Anti-idiotypic antibody mimics proteolytic function of parent antigen

Biochemistry

Volumn 46, Issue 50, 2007, Pages 14598-14609

  Ponomarenko, Natalia A ^a   Pillet, Dominique ^b   Paon, Marjorie ^b   Vorobiev, Ivan I ^a   Smirnov, Ivan V ^a,c   Adenier, Hervé ^b   Avalle, Bérangère ^b   Kolesnikov, Alexander V ^a   Kozyr, Arina V ^a   Thomas, Daniel ^b   Gabibov, Alexander G ^a,d   Friboulet, Alain ^b  

^a SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^b UNIVERSITÉ DE TECHNOLOGIE DE COMPIÈGNE   (France)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

^d INSTITUTE OF GENE BIOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOPEPTIDASE; ESTERASE ACTIVITIES; IDIOTYPIC NETWORKS; ZYMOGRAPHY;

ANTIBODIES; CATALYST ACTIVITY; ENZYME ACTIVITY; FLUORESCENCE; HYDROLYSIS; IMAGE ANALYSIS;

ANTIGENS;

AMIDASE; ANTIBODY; ANTIGEN; BENZYLSULFONYL FLUORIDE; ESTERASE; FLUORESCEIN; MONOCLONAL ANTIBODY AB1 5H4; MONOCLONAL ANTIBODY AB2 6B8 E12; PROTEINASE; RIBONUCLEASE A; SERINE DEHYDRATASE; SUBTILISIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CATALYSIS; CLONING; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ESCHERICHIA COLI; HYDROLYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, ANTI-IDIOTYPIC; ANTIBODIES, MONOCLONAL; ANTIGENS; BASE SEQUENCE; BINDING SITES; CATALYSIS; HYDROLYSIS; MICE; MICE, INBRED BALB C; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SEQUENCE ALIGNMENT; SUBTILISINS;

ESCHERICHIA COLI;

EID: 37249056465     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7013954     Document Type: Article

References (53)

1. Bamias, G., and Cominelli, F. (2006) Novel strategies to attenuate immune activation in Crohn's disease. Curr. Opin. Pharmacol. 6, 401-407.
2. Paul, S., Nishiyama, Y., Planque, S., and Tagushi, H. (2006) Theory of proteolytic antibody occurrence. Immunol. Lett. 103, 8-16.
3. Hilvert, D. (2005) Mimicking enzymes with antibodies, In Artificial Enzymes (Breslow, R., Ed.) pp 89-109, Wiley-VCH, Weinheim.
4. Gabibov, A. G. (2006) Antibody catalysis: Biochemistry, immunology, pathology. Immunol. Lett. 103, 1-2.
5. Tramontano, A., Janda, K. D., and Lerner, R. A. (1986) Catalytic antibodies. Science 234, 1566-1570.
6. Pollack, S. J., Jacobs, J. W., and Schultz, P. G. (1986) Selective chemical catalysis by an antibody. Science 234, 1570-1573.
7. Hilvert, D. (2000) Critical analysis of antibody catalysis. Annu. Rev. Biochem. 69, 751-793.
8. Kalaga, R., Li, L., O'Dell, J. R., and Paul, S. (1995) Unexpected presence of polyreactive catalytic Abs in IgG from unimmunized donors and decreased levels in rheumatoid arthritis. J. Immunol. 155, 2695-2702.
9. Planque, S., Bangale, Y., Song, X. T., Karle, S., Tagushi, H., Poindexter, B., Bick, R., Edmundson, A., Nishiyama, Y., and Paul, S. (2004) Ontogeny of proteolytic immunity: IgM serine proteases. J. Biol. Chem. 279, 14024-14032.
10. Paul, S., Volle, D. J., Beach, C. M., Johnson, D. R., Powell, M. J., and Massey, R. J. (1989) Catalytic hydrolysis of vasoactive intestinal peptide by human autoantibody. Science 244, 1158-1162.
11. Shuster, A. M., Gololobov, G. V., Kvashuk, O. A., Bogomolova, A. E., Smirnov, I. V., and Gabibov, A. G. (1992) DNA hydrolyzing autoantibodies. Science 256, 665-667.
12. Gololobov, G. V., Chernova, E. A., Schourouv, D. V., Smirnov, I. V., Kudelina, I. A., and Gabibov, A. G. (1995) Cleavage of supercoiled plasmid DNA by autoantibody Fab fragment: Application of the flow linear dichroism technique. Proc. Natl. Acad. Sci. U.S.A. 92, 254-257.
13. Li, L., Paul, S., Tyutyulkova, S., Kazatchkine, M. D., and Kaveri, S. (1995) Catalytic activity of anti-thyroglobulin antibodies. J. Immunol. 154, 3328-3332.
14. Lacroix-Desmazes, S., Bayry, J., Kaveri, S., Hayon-Sonsino, D., Thorenoor, N., Charpentier, J., Luyt, C. E., Mira, J. P., Nagaraja, V., Kazatchkine, M. D., Dhainaut, J. F., and Mallet, V. O. (2005) High levels of catalytic antibodies correlate with favorable outcome in sepsis. Proc. Natl. Acad. Sci. U.S.A. 102, 4109-4113.
15. Ponomarenko, N. A., Durova, O. M., Vorobiev, I. I., Belogurov, A. A., Telegin, G. B., Suchkov, S. V., Misikov, V. K., Kiselev, S. L., Lagarkova, M. A., Govorun, V. M., Serebryakova, M. V., Avalle, B., Tornatore, P., Karavanov, A., Morse, H. C., Thomas, D., Friboulet, A., and Gabibov, A. G. (2006) Autoantibodies to myelin basic protein catalyze site-specific degradation of their antigen. Proc. Natl. Acad. Sci. U.S.A. 103, 281-286.
16. Ponomarenko, N. A., Durova, O. M., Vorobiev, I. I., Belogurov, A. A., Telegin, G. B., Suchkov, S. V., Misikov, V. K., Morse, H. C., and Gabibov, A. G. (2006) Catalytic activity of autoantibodies toward myelin basic protein correlates with the scores on the multiple sclerosis expanded disability status scale. Immunol. Lett. 103, 45-50.
17. Lacroix-Desmazes, S., Moreau, A., Sooryanarayana, Bonnemain, C. Stieltjes, N., Pashov, A., Sultan, Y., Hoebeke, J., Kazatchkine, M. D., and Kaveri, S. V. (1999) Catalytic activity of antibodies against factor VIII in patients with hemophila A. Nat. Med. 5, 1044-1047.
18. Blackburn, G. M., and Garçon, A. (2000) Catalytic antibodies, in Biotechnology vol.8, (Rehm, H. J., and Reed, G., Eds.) pp 404-490, Wiley VCH, Weinheim.
19. Thayer, M. M., Olender, E. H., Arvai, A. S., Koike, C. K., Canestrelli, I. L., Stewart, J. D., Benkovic, S. J., Getzoff, E. D., and Roberts, V. A. (1999) Structural basis for amide hydrolysis catalyzed by the 43C9 antibody. J. Mol. Biol. 291, 329-345.
20. Chong, L. T., Bandyopadhyay, P., Scanlan, T. S., Kuntz, I. D., and Kollman, P. A. (2003) Direct hydroxide attack is a plausible mechanism for amidase antibody 43C9. J. Comput. Chem. 24, 1371-1377.
21. Benedetti, F., Berti, F., Brady, K., Colombatti, A., Pauletto, A., Pucillo, C., and Thomas, N. R. (2004) An unprecedented catalytic motif revealed in the model structure of amide hydrolyzing antibody 312d6. Chembhchem 5, 129-131.
22. Kim, Y. R., Kim, J. S., Lee, S. H., Lee, W. R., Sohn, J. N., Chung, Y. C., Shim, H. K., Lee, S. C., Kwon, M. H., and Kim, Y. S. (2006) Heavy and light chain variable single domains of an anti-DNA binding antibody hydrolyze both double- and single-stranded DNAs without sequence specificity. J. Biol. Chem. 281, 15287-15295.
23. Jerne, N. (1974) Towards a network theory of the immune system. Ann. Immunol. (Paris) 125c, 373-389.
24. Izadyar, L., Friboulet, A., Rémy, M. H., Roseto, A., and Thomas, D. (1993) Monoclonal anti-idiotypic antibodies as functional internal images of enzyme active sites: Production of a catalytic antibody with a Cholinesterase activity. Proc. Natl. Acad. Sci. U.S.A. 90, 8876-8880.
25. Kolesnikov, A. V., Kozyr, A. V., Alexandrova, E. S., Koralewski, F., Demin, A. V., Titov, M. I., Avalle, B., Tramontano, A., Paul, S., Thomas, D., Gabibov, A. G., and Friboulet, A. (2000) Enzyme mimicry by the anti-idiotypic antibody approach. Proc. Natl. Acad. Sci. U.S.A. 97, 13526-13531.
26. Avalle, B., Thomas, D., and Friboulet, A. (1998) Functional mimicry: Elicitation of a monoclonal anti-idiotypic antibody hydrolyzing β-lactams. FASEB J. 12, 1055-1060.
27. Débat, H., Avalle, B., Chose, O., Sarde, C. O., Friboulet, A., and Thomas, D. (2001) Overpassing an aberrant Vk gene to sequence an anti-idiotypic abzyme with β-lactamase-like activity that could have a linkage with autoimmune diseases. FASEB J. 15, 815-822.
28. Padiolleau-Lefèvre, S., Débat, H., Phichith, D., Thomas, D., Friboulet, A., and Avalle, B. (2006) Expression of a functional scFv fragment of an anti-idiotypic antibody with a β-lactam hydrolytic activity. Immunol. Lett. 103, 39-44.
29. Pillet, D., Paon, M., Vorobiev, I. I., Gabibov, A. G., Thomas, D., and Friboulet, A. (2002) Idiotypic network mimicry and antibody catalysis: Lessons for the elicitation of efficient anti-idiotypic protease antibodies. J. Immunol. Methods 269, 5-12.
30. Voss, E. W., Workmann, C. J., and Mummert, M. E. (1996) Detection of protease activity using a fluorescence-enhancement globular substrate. Biotechniques 20, 286-291.
31. Ponomarenko, N. A., Durova, O. M., Vorobiev, I. I., Alexandrova, E. A., Telegin, G. B., Chamborant, O. A., Sidorik, L. L., Suchkov, S. V., Alekberova, Z. S., Gnuchev, N. V., and Gabibov, A. G. (2002) Catalytic antibodies in clinical and experimental pathology: Human and mouse models. J. Immunol. Methods 269, 197-211.
32. Avalle, B., Friboulet, A., and Thomas, D. (1998) Screening of inhibitory monoclonal antibody. A critical step for producing antiidiotypic catalytic antibodies. Ann. N.Y. Acad. Sci. 864, 118-130.
33. Keitel, T., Kramer, A., Wessner, H., Scholz, C., Schreider-Mergener, J., and Höhne, W. (1997) Crystallographic analysis of anti-p24 (HIV-1) monoclonal antibody cross-reactivity and polyspecificity. Cell 91, 811-820.
34. Lescar, J., Stouracova, R., Riottot, M. M., Chitarra, V., Brynda, J., Fabry, M., Horejsi, M., Sedlacek, J., and Bentley, G. A. (1997) Three-dimensional structure of an Fab-peptide complex: Structural basis of HIV-1 protease inhibition by a monoclonal antibody. J. Mol. Biol. 267, 1207-1222.
35. Chavali, G., Papageorgiou, A., Olson, K., Fett, J., Hu, G., Shapiro, R., and Acharya, K. R. (2003) The crystal structure of human angiogenin in complex with an antitumor neutralizing antibody. Structure 11, 875-885.
36. Ay, J., Keitel, T., Küttner, G., Wessner, H., Scholz, C., Hahn, M., and Höhne, W. (2000) Crystal structure of a phage library-derived single-chain Fv fragment complexed with turkey egg-white lysozyme at 2.0 A resolution. J. Mol. Biol. 301, 239-245.
37. Rezacova, P., Lescar, J., Brynda, J., Fabry, M., Horejsi, M., Sedlacek, J., and Bentley, G. A. (2001) Structural basis of HIV-1 and HIV-2 protease inhibition by a monoclonal antibody. Structure 9, 887-895.
38. Zhou, T., Hamer, D. H., Hendrickson, W. A., Sattentau, Q. J., and Kwong, P. D. (2005) Interfacial metal and antibody recognition. Proc. Natl. Acad. Sci. U.S.A. 102, 14575-14580.
39. Young, A. C. M., Valadon, A. C., Casadevall, A., Scharff, M. D., and Sacchettini, J. C. (1997) The three-dimensional structures of a polysaccharide binding antibody to Cryptococcus neoformans and its complex with a peptide from a phage display library: Implications for the identification of peptide mimotopes. J. Mol. Biol. 274, 622-634.
40. Brunger, A. T., Leahy, D. J., Hynes, T. R., and Fox, R. O. (1991) 2.9 A resolution structure of an anti-dinitrophenyl-spin-label monoclonal antibody Fab fragment with bound hapten. J. Mol. Biol. 221, 239-256.
41. Boehm, M. K., Corper, A. L., Wan, T., Sohi, M. K., Sutton, B. J., Thornton, J. P., Keep, P. A., Chester, K. A., Begent, R. H., and Perkins, S. J. (2000) Crystal structure of the anti-(carcinoembryonic antigen) single-chain Fv antibody MFE-23 and a model for antigen binding based on intermolecular contacts. Biochem. J. 346, 519-528.
42. Lindner, A. B., Eshhar, Z., and Tawfik, D. S. (1999) Conformational changes affect binding and catalysis by ester hydrolysing antibodies. J. Mol. Biol. 285, 421-430.
43. Hifumi, E., Hatiuchi, K., Okuda, T., Nichizono, A., Okamura, Y., and Uda, T. (2005) Specific degradation of H. pylori urease by a catalytic antibody light chain. FEBS J. 272, 4497-4505.
44. Gao, Q. S., Sun, M., Tyutyulkova, S., Webster, D., Rees, A., Tramontano, A., Massey, R. J., and Paul, S. (1994) Molecular cloning of a proteolytic antibody light chain. J. Biol. Chem. 269, 32389-32393.
45. Gibbs, R. A., Posner, B. A., Filpula, D. R., Dodd, S. W., Finkelman, M. A., Lee, T. K., Wroble, M., Whitlow, M., and Benkovic, S. J. (1991) Construction and characterization of a single-chain catalytic antibody. Proc. Natl. Acad. Sci. U.S.A. 88, 4001-4004.
46. Paul, S., Li, L., Kalaga, R., Wilkins-Stevens, P., Stevens, F. J., and Solomon, A. (1995) Natural catalytic antibodies: Peptide-hydrolyzing activities of Bence Jones proteins and VL fragment. J. Biol. Chem. 270, 15257-15261.
47. Schulze-Gahmen, U., Rini, J. M., and Wilson, I. A. (1993) Detailed analysis of the free and bound conformations of an antibody. X-ray structures of Fab 17/9 and three different Fab-peptide complexes. J. Mol. Biol. 234, 1098-1118.
48. Monsellier, E., and Bedouelle, H. (2006) Improving the stability of an antibody variable fragment by a combination of knowledge-based approaches: Validation and mechanisms. J. Mol. Biol. 362, 580-593.
49. Ponomarenko, N. A., Vorobiev, I. I., Alexandrova, E. S., Reshetnyak, A. V., Telegin, G. B., Khaidurov, S. V., Avalle, B., Karavanov, A., Morse, H. C., Thomas, D., Friboulet, A., and Gabibov, A. G. (2006) Induction of a protein-targeted catalytic response in autoimmune prone mice: Antibody-mediated cleavage of HIV-1 glycoprotein gp120. Biochemistry 45, 324-330.
50. Whitelegg, N. R. J., and Rees, A. R. (2000) WAM: An improved algorithm for modeling antibodies on the WEB. Protein Eng. 13, 819-824.
51. Yin, J., Mundorff, E. C., Yang, P. L., Wendt, K. U., Hanway, D., Stevens, R. C., and Schultz, P. G. (2001) A comparative analysis of the immunological evolution of antibody 28B4. Biochemistry 40, 10764-10773.
52. Yang, P. L., and Schultz, P. G. (1999) Mutational analysis of the affinity maturation of antibody 48G7. J. Mol. Biol. 294, 1191-1201.
53. Arkin, M. R., and Wells, J. A. (1998) Probing the importance of second sphere residues in an esterolytic antibody by phage display. J. Mol. Biol. 284, 1083-1094.