PIN-bodies: A new class of antibody-like proteins with CD4 specificity derived from the protein inhibitor of neuronal nitric oxide synthase

Biochemical and Biophysical Research Communications

Volumn 343, Issue 1, 2006, Pages 334-344

  Bès, Cédric ^a   Troadec, Samuel ^a   Chentouf, Myriam ^a   Breton, Hélène ^a   Lajoix, Anne Dominique ^a   Heitz, Frédéric ^b   Gross, René ^a   Plückthun, Andreas ^c   Chardès, Thierry ^a  

^a CNRS   (France)

^b Centre National de la Recherche Scientifique   (France)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Antibody; CD4; Ligand binding; Paratope derived peptide; Protein inhibitor of neuronal nitric oxide synthase; Scaffold protein

Indexed keywords

ANTIBODY; CANNABINOID; CD4 ANTIGEN; NITRIC OXIDE SYNTHASE; PROTEIN PIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; ENZYME LINKED IMMUNOSORBENT ASSAY; NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; ANTIGEN PRESENTATION; ANTIGENS, CD4; DYNEIN ATPASE; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN CONFORMATION; T-LYMPHOCYTES;

EID: 33645108874     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2006.02.126     Document Type: Article

References (51)

1. D. Laune, F. Molina, G. Ferrières, S. Villard, C. Bès, F. Rieunier, T. Chardès, and C. Granier Application of the Spot method to the identification of peptides and amino-acids from the antibody paratope that contribute to antigen binding J. Immunol. Methods 267 2002 53 70
2. C. Bès, L. Briant-Longuet, M. Pugnière, D. Bresson, M. Cerutti, J.-C. Mani, B. Pau, P. De Berardinis, G. Devauchelle, C. Devaux, C. Granier, and T. Chardès Efficient CD4-binding and immunosuppressive properties of the 13B8.2 monoclonal antibody are displayed by its CDR-H1-derived peptide CB1 FEBS Lett. 508 2001 67 74
3. K. Hilpert, H. Wessner, J. Schneider-Mergener, K. Welfe, R. Misselwitz, H. Welfe, A.C. Hocke, S. Hippenstiel, and W. Höne Design and characterization of a hybrid miniprotein that specifically inhibits porcine pancreatic elastase J. Biol. Chem. 278 2003 24986 24993
4. R. Hussain, N.S. Courtenay-Lucket, and G. Siligardi Structure-function correlation and biostability of antibody CDR-derived peptides as tumour imaging agents Biomed. Pept. Proteins Nucleic Acids 2 1996 67 70
5. N. Benkirane, G. Guichard, J.-P. Briand, and S. Muller Exploration of requirements for peptidomimetic immune recognition. Antigenic and immunogenic properties of reduced peptide bond pseudopeptide analogues of a histone hexapeptide J. Biol. Chem. 271 1996 33218 33224
6. F. Casset, F. Roux, P. Mouchet, C. Bès, T. Chardès, C. Granier, J.-C. Mani, M. Pugnière, D. Laune, B. Pau, M. Kaczorek, R. Lahana, and A. Rees A peptide mimetic of an anti-CD4 monoclonal antibody by rational design Biochem. Biophys. Res. Commun. 307 2003 198 205
7. M.H. Van Regenmortel, and S. Muller D-peptides as immunogens and diagnostic reagents Curr. Opin. Biotechnol. 9 1998 377 382
8. H.M. Dintzis, D.E. Symer, R.Z. Dintzis, L.E. Zawadzke, and J.M. Berg A comparison of the immunogenicity of a pair of enantiomeric proteins Proteins 16 1993 306 308
9. A. Skerra Engineered protein scaffolds for molecular recognition J. Mol. Recogn. 13 2000 167 187
10. S.M. King, and R.S. Patel-King The M(r) = 8000 and 11,000 outer arm dynein light chains from Chlamydomonas flagella have cytoplasmic homologues J. Biol. Chem. 270 1995 11445 11452
11. S.M. King, E. Barbarese, J.F. Dillman, R.S. Patel-King, J.H. Carson, and K.K. Pfister Brain cytoplasmic and flagellar outer arm dyneins share a highly conserved Mr 8,000 light chain J. Biol. Chem. 271 1996 19358 19366
12. S.E. Benashski, A. Harrison, R.S. Patel-King, and S.M. King Dimerization of the highly conserved light chain shared by dynein and myosin V J. Biol. Chem. 272 1997 20929 20935
13. F.S. Espindola, D.M. Suter, L.B. Partata, T. Cao, J.S. Wolenski, R.E. Cheney, S.M. King, and M.S. Mooseker The light chain composition of chicken brain myosin-Va: calmodulin, myosin-II essential light chains, and 8-kDa dynein light chain/PIN Cell Motil. Cytoskeleton 47 2000 269 281
14. S.R. Jaffrey, and S.H. Snyder PIN: an associated protein inhibitor of neuronal nitric oxide synthase Science 274 1996 774 777
15. A.D. Lajoix, R. Gross, C. Aknin, S. Dietz, C. Granier, and D. Laune Cellulose membrane supported peptide arrays for deciphering protein-protein interaction sites: the case of PIN, a protein with multiple natural partners Mol. Divers. 8 2004 281 290
16. J. Liang, S.R. Jaffrey, W. Guo, S.H. Snyder, and J. Clardy Structure of the PIN/LC8 dimer with a bound peptide Nat. Struct. Biol. 6 1996 735 740
17. H. Tochio, S. Ohki, Q. Zhang, M. Li, and M. Zhang Solution structure of a protein inhibitor of neuronal nitric oxide synthase Nat. Struct. Biol. 5 1998 965 969
18. J. Fan, Q. Zhang, H. Tochio, M. Li, and M. Zhang Structural basis of diverse sequence-dependent target recognition by the 8 kDa dynein light chain J. Mol. Biol. 306 2001 97 108
19. M.F. Krummel, and M.M. Davis Dynamics of the immunological synapse: finding, establishing and solidifying a connection Curr. Opin. Immunol. 14 2002 66 74
20. L. Briant, and C. Devaux Bioactive CD4 ligands as pre and/or postbinding inhibitors of HIV-1 Adv. Pharmacol. 48 2000 373 407
21. C. Bès, M. Cerutti, L. Briant-Longuet, D. Bresson, S. Péraldi-Roux, M. Pugnière, J.-C. Mani, B. Pau, C. Devaux, C. Granier, G. Devauchelle, and T. Chardès The chimeric mouse-human anti-CD4 Fab 13B8.2 expressed in baculovirus inhibits both antigen presentation and HIV-1 promoter activation Hum. Antibodies 10 2001 67 76
22. M. Benkirane, P. Corbeau, V. Housset, and C. Devaux An antibody that binds the immunoglobulin CDR3-like region of the CD4 molecule inhibits provirus transcription in HIV-infected T cells EMBO J. 12 1993 4909 4921
23. S. Troadec, C. Bès, M. Chentouf, B. Nguyen, L. Briant, C. Jacquet, K. Chebli, M. Pugnière, F. Roquet, M. Cerutti, and T. Chardès Biological activities on T lymphocytes of a baculovirus-expressed chimeric recombinant IgG1 antibody with specificity for the CDR3-like loop on the D1 domain of the CD4 molecule Clin. Immunol. 119 2006 38 50
24. D. Laune, F. Molina, G. Ferrieres, J.-C. Mani, P. Cohen, D. Simon, T. Bernardi, M. Piechaczyk, B. Pau, and C. Granier Systematic exploration of the antigen binding activity of synthetic peptides isolated from the variable regions of immunoglobulins J. Biol. Chem. 272 1997 30937 30944
25. C. Monnet, D. Laune, J. Laroche-Traineau, M. Biard-Piechaczyk, L. Briant, C. Bès, M. Pugnière, J.-C. Mani, B. Pau, M. Cerutti, G. Devauchelle, C. Devaux, C. Granier, and T. Chardès Synthetic peptides derived from the variable regions of an anti-CD4 monoclonal antibody bind to CD4 and inhibit HIV-1 promoter activation in virus-infected cell J. Biol. Chem. 274 1999 3789 3796
26. M. Pugnière, T. Chardès, C. Bès, C. Monnet, D. Laune, C. Granier, and J.-C. Mani Interaction analysis of CD4 with a synthetic peptide derived from the paratope of ST-40, an anti-CD4 monoclonal antibody Int. J. Biochromatogr. 5 2000 187 197
27. R. Franck Spot-synthesis: an easy technique for the positionally addressable, parallel chemical synthesis on a membrane support Tetrahedron 98 1992 9217 9232
28. F. Molina, D. Laune, C. Gougat, B. Pau, and C. Granier Improved performances of spot multiple peptide synthesis Pept. Res. 9 1996 151 155
29. C. Bès, L. Briant-Longuet, M. Cerutti, F. Heitz, S. Troadec, M. Pugnière, F. Roquet, F. Molina, F. Casset, D. Bresson, S. Péraldi-Roux, G. Devauchelle, C. Devaux, C. Granier, and T. Chardès Mapping the paratope of anti-CD4 recombinant Fab 13B8.2 by combining parallel peptide synthesis and site-directed mutagenesis J. Biol. Chem. 278 2003 14265 14273
30. S.N. Ho, H.D. Hunt, R. Horton, J.K. Pullen, and L. Pease Site-directed mutagenesis by overlap extension using the polymerase chain reaction Gene 77 1989 51 58
31. F. Manca, P. De Berardinis, D. Fenoglio, M.N. Ombra, G. Li Pira, D. Saverino, M. Autiero, L. Lozzi, L. Bracci, and J. Guardiola Antigenicity of HIV-derived T helper determinants in the context of carrier recombinant proteins: effect on T helper cell repertoire selection Eur. J. Immunol. 26 1996 2461 2469
32. Y. Cheng, and W.H. Prusoff Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 percent inhibition (I50) of an enzymatic reaction Biochem. Pharmacol. 22 1973 3099 3108
33. H.K. Binz, P. Amstutz, and A. Plückthun Engineering novel binding proteins from nonimmunoglobulin domains Nat. Biotechnol. 23 2005 1257 1268
34. R.C. Ladner Constrained peptides as binding entities Trends Biotechnol. 13 1995 426 430
35. L.R. Helms, and R. Wetzel Proteolytic excision and in situ cyclization of a bioactive loop from an REI-VL presentation scaffold Protein Sci. 3 1994 1108 1113
36. J. Janin, and C. Chotia The structure of protein-protein recognition sites J. Biol. Chem. 265 1990 16027 16030
37. J.W. Smith, D. Hu, K. Satterthwait, S. Pinz-Sweeney, and C.F. Barbas III Building synthetic antibodies as adhesive ligands for integrins J. Biol. Chem. 269 1994 32788 32795
38. E. Barbar, M. Hare, M. Makokha, G. Barany, and C. Woodward Dimerization and folding of LC8, a highly conserved light chain of cytoplasmic dynein Biochemistry 40 2001 9734 9742
39. B. Peelle, J. Lorens, W. Li, J. Bogenberger, D.G. Payan, and D.C. Anderson Intracellular protein scaffold-mediated display of random peptide libraries for phenotypic screens in mammalian cells Chem. Biol. 8 2001 521 534
40. D.A. Laplagne, V. Zylberman, N. Ainciart, M.W. Steward, E. Sciutto, C.A. Fossati, and F.A. Goldbaum Engineering of a polymeric bacterial protein as a scaffold for the multiple display of peptides Proteins 57 2004 820 828
41. E.S. Ward, D. Güssow, A.D. Griffith, P.T. Jones, and G. Winter Binding activities of a repertoire of single immunoglobulin variable domains secreted from Escherichia coli Nature 341 1989 544 546
42. B.L. Roberts, W. Markland, A.C. Ley, R.B. Kent, D.W. White, S.K. Guterman, and R.C. Ladner Directed evolution of a protein: selection of potent neutrophil elastase inhibitors displayed on M13 fusion phage Proc. Natl. Acad. Sci. USA 89 1992 2429 2433
43. C.I. Wang, Q. Yang, and S. Craik Isolation of a high affinity inhibitor of urokinase-type plasminogen activator by phage display of ecotin J. Biol. Chem. 270 1995 12250 12256
44. M. Uhlén, G. Forsberg, T. Moks, M. Hartmanis, and B. Nilsson Fusion proteins in biotechnology Curr. Opin. Biotechnol. 3 1992 363 369
45. G. Beste, F.S. Schmidt, T. Stibora, and A. Skerra Small antibody-like proteins with prescribed ligand specificities derived from the lipocalin fold Proc. Natl. Acad. Sci. USA 96 1999 1898 1903
46. D.L. Le Nguyen, A. Heitz, L. Chiche, B. Castro, R.A. Boigegrain, A. Favel, and M.A. Coletti-Previero Molecular recognition between serine proteases and new bioactive microproteins with a knotted structure Biochimie 72 1990 431 435
47. C. Vita, J. Vizzavona, E. Drakopoulou, S. Zinn-Justin, B. Gilquin, and A. Ménez Novel miniproteins engineered by the transfer of active sites to small natural scaffolds Biopolymers 47 1998 93 100
48. C. Vita, E. Drakopoulou, J. Vizzanova, S. Rochette, L. Martin, A. Ménez, C. Roumestand, Y.-S. Yang, L. Ylisastigui, A. Benjouad, and J.-C. Gluckman Rational engineering of a miniprotein that reproduces the core of the CD4 site interacting with HIV-1 envelope glycoprotein Proc. Natl. Acad. Sci. USA 96 1999 13091 13096
49. Z. Lu, K.S. Murray, V. Van Cleave, E.R. LaVallie, M.L. Stahl, and J.M. McCoy Expression of thioredoxin random peptide libraries on the Escherichia coli cell surface as functional fusions to flagellin: a system designed for exploring protein-protein interactions Bio/Technology 13 1995 366 372
50. G. Lee, W. Chan, M.R. Hurle, R.L. Desjalais, F. Watson, G.M. Sathe, and R. Wetzel Strong inhibition of fibrinogen binding to platelet receptor alpha IIb beta 3 by RGD sequences installed into a presentation scaffold Protein Eng. 6 1993 745 754
51. B. Zhao, L.R. Helms, R.L. Desjalais, S.S. Abdel-Meguid, and R. Wetzel A paradigm for drug discovery using a conformation from the crystal structure of a presentation scaffold Nat. Struct. Biol. 2 1995 1131 1137