et al (2008) Minimally cationic cell-permeable miniature proteins via a-helical arginine display. J Am Chem Soc 130:2948-2949
40. Harker EA, Schepartz A (2009) Cell-permeable b-peptide inhibitors of p53/hDM2 complexation. Chembiochem 10:990-993
41. Cummings CG, Hamilton AD (2010) Disrupting protein-protein interactions with nonpeptidic, small molecule a-helix mimetics. Curr Opin Chem Biol 14:341-346
42. Hammond MC, Harris BZ, Lim WA, Bartlett PA (2006) b strand peptidomimetics as potent PDZ domain ligands. Chem Biol 13:1247-1251
43. Bourgeas R, Basse MJ, Morelli X, Roche P (2010) Atomic analysis of protein-protein interfaces with known inhibitors: the 2P2I database. PLoS One 5:e9598
44. Davis JM, Tsou LK, Hamilton AD (2007) Synthetic non-peptide mimetics of a-helices. Chem Soc Rev 36:326-334
45. Duca M, Vekhoff P, Oussedik K et al (2008) The triple helix: 50 years later, the outcome. Nucleic Acids Res 36:5123-5138
46. Higueruelo AP, Schreyer A, Bickerton GR et al (2009) Atomic interactions and profile of small molecules disrupting protein-protein interfaces: the TIMBAL database. Chem Biol Drug Des 74:457-467
47. Jamieson AC, Miller JC, Pabo CO (2003) Drug discovery with engineered zinc-finger proteins. Nat Rev Drug Discov 2:361-368
48. Ray A, Norden B (2000) Peptide nucleic acid (PNA): its medical and biotechnical applications and promise for the future. FASEB J 14:1041-1060
49. Reynes C, Host H, Camproux AC et al (2010) Designing focused chemical libraries enriched in protein-protein interaction inhibitors using machine-learning methods. PLoS Comput Biol 6:e1000695
50. Jochim AL, Arora PS (2010) Systematic analysis of helical protein interfaces reveals targets for synthetic inhibitors. ACS Chem Biol 5:919-923
51. Jochim AL, Arora PS (2009) Assessment of helical interfaces in protein-protein interactions. Mol Biosyst 5:924-926
52. Henchey LK, Jochim AL, Arora PS (2008) Contemporary strategies for the stabilization of peptides in the a-helical conformation. Curr Opin Chem Biol 12:692-697
53. Kritzer JA, Lear JD, Hodsdon ME, Schepartz A (2004) Helical b-peptide inhibitors of the p53-hDM2 interaction. J Am Chem Soc 126:9468-9469
54. Henchey LK, Kushal S, Dubey R et al (2010) Inhibition of hypoxia inducible factor 1-transcription coactivator interaction by a hydrogen bond surrogate a-helix. J Am Chem Soc 132:941-943
55. Nam Y, Sliz P, Song L et al (2006) Structural basis for cooperativity in recruitment of MAML coactivators to Notch transcription complexes. Cell 124:973-983
56. Cunningham BC, Wells JA (1989) High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis. Science 244:1081-1085
57. Tovar C, Rosinski J, Filipovic Z et al (2006) Small-molecule MDM2 antagonists reveal aberrant p53 signaling in cancer: implications for therapy. Proc Natl Acad Sci USA 103:1888-1893
58. Fechter EJ, Olenyuk B, Dervan PB (2004) Design of a sequence-specific DNA bisintercalator. Angew Chem Int Ed Engl 43:3591-3594
59. Vassilev LT (2007) MDM2 inhibitors for cancer therapy. Trends Mol Med 13:23-31
60. White RJ, Sharrocks AD (2010) Coordinated control of the gene expression machinery. Trends Genet 26:214-220
61. Berman HM, Westbrook J, Feng Z et al (2000) The protein data bank. Nucleic Acids Res 28:235-242
62. Li W, Jaroszewski L, Godzik A (2001) Clustering of highly homologous sequences to reduce the size of large protein databases. Bioinformatics 17:282-283
63. Kuhlman B, Baker D (2000) Native protein sequences are close to optimal for their structures. Proc Natl Acad Sci USA 97:10383-10388
64. Kortemme T, Baker D (2002) A simple physical model for binding energy hot spots in protein-protein complexes. Proc Natl Acad Sci USA 99:14116-14121
65. Kortemme T, Kim DE, Baker D (2004) Computational alanine scanning of protein-protein interfaces. Sci STKE 2004:pl2
66. Murray JK, Gellman SH (2007) Targeting protein-protein interactions: lessons from p53/ MDM2. Biopolymers 88:657-686
67. Bullock BN, Jochim AL, Arora PS (2011) Assessing helical protein interfaces for inhibitor design. J Am Chem Soc 133:14220-14223
68. Arora PS, Ansari AZ, Best TP et al (2002) Design of artificial transcriptional activators with rigid poly-L-proline linkers. J Am Chem Soc 124:13067-13071
69. Edwards TA, Wilson AJ (2011) Helix-mediated protein-protein interactions as targets for intervention using foldamers. Amino Acids 41:743-754
70. Schafmeister CE, Po J, Verdine GL (2000) An all-hydrocarbon cross-linking system for enhancing the helicity and metabolic stability of peptides. J Am Chem Soc 122:5891-5892
71. Patgiri A, Jochim AL, Arora PS (2008) A hydrogen bond surrogate approach for stabilization of short peptide sequences in alpha-helical conformation. Acc Chem Res 41:1289-1300
72. Gellman SH (1998) Foldamers: a manifesto. Acc Chem Res 31:173-180
73. Cheng RP, Gellman SH, DeGrado WF (2001) b-peptides: from structure to function. Chem Rev 101:3219-3232
74. Horne WS, Gellman SH (2008) Foldamers with heterogeneous backbones. Acc Chem Res 41:1399-1408
75. Seebach D, Gardiner J (2008) b-peptidic peptidomimetics. Acc Chem Res 41:1366-1375
76. Yoo B, Kirshenbaum K (2008) Peptoid architectures: elaboration, actuation, and application. Curr Opin Chem Biol 12:714-721
77. Marimganti S, Cheemala MN, Ahn JM (2009) Novel amphiphilic a-helix mimetics based on a bis-benzamide scaffold. Org Lett 11:4418-4421
78. Plante JP, Burnley T, Malkova B et al (2009) Oligobenzamide proteomimetic inhibitors of the p53-hDM2 protein-protein interaction. Chem Commun 34:5091-5093
79. Shaginian A, Whitby LR, Hong S et al (2009) Design, synthesis, and evaluation of an a-helix mimetic library targeting protein-protein interactions. J Am Chem Soc 131:5564-5572
80. Restorp P, Rebek J Jr (2008) Synthesis of a-helix mimetics with four side-chains. Bioorg Med Chem Lett 18:5909-5911
81. Tosovska P, Arora PS (2010) Oligooxopiperazines as nonpeptidic a-helix mimetics. Org Lett 12:1588-1591
82. Lee JH, Zhang Q, Jo S et al (2011) Novel pyrrolopyrimidine-based a-helix mimetics: cellpermeable inhibitors of protein-protein interactions. J Am Chem Soc 133:676-679
83. Buhrlage SJ, Bates CA, Rowe SP et al (2009) Amphipathic small molecules mimic the binding mode and function of endogenous transcription factors. ACS Chem Biol 4:335-344
84. Nelson DL, Lehninger AL, Cox MM (2008) Principles of biochemistry, 5th edn. W.H Freeman, New York
85. Kossiakoff AA, Koide S (2008) Understanding mechanisms governing protein-protein interactions from synthetic binding interfaces. Curr Opin Struct Biol 18:499-506
86. Argos P (1988) An investigation of protein subunit and domain interfaces. Protein Eng 2:101-113
87. Ko E, Liu J, Perez LM et al (2010) Universal peptidomimetics. J Am Chem Soc 133:462-477
88. Campbell F, Plante JP, Edwards TA et al (2010) N-alkylated oligoamide a-helical proteomimetics. Org Biomol Chem 8:2344-2351
89. Murray JK, Farooqi B, Sadowsky JD et al (2005) Efficient synthesis of a b-peptide combinatorial library with microwave irradiation. J Am Chem Soc 127:13271-13280
90. Sheinerman FB, Norel R, Honig B (2000) Electrostatic aspects of protein-protein interactions. Curr Opin Struct Biol 10:153-159
91. Jones S, Thornton JM (1996) Principles of protein-protein interactions. Proc Natl Acad Sci USA 93:13-20
92. Barlow DJ, Thornton JM (1988) Helix geometry in proteins. J Mol Biol 201:601-619
93. Tyndall JD, Nall T, Fairlie DP (2005) Proteases universally recognize b strands in their active sites. Chem Rev 105:973-999
94. Garner J, Harding MM (2007) Design and synthesis of a-helical peptides and mimetics. Org Biomol Chem 5:3577-3585
95. Felix AM, Heimer EP, Wang CT et al (1988) Synthesis, biological activity and conformational analysis of cyclic GRF analogs. Int J Pept Protien Res 32:441-454
96. Osapay G, Taylor JW (1992) Multicyclic polypeptide model compounds.2. Synthesis and conformational properties of a highly a-helical uncosapeptide constrained by 3 side-chain to side-chain lactam bridges. J Am Chem Soc 114:6966-6973
97. Phelan JC, Skelton NJ, Braisted AC, McDowell RS (1997) A general method for constraining short peptides to an a-helical conformation. J Am Chem Soc 119:455-460
98. Taylor JW (2002) The synthesis and study of side-chain lactam-bridged peptides. Biopolymers 66:49-75
99. Jackson DY, King DS, Chmielewski J et al (1991) General-approach to the synthesis of short a-helical peptides. J Am Chem Soc 113:9391-9392
100. Leduc AM, Trent JO, Wittliff JL et al (2003) Helix-stabilized cyclic peptides as selective inhibitors of steroid receptor-coactivator interactions. Proc Natl Acad Sci USA 100:11273-11278
101. Ghadiri MR, Choi C (1990) Secondary structure nucleation in peptides - transition-metal ion stabilized a-helices. J Am Chem Soc 112:1630-1632
102. Kelso MJ, Beyer RL, Hoangt HN et al (2004) a-turn mimetics: short peptide a-helices composed of cyclic metallopentapeptide modules. J Am Chem Soc 126:4828-4842
103. Ruan FQ, Chen YQ, Hopkins PB (1990) Metal-ion enhanced helicity in synthetic peptides containing unnatural, metal-ligating residues. J Am Chem Soc 112:9403-9404
104. Brunel FM, Dawson PE (2005) Synthesis of constrained helical peptides by thioether ligation: application to analogs of gp41. Chem Commun 20:2552-2554
105. Judice JK, Tom JY, HuangWet al (1997) Inhibition of HIV type 1 infectivity by constrained a-helical peptides: implications for the viral fusion mechanism. Proc Natl Acad Sci USA 94:13426-13430
106. Sia SK, Carr PA, Cochran AG et al (2002) Short constrained peptides that inhibit HIV-1 entry. Proc Natl Acad Sci USA 99:14664-14669
107. Geistlinger TR, Guy RK (2003) Novel selective inhibitors of the interaction of individual nuclear hormone receptors with a mutually shared steroid receptor coactivator 2. J Am Chem Soc 125:6852-6853
108. Mills NL, Daugherty MD, Frankel AD, Guy RK (2006) An a-helical peptidomimetic inhibitor of the HIV-1 Rev-RRE interaction. J Am Chem Soc 128:3496-3497
109. Shepherd NE, Hoang HN, Desai VS et al (2006) Modular a-helical mimetics with antiviral activity against respiratory syncitial virus. J Am Chem Soc 128:13284-13289
110. Blackwell HE, Grubbs RH (1998) Highly efficient synthesis of covalently cross-linked peptide helices by ring-closing metathesis. Angew Chem Int Ed Engl 37:3281-3284
111. Bernal F, Tyler AF, Korsmeyer SJ et al (2007) Reactivation of the p53 tumor suppressor pathway by a stapled p53 peptide. J Am Chem Soc 129:2456-2457
112. Zhang H, Zhao Q, Bhattacharya S et al (2008) A cell-penetrating helical peptide as a potential HIV-1 inhibitor. J Mol Biol 378:565-580
113. Zhang FZ, Sadovski O, Xin SJ, Woolley GA (2007) Stabilization of folded peptide and protein structures via distance matching with a long, rigid cross-linker. J Am Chem Soc 129:14154-14155
114. Fujimoto K, Kajino M, Inouye M (2008) Development of a series of cross-linking agents that effectively stabilize a-helical structures in various short peptides. Chem Eur J 14:857-863
115. Debnath AK (2006) Prospects and strategies for the discovery and development of smallmolecule inhibitors of six-helix bundle formation in class 1 viral fusion proteins. Curr Opin Investig Drugs 7:118-127
116. Labi V, Grespi F, Baumgartner F, Villunger A (2008) Targeting the Bcl-2-regulated apoptosis pathway by BH3 mimetics: a breakthrough in anticancer therapy? Cell Death Differ 15:977-987
117. Walensky LD, Pitter K, Morash J et al (2006) A stapled BID BH3 directly binds and activates BAX. Mol Cell 24:199-210
118. Gavathiotis E, Reyna DE, Davis ML et al (2010) BH3-triggered structural reorganization drives the activation of proapoptotic BAX. Mol Cell 40:481-492
119. Gavathiotis E, Suzuki M, Davis ML et al (2008) BAX activation is initiated at a novel interaction site. Nature 455:1076-1081
120. Danial NN, Walensky LD, Zhang CY et al (2008) Dual role of proapoptotic BAD in insulin secretion and beta cell survival. Nat Med 14:144-153
121. Stewart ML, Fire E, Keating AE, Walensky LD (2010) The MCL-1 BH3 helix is an exclusive MCL-1 inhibitor and apoptosis sensitizer. Nat Chem Biol 6:595-601
122. Lai EC (2004) Notch signaling: control of cell communication and cell fate. Development 131:965-973
123. Nam Y, Aster JC, Blacklow SC (2002) Notch signaling as a therapeutic target. Curr Opin Chem Biol 6:501-509
124. Real PJ, Tosello V, Palomero T et al (2009) g-Secretase inhibitors reverse glucocorticoid resistance in T cell acute lymphoblastic leukemia. Nat Med 15:50-58
125. Trnka TM, Grubbs RH (2001) The development of L2X2Ru?CHR olefin metathesis catalysts: an organometallic success story. Acc Chem Res 34:18-29
126. Hoveyda AH, Gillingham DG, Van Veldhuizen JJ et al (2004) Ru complexes bearing bidentate carbenes: from innocent curiosity to uniquely effective catalysts for olefin metathesis. Org Biomol Chem 2:8-23
127. Zimm BH, Bragg JK (1959) Theory of the phase transition between helix and random coil in polypeptide chains. J Chem Phys 31:526-535
128. Lifson S, Roig A (1961) On the theory of helix-coil transitions in polypeptides. J Chem Phys 34:1963-1974
129. Scholtz JM, Baldwin RL (1992) The mechanism of alpha-helix formation by peptides. Annu Rev Biophys Biomol Struct 21:95-118
130. Chapman R, Kulp JL III, Patgiri A et al (2008) Trapping a folding intermediate of the alphahelix: stabilization of the pi-helix. Biochemistry 47:4189-4195
131. Wang D, Chen K, Kulp JL III, Arora PS (2006) Evaluation of biologically relevant short a-helices stabilized by a main-chain hydrogen-bond surrogate. J Am Chem Soc 128:9248-9256
132. Wang D, Chen K, Dimartino G, Arora PS (2006) Nucleation and stability of hydrogen-bond surrogate-based a-helices. Org Biomol Chem 4:4074-4081
133. Liu J, Wang D, Zheng Q et al (2008) Atomic structure of a short a-helix stabilized by a main chain hdrogen surrogate. J Am Chem Soc 130:4334-4337
134. Blume-Jensen P, Hunter T (2001) Oncogenic kinase signalling. Nature 411:355-365
135. Patgiri A, Yadav KK, Arora PS, Bar-Sagi D (2011) An orthosteric inhibitor of the Ras-Sos interaction. Nat Chem Biol 7:585-587
136. Buday L, Downward J (2008) Many faces of Ras activation. Biochim Biophys Acta 1786:178-187
137. Downward J (2003) Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 3:11-22
138. Joerger AC, Fersht AR (2008) Structural biology of the tumor suppressor p53. Annu Rev Biochem 77:557-582
139. Guarracino DA, Arora PS (2009) Making strides in peptide-based therapeutics. Chem Biol 16:919-920
140. Seebach D, Hook DF, Glattli A (2006) Helices and other secondary structures of b- and g-peptides. Biopolymers 84:23-37
141. Choi SH, Guzei IA, Spencer LC, Gellman SH (2010) Crystallographic characterization of 12-helical secondary structure in b-peptides containing side chain groups. J Am Chem Soc 132:13879-13885
142. Hook DF, Bindschadler P, Mahajan YR et al (2005) The proteolytic stability of designed bpeptides containing a-peptide-bond mimics and of mixed a, b-peptides: application to the construction of MHC-binding peptides. Chem Biodivers 2(5):591-632
143. Kritzer JA, Stephens OM, Guarracino DA et al (2005) b-Peptides as inhibitors of proteinprotein interactions. Bioorg Med Chem 13:11-16
144. Kritzer JA, Luedtke NW, Harker EA, Schepartz A (2005) A rapid library screen for tailoring b-peptide structure and function. J Am Chem Soc 127:14584-14585
145. Kritzer JA, Tirado-Rives J, Hart SA et al (2005) Relationship between side chain structure and 14-helix stability of b3-peptides in water. J Am Chem Soc 127:167-178
146. Chan DC, Fass D, Berger JM, Kim PS (1997) Core structure of gp41 from the HIV envelope glycoprotein. Cell 89:263-273
147. Dimitrov DS (2004) Virus entry: molecular mechanisms and biomedical applications. Nat Rev Microbiol 2:109-122
148. Guarracino DA, Bullock BN, Arora PS (2011) Protein-protein interactions in transcription: a fertile ground for helix mimetics. Biopolymers 95:1-7
149. Yin H, Lee GI, Park HS et al (2005) Terphenyl-based helical mimetics that disrupt the p53/HDM2 interaction. Angew Chem Int Ed Engl 44:2704-2707
150. Shiau AK, Barstad D, Loria PM et al (1998) The structural basis of estrogen receptor/ coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 95:927-937
151. Becerril J, Hamilton AD (2007) Helix mimetics as inhibitors of the interaction of the estrogen receptor with coactivator peptides. Angew Chem Int Ed Engl 46:4471-4473
152. Rutledge SE, Volkman HM, Schepartz A (2003) Molecular recognition of protein surfaces: high affinity ligands for the CBPKIX domain. J Am Chem Soc 125:14336-14347
153. Volkman HM, Rutledge SE, Schepartz A (2005) Binding mode and transcriptional activation potential of high affinity ligands for the CBPKIX domain. J Am Chem Soc 127:4649-4658
154. Li C, Pazgier M, Li J et al (2010) Limitations of peptide retro-inverso isomerization in molecular mimicry. J Biol Chem 285:19572-19581
155. Kritzer JA, Zutshi R, Cheah M et al (2006) Miniature protein inhibitors of the p53-hDM2 interaction. Chembiochem 7:29-31
156. Li C, Liu M, Monbo J et al (2008) Turning a scorpion toxin into an antitumor miniprotein. J Am Chem Soc 130:13546-13548
157. Li C, Pazgier M, Liu M, Lu WY (2009) Apamin as a template for structure-based rational design of potent peptide activators of p53. Angew Chem Int Ed Engl 48:8712-8715