Truncated and Helix-Constrained Peptides with High Affinity and Specificity for the cFos Coiled-Coil of AP-1

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Rao, Tara ^a   Ruiz Gómez, Gloria ^b   Hill, Timothy A ^b   Hoang, Huy N ^b   Fairlie, David P ^b   Mason, Jody M ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN C FOS; PROTEIN C JUN; TRANSCRIPTION FACTOR AP 1;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; ENTHALPY; ENTROPY; HUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; CALORIMETRY; CIRCULAR DICHROISM; HUMANS; LEUCINE ZIPPERS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PEPTIDES; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-FOS; TEMPERATURE; TRANSCRIPTION FACTOR AP-1;

EID: 84875455700     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059415     Document Type: Article

References (58)

1. Mason JM, (2010) Design and development of peptides and peptide mimetics as antagonists for therapeutic intervention. Future Med Chem 2: 1813-1822.
2. Fairlie DP, West ML, Wong AK, (1998) Towards protein surface mimetics. Curr Med Chem 5: 29-62.
3. Derossi D, Joliot AH, Chassaing G, Prochiantz A, (1994) The third helix of the Antennapedia homeodomain translocates through biological membranes. J Biol Chem 269: 10444-10450.
4. Fuchs SM, Raines RT, (2006) Internalization of cationic peptides: the road less (or more?) traveled. Cell Mol Life Sci 63: 1819-1822.
5. Vives E, Brodin P, Lebleu B, (1997) A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J Biol Chem 272: 16010-16017.
6. Judice JK, Tom JY, Huang W, Wrin T, Vennari J, et al. (1997) Inhibition of HIV type 1 infectivity by constrained alpha-helical peptides: implications for the viral fusion mechanism. Proc Natl Acad Sci U S A 94: 13426-13430.
7. Walensky LD, Kung AL, Escher I, Malia TJ, Barbuto S, et al. (2004) Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix. Science 305: 1466-1470.
8. Kutchukian PS, Yang JS, Verdine GL, Shakhnovich EI, (2009) All-atom model for stabilization of alpha-helical structure in peptides by hydrocarbon staples. J Am Chem Soc 131: 4622-4627.
9. Harrison RS, Shepherd NE, Hoang HN, Ruiz-Gomez G, Hill TA, et al. (2010) Downsizing human, bacterial, and viral proteins to short water-stable alpha helices that maintain biological potency. Proc Natl Acad Sci U S A 107: 11686-11691.
10. Bird GH, Madani N, Perry AF, Princiotto AM, Supko JG, et al. (2010) Hydrocarbon double-stapling remedies the proteolytic instability of a lengthy peptide therapeutic. Proc Natl Acad Sci U S A 107: 14093-14098.
11. Shepherd NE, Hoang HN, Abbenante G, Fairlie DP, (2005) Single turn peptide alpha helices with exceptional stability in water. J Am Chem Soc 127: 2974-2983.
12. Bernal F, Tyler AF, Korsmeyer SJ, Walensky LD, Verdine GL, (2007) Reactivation of the p53 tumor suppressor pathway by a stapled p53 peptide. J Am Chem Soc 129: 2456-2457.
13. Walensky LD, Pitter K, Morash J, Oh KJ, Barbuto S, et al. (2006) A stapled BID BH3 helix directly binds and activates BAX. Mol Cell 24: 199-210.
14. Bird GH, Bernal F, Pitter K, Walensky LD, (2008) Synthesis and biophysical characterization of stabilized alpha-helices of BCL-2 domains. Methods Enzymol 446: 369-386.
15. Moellering RE, Cornejo M, Davis TN, Del Bianco C, Aster JC, et al. (2009) Direct inhibition of the NOTCH transcription factor complex. Nature 462: 182-188.
16. Kim YW, Verdine GL, (2009) Stereochemical effects of all-hydrocarbon tethers in i,i+4 stapled peptides. Bioorg Med Chem Lett 19: 2533-2536.
17. Bernal F, Wade M, Godes M, Davis TN, Whitehead DG, et al. (2010) A stapled p53 helix overcomes HDMX-mediated suppression of p53. Cancer Cell 18: 411-422.
18. Kim YW, Grossmann TN, Verdine GL, (2011) Synthesis of all-hydrocarbon stapled alpha-helical peptides by ring-closing olefin metathesis. Nat Protoc 6: 761-771.
19. Baek S, Kutchukian PS, Verdine GL, Huber R, Holak TA, et al. (2012) Structure of the stapled p53 peptide bound to Mdm2. J Am Chem Soc 134: 103-106.
20. Chapman RN, Dimartino G, Arora PS, (2004) A highly stable short alpha-helix constrained by a main-chain hydrogen-bond surrogate. J Am Chem Soc 126: 12252-12253.
21. Wang D, Liao W, Arora PS, (2005) Enhanced metabolic stability and protein-binding properties of artificial alpha helices derived from a hydrogen-bond surrogate: application to Bcl-xL. Angew Chem Int Ed Engl 44: 6525-6529.
22. Wang D, Chen K, Kulp Iii JL, Arora PS, (2006) Evaluation of biologically relevant short alpha-helices stabilized by a main-chain hydrogen-bond surrogate. J Am Chem Soc 128: 9248-9256.
23. Wang D, Chen K, Dimartino G, Arora PS, (2006) Nucleation and stability of hydrogen-bond surrogate-based alpha-helices. Org Biomol Chem 4: 4074-4081.
24. 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.
25. Chapman R, Kulp JL 3rd, Patgiri A, Kallenbach NR, Bracken C, et al (2008) Trapping a folding intermediate of the alpha-helix: stabilization of the pi-helix. Biochemistry 47: 4189-4195.
26. Liu J, Wang D, Zheng Q, Lu M, Arora PS, (2008) Atomic structure of a short alpha-helix stabilized by a main chain hydrogen-bond surrogate. J Am Chem Soc 130: 4334-4337.
27. Wang D, Lu M, Arora PS, (2008) Inhibition of HIV-1 fusion by hydrogen-bond-surrogate-based alpha helices. Angew Chem Int Ed Engl 47: 1879-1882.
28. Henchey LK, Kushal S, Dubey R, Chapman RN, Olenyuk BZ, et al. (2010) Inhibition of hypoxia inducible factor 1-transcription coactivator interaction by a hydrogen bond surrogate alpha-helix. J Am Chem Soc 132: 941-943.
29. Guarracino DA, Bullock BN, Arora PS, (2011) Mini review: protein-protein interactions in transcription: a fertile ground for helix mimetics. Biopolymers 95: 1-7.
30. Bullock BN, Jochim AL, Arora PS, (2011) Assessing helical protein interfaces for inhibitor design. J Am Chem Soc 133: 14220-14223.
31. Appella DH, Christianson LA, Klein DA, Powell DR, Huang X, et al. (1997) Residue-based control of helix shape in beta-peptide oligomers. Nature 387: 381-384.
32. Seebach D, Gardiner J, (2008) Beta-peptidic peptidomimetics. Acc Chem Res 41: 1366-1375.
33. Shepherd NE, Abbenante G, Fairlie DP, (2004) Consecutive cyclic pentapeptide modules form short alpha-helices that are very stable to water and denaturants. Angew Chem Int Ed Engl 43: 2687-2690.
34. Shepherd NE, Hoang HN, Desai VS, Letouze E, Young PR, et al. (2006) Modular alpha-helical mimetics with antiviral activity against respiratory syncitial virus. J Am Chem Soc 128: 13284-13289.
35. 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.
36. Ozanne BW, Spence HJ, McGarry LC, Hennigan RF, (2007) Transcription factors control invasion: AP-1 the first among equals. Oncogene 26: 1-10.
37. Eferl R, Wagner EF, (2003) AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 3: 859-868.
38. Libermann TA, Zerbini LF, (2006) Targeting transcription factors for cancer gene therapy. Curr Gene Ther 6: 17-33.
39. Zenz R, Eferl R, Scheinecker C, Redlich K, Smolen J, et al. (2008) Activator protein 1 (Fos/Jun) functions in inflammatory bone and skin disease. Arthritis Res Ther 10: 201.
40. Wagner EF, Eferl R, (2005) Fos/AP-1 proteins in bone and the immune system. Immunol Rev 208: 126-140.
41. Aud D, Peng SL, (2006) Mechanisms of disease: Transcription factors in inflammatory arthritis. Nat Clin Pract Rheumatol 2: 434-442.
42. Mason JM, Muller KM, Arndt KM, (2007) Positive aspects of negative design: simultaneous selection of specificity and interaction stability. Biochemistry 46: 4804-4814.
43. Lavigne P, Sonnichsen FD, Kay CM, Hodges RS, (1996) Interhelical salt bridges, coiled-coil stability, and specificity of dimerization. Science 271: 1136-1138.
44. O'Shea EK, Lumb KJ, Kim PS, (1993) Peptide 'Velcro': design of a heterodimeric coiled coil. Curr Biol 3: 658-667.
45. O'Shea EK, Rutkowski R, Kim PS, (1989) Evidence that the leucine zipper is a coiled coil. Science 243: 538-542.
46. O'Shea EK, Rutkowski R, Kim PS, (1992) Mechanism of specificity in the Fos-Jun oncoprotein heterodimer. Cell 68: 699-708.
47. Mason JM, Schmitz MA, Muller KM, Arndt KM, (2006) Semirational design of Jun-Fos coiled coils with increased affinity: Universal implications for leucine zipper prediction and design. Proc Natl Acad Sci U S A 103: 8989-8994.
48. Mason JM, Hagemann UB, Arndt KM, (2009) Role of hydrophobic and electrostatic interactions in coiled coil stability and specificity. Biochemistry 48: 10380-10388.
49. Crooks RO, Rao T, Mason JM, (2011) Truncation, Randomization, and Selection: Generation of a Reduced Length c-Jun Antagonist That Retains High Interaction Stability. J Biol Chem 286: 29470-29479.
50. Dixon JM, Taniguchi M, Lindsey JS, (2005) PhotochemCAD 2: a refined program with accompanying spectral databases for photochemical calculations. Photochem Photobiol 81: 212-213.
51. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, et al. (1983) CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem 4: 187-217.
52. Ibarra-Molero B, Makhatadze GI, Matthews CR, (2001) Mapping the energy surface for the folding reaction of the coiled-coil peptide GCN4-p1. Biochemistry 40: 719-731.
53. Krylov D, Barchi J, Vinson C, (1998) Inter-helical interactions in the leucine zipper coiled coil dimer: pH and salt dependence of coupling energy between charged amino acids. J Mol Biol 279: 959-972.
54. Fairlie DP, Tyndall JD, Reid RC, Wong AK, Abbenante G, et al. (2000) Conformational selection of inhibitors and substrates by proteolytic enzymes: implications for drug design and polypeptide processing. J Med Chem 43: 1271-1281.
55. Tyndall JD, Nall T, Fairlie DP, (2005) Proteases universally recognize beta strands in their active sites. Chem Rev 105: 973-999.
56. Johnson LM, Horne WS, Gellman SH, (2011) Broad distribution of energetically important contacts across an extended protein interface. J Am Chem Soc 133: 10038-10041.
57. Wiseman T, Williston S, Brandts JF, Lin LN, (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal Biochem 179: 131-137.
58. Glover JN, Harrison SC, (1995) Crystal structure of the heterodimeric bZIP transcription factor c-Fos-c-Jun bound to DNA. Nature 373: 257-261.