A novel molecular analysis of genes encoding catalytic antibodies

Molecular Immunology

Volumn 50, Issue 3, 2012, Pages 160-168

  Le Minoux, Damien ^a   Mahendra, Ankit ^b,c,d   Kaveri, Srini ^b,c,d   Limnios, Nikolaos ^e   Friboulet, Alain ^a   Avalle, Bérangère ^a   Boquet, Didier ^f   Lacroix Desmazes, Sébastien ^b,c,d   Padiolleau Lefèvre, Séverine ^a  

^a UNIVERSITÉ DE TECHNOLOGIE DE COMPIÈGNE   (France)

^b CENTRE DE RECHERCHE DES CORDELIERS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d INDIAN COUNCIL OF MEDICAL RESEARCH   (India)

^e UNIVERSITÉ DE TECHNOLOGIE DE COMPIÈGNE   (France)

^f Service de Pharmacologie et Immunoanalyse   (France)

Author keywords

Abzymes; Autoimmune diseases; Catalytic antibodies; Germlines; Somatic hypermutations

Indexed keywords

AMINO ACID; CATALYTIC ANTIBODY;

ARTICLE; AUTOIMMUNE DISEASE; BINDING AFFINITY; CHEMICAL MODIFICATION; ENZYME ACTIVITY; GENE FREQUENCY; GENETIC ANALYSIS; GERMLINE MICRONUCLEUS; HUMAN; MATURATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; SOMATIC HYPERMUTATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, CATALYTIC; MICE; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, PROTEIN; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN;

EID: 84857363742     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2012.01.004     Document Type: Article

References (80)

1. Aggarwal R., Benedetti F., Berti F., Buchini S., Colombatti A., Dinon F., Galasso V., Norbedo S. A catalytic antibody programmed for torsional activation of amide bond hydrolysis. Chemistry 2003, 9:3132-3142.
2. Avalle B., Thomas D., Friboulet A. Functional mimicry: elicitation of a monoclonal anti-idiotypic antibody hydrolyzing beta-lactams. FASEB J. 1998, 12:1055-1060.
3. Bangale Y., Karle S., Planque S., Zhou Y.X., Taguchi H., Nishiyama Y., Li L., Kalaga R., Paul S. VIPase autoantibodies in Fas-defective mice and patients with autoimmune disease. FASEB J. 2003, 17:628-635.
4. Barrera G.J., Portillo R., Mijares A., Rocafull M.A., del Castillo J.R., Thomas L.E. Immunoglobulin A with protease activity secreted in human milk activates PAR-2 receptors, of intestinal epithelial cells HT-29, and promotes beta-defensin-2 expression. Immunol. Lett. 2009, 123:52-59.
5. Belogurov A.J., Kozyr A., Ponomarenko N., Gabibov A. Catalytic antibodies: balancing between Dr. Jekyll and Mr. Hyde. Bioessays 2009, 31:1161-1171.
6. Berek C., Milstein C. Mutation drift and repertoire shift in the maturation of the immune response. Immunol. Rev. 1987, 96:23-41.
7. Brochet X., Lefranc M.P., Giudicelli V. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res. 2008, 36:W503-W508.
8. Brooks L., Suckling C.J., Stimson W.H. Construction of a single-chain Fv from an antibody which catalyses a Diels Alder cycloaddition. Biochem. Soc. Trans. 1996, 24:313.
9. Casali P., Notkins A.L. CD5+ B lymphocytes, polyreactive antibodies and the human B-cell repertoire. Immunol. Today 1989, 10:364-368.
10. Charbonnier J.B., Carpenter E., Gigant B., Golinelli-Pimpaneau B., Eshhar Z., Green B.S., Knossow M. Crystal structure of the complex of a catalytic antibody Fab fragment with a transition state analog: structural similarities in esterase-like catalytic antibodies. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:11721-11725.
11. Debler E.W., Müller R., Hilvert D., Wilson I.A. An aspartate and a water molecule mediate efficient acid-base catalysis in a tailored antibody pocket. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:18539-18544.
12. D'Souza L.J., Gigant B., Knossow M., Green B.S. Remarkable remote chiral recognition in a reaction mediated by a catalytic antibody. J. Am. Chem. Soc. 2002, 124:2114-2115.
13. Durova O.M., Vorobiev I.I., Smirnov I.V., Reshetnyak A.V., Telegin G.B., Shamborant O.G., Orlova N.A., Genkin D.D., Bacon A., Ponomarenko N.A., Friboulet A., Gabibov A.G. Strategies for induction of catalytic antibodies toward HIV-1 glycoprotein gp120 in autoimmune prone mice. Mol. Immunol. 2009, 47:87-95.
14. Ehrenmann F., Kaas Q., Lefranc M.P. IMGT/3D structure-DB and IMGT/DomainGapAlign: a database and a tool for immunoglobulins or antibodies, T cell receptors, MHC, IgSF and MhcSF. Nucleic Acids Res. 2010, 38:D301-D307.
15. Ehrenmann F., Lefranc M.P. IMGT/DomainGapAlign: IMGT standardized analysis of amino acid sequences of variable, constant, and groove domains (IG, TR, MH, IgSF, MhSF). Cold Spring Harb Protoc 2011, (6):737-749. 10.1101/pdb.prot5636.
16. Erhan S., Greller L.D. Do immunoglobulins have proteolytic activity?. Nature 1974, 251:353-355.
17. Ganesh K., Neuberger M.S. The relationship between hypothesis and experiment in unveiling the mechanisms of antibody gene diversification. FASEB J. 2011, 25:1123-1132.
18. Gao Q.S., Sun M., Tyutyulkova S., Webster D., Rees A., Tramontano A., Massey R.J., Paul S. Molecular cloning of a proteolytic antibody light chain. J. Biol. Chem. 1994, 269:32389-32393.
19. Gigant B., Charbonnier J.B., Eshhar Z., Green B.S., Knossow M. Crossreactivity, efficiency and catalytic specificity of an esterase-like antibody. J. Mol. Biol. 1998, 284:741-750.
20. Gigant B., Tsumuraya T., Fujii I., Knossow M. Diverse structural solutions to catalysis in a family of antibodies. Structure 1999, 7:1385-1393.
21. Giudicelli V., Brochet X., Lefranc M.P. IMGT/V-QUEST: IMGT standardized analysis of the immunoglobulin (IG) and T cell receptor (TR) nucleotide sequences. Cold Spring Harb. Protoc. 2011, (6):695-715. 10.1101/pdb.prot5633.
22. Golinelli-Pimpaneau B., Lüthi C., Christen P. Structural basis for d-amino acid transamination by the pyridoxal 5'-phosphate-dependent catalytic antibody 15A9. J. Biol. Chem. 2006, 281:23969-23977.
23. Gololobov G., Sun M., Paul S. Innate antibody catalysis. Mol. Immunol. 1999, 36:1215-1222.
24. Hifumi E., Hatiuchi K., Okuda T., Nishizono A., Okamura Y., Uda T. Specific degradation of H. pylori urease by a catalytic antibody light chain. FEBS J. 2005, 272:4497-4505.
25. Hifumi E., Mitsuda Y., Ohara K., Uda T. Targeted destruction of the HIV-1 coat protein gp41 by a catalytic antibody light chain. J. Immunol. Methods 2002, 269:283-298.
26. Hifumi E., Morihara F., Hatiuchi K., Okuda T., Nishizono A., Taizo U. Catalytic features and eradication ability of antibody light-chain UA15-L against Helicobacter pylori. J. Biol. Chem. 2008, 283:899-907.
27. Hifumi E., Yamada Y., Uda T. A catalytic antibody heavy chain HpU-2 degrading its epitope peptide and H. pylori urease. Immunol. Lett. 2006, 103:68-74.
28. Hoel P.G., Port S.C., Stone C.J. Introduction to Statistical Theory 1971, Houghton Mifflin Co., Boston.
29. Hotta K., Lange H., Tantillo D.J., Houk K.N., Hilvert D., Wilson I.A. Catalysis of decarboxylation by a preorganized heterogeneous microenvironment: crystal structures of abzyme 21D8. J. Mol. Biol. 2000, 302:1213-1225.
30. Hugot M., Bensel N., Vogel M., Reymond M.T., Stadler B., Reymond J.L., Baumann U. A structural basis for the activity of retro-Diels-Alder catalytic antibodies: evidence for a catalytic aromatic residue. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:9674-9678.
31. Kalaga R., Li L., O'Dell J.R., Paul S. Unexpected presence of polyreactive catalytic antibodies in IgG from unimmunized donors and decreased levels in rheumatoid arthritis. J. Immunol. 1995, 155:2695-2702.
32. 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., Kim Y.S. Heavy and light chain variable single domains of an anti-DNA binding antibody hydrolyze both double- and single-stranded dans without sequence specificity. J. Biol. Chem. 2006, 281:15287-15295.
33. Kit Y.Y., Semenov D.V., Nevinsky G.A. Phosphorylation of different human milk proteins by human catalytic secretory immunoglobulin A. Biochem. Mol. Biol. Int. 1996, 39:521-527.
34. 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., Friboulet A. Enzyme mimicry by the antiidiotypic antibody approach. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:13526-13531.
35. Lefranc M.-P. IMGT Collier de Perles for the variable (V), constant (C), and groove (G) domains of IG, TR, MH, IgSF, and MhSF. Cold Spring Harb. Protoc. 2011, 10.1101/pdb.ip86.
36. ®. Nucleic Acids Res. 2009, 37:D1006-D1012.
37. Lefranc M.P., Lefranc G. The Immunoglobulin Facts Book 2001, Academic Press, 458 p.
38. Lefranc M.-P., Pommié C., Ruiz M., Giudicelli V., Foulquier E., Truong L., Thouvenin-Contet V., Lefranc G. IMGT unique numbering for immunoglobulin and T cell receptor variable domains and Ig superfamily V-like domains. Dev. Comp. Immunol. 2003, 27:55-77.
39. Lerner R.A. Rare antibodies from combinatorial libraries suggest an S.O.S. componant of the human immunological repertoire. Mol. Biosyst. 2011, 7:1004-1012.
40. Ma B., Nussinov R. Enzyme dynamics point to stepwise conformational selection in catalysis. Curr. Opin. Chem. Biol. 2010, 14:652-659.
41. McKenzie K.M., Mee J.M., Rogers C.J., Hixon M.S., Kaufmann G.F., Janda K.D. Identification and characterization of single chain anti-cocaine catalytic antibodies. J. Mol. Biol. 2007, 365:722-731.
42. Mitsuda Y., Hifumi E., Tsuruhata K., Fujinami H., Yamamoto N., Uda T. Catalytic antibody light chain capable of cleaving a chemokine receptor CCR-5 peptide with a high reaction rate constant. Biotechnol. Bioeng. 2004, 86:217-225.
43. Oda M., Ito N., Tsumuraya T., Suzuki K., Sakakura M., Fujii I. Thermodynamic and structural basis for transition-state stabilization in antibody-catalyzed hydrolysis. J. Mol. Biol. 2007, 369:198-209.
44. Patten P.A., Gray N.S., Yang P.L., Marks C.B., Wedemayer G.J., Boniface J.J., Stevens R.C., Schultz P.G. The immunological evolution of catalysis. Science 1996, 271:1086-1091.
45. Paul S., Karle S., Planque S., Taguchi H., Salas M., Nishiyama Y., Handy B., Hunter R., Edmundson A., Hanson C. Naturally occurring proteolytic antibodies: selective immunoglobulin M-catalyzed hydrolysis of HIV gp120. J. Biol. Chem. 2004, 279:39611-39619.
46. Paul S., Nishiyama Y., Planque S., Taguchi H. Theory of prroteolytic antibody occurrence. Immunol. Lett. 2006, 103:8-16.
47. Paul S., Tramontano A., Gololobov G., Zhou Y.X., Taguchi H., Karle S., Nishiyama Y., Planque S., George S. Phosphonate ester probes for proteolytic antibodies. J. Biol. Chem. 2001, 276:28314-28320.
48. Pillet D., Paon M., Vorobiev I.I., Gabibov A.G., Thomas D., Friboulet A. Idiotypic network mimicry and antibody catalysis: lessons for the elicitation of efficient anti-idiotypic protease antibodies. J. Immunol. Lett. 2002, 269:5-12.
49. Planque S., Bangale Y., Song X.T., Karle S., Taguchi H., Poindexter B., Bick R., Edmundson A., Nishiyama Y., Paul S. Ontogeny of proteolytic immunity: IgM serine proteases. J. Biol. Chem. 2004, 279:14024-14032.
50. Pollack S.J., Jacobs J.W., Schultz P.G. Selective chemical catalysis by an antibody. Science 1986, 234:1570-1573.
51. Ponomarenko N.A., Durova O.M., Vorobiev I.I., Aleksandrova E.S., Telegin G.B., Chamborant O.G., Sidorik L.L., Suchkov S.V., Alekberova Z.S., Gnuchevf N.V., Gabibov A.G. Catalytic antibodies in clinical and experimental pathology: human and mouse models. J. Immunol. Methods 2002, 269:197-211.
52. Ponomarenko N.A., Durova O.M., Vorobiev I.I., Belugorov A.A., Kurkova I.N., Petrenko A.G., Telegin G.B., Suchkov S.V., 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., Gabibov A.A. Autoantibodies to myelin basic protein catalyze site-specific degradation of their antigen. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:281-286.
53. Poulsen T.R., Meijer P.J., Jensen A., Nielsen N.S., Andersen P.S. Kinetic, affinity, and diversity limits of human polyclonal antibody responses against tetanus toxois. J. Immunol. 2007, 179:3841-3850.
54. Ramsland P.A., Terzyan S.S., Cloud G., Bourne C.R., Farrugia W., Tribbick G., Geysen H.M., Moomaw C.R., Slaughter C.A., Edmundson A.B. Crystal structure of a glycosylated Fab from an IgM cryoglobulin with properties of a natural proteolytic antibody. Biochem. J. 2006, 395:473-481.
55. Romesberg F.E., Spiller B., Schultz P.G., Stevens R.C. Immunological origins of binding and catalysis in a Diels-Alderase antibody. Science 1998, 279:1929-1933.
56. Sharma V., Heriot W., Trisler K., Smider V. A human germline antibody light chain with hydrolytic properties associated with multimerization status. J. Biol. Chem. 2009, 284:33079-33087.
57. Shuster A.M., Gololobov G.V., Kvashuk O.A., Bogomolova A.E., Smirnov I.V., Gabibov A.G. DNA hydrolyzing autoantibodies. Science 1992, 256:665-667.
58. Smirnov I., Carletti E., Kurkova I., Nachon F., Nicolet Y., Mitkevitch V.A., Débat H., Avalle B., Belogurov A.A., Kuznetsov N., Reshetnyak A., Masson P., Tonevitsky A.G., Ponomarenko N., Makarov A.A., Friboulet A., Tramontano A., Gabibov A. Reactibodies generated by kinetic selection couple chemical reactivity with favorable protein dynamics. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:15954-15959.
59. Sun J., Takahashi N., Kakinuma H., Nishi Y. Molecular evolution of catalytic antibodies in autoimmune mice. J. Immunol. 2001, 167:5775-5785.
60. Taguchi H., Planque S., Sapparapu G., Boivin S., Hara M., Nishiyama Y., Sudhir P. Exceptional amyloid beta peptide hydrolyzing activity of nonphysiological immunoglobulin variable domain scaffolds. J. Biol. Chem. 2008, 283:36724-36733.
61. Tanaka F., Almer H., Lerner R.A., Barbas C.F Catalytic single-chain antibodies possessing β-lactamase activity selected from a phage-displayed combinatorial library using a mechanism-based inhibitor. Tetrahedron Lett. 1999, 40:8063-8066.
62. Tawfik D.S., Chap R., Green B.S., Sela M., Eshhar Z. Unexpectedly high occurrence of catalytic antibodies in MRL/lpr and SJL mice immunized with a transition-state analog: is there a linkage to autoimmunity?. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:2145-2149.
63. Thayer M.M., Olender E.H., Arvai A.S., Koike C.K., Canestrelli I.L., Stewart J.D., Benkovic S.J., Getzoff E.D., Roberts V.A. Structural basis for amide hydrolysis catalyzed by the 43C9 antibody. J. Mol. Biol. 1999, 291:329-345.
64. Tramontano A., Janda K.J., Lerner R. Chemical reactivity at an antibody binding site elicited by mechanistic design of a synthetic antigen. Proc. Natl. Acad. Sci. U.S.A. 1986, 83:6736-6740.
65. Uda T., Hifumi E. Super catalytic antibody and antigenase. J. Biosci. Bioeng. 2004, 97:143-152.
66. Ulrich H.D., Mundorff E., Santarsiero B.D., Driggers E.M., Stevens R.C., Schultz P.G. The interplay between binding energy and catalysis in the evolution of a catalytic antibody. Nature 1997, 389:271-275.
67. Venkateshrao S., Yin J., Jarzecki A.A., Schultz P.G., Spiro T.G. Porphyrin distortion during affinity maturation of a ferrochelatase antibody, monitored by Resonance Raman spectroscopy. J. Am. Chem. Soc. 2004, 126:16361-16367.
68. Wang M., Rada C., Neuberger M.S. Altering the spectrum of immunoglobulin V gene somatic hypermutation by modifying the active site of AID. J. Exp. Med. 2010, 207:141-153.
69. Wedemayer G.J., Patten P.A., Wang L.H., Schultz P.G., Stevens R.C. Structural insights into the evolution of an antibody combining site. Science 1997, 276:1665-1669.
70. Wootla B., Christophe O.D., Mahendra A., Dimitrov J.D., Repessé Y., Ollivier V., Friboulet A., Borel-Derlon A., Levesque H., Borg J.Y., Andre S., Bayry J., Calvez T., Kaveri S.V., Lacroix-Desmazes S. Proteolytic antibodies activate factor IX in patients with acquired hemophilia. Blood 2011, 117:2257-2264.
71. Wootla B., Dasgupta S., Dimitrov J.D., Bayry J., Lévesque H., Borg J.Y., Borel-Delon A., Rao D.N., Friboulet A., Kaveri S.V., Lacroix-Desmazes S. Factor VIII hydrolysis mediated by anti-factor VIII autoantibodies in acquired hemophilia. J. Immunol. 2008, 180:7714-7720.
72. Xu J., Deng Q., Chen J., Houk K.N., Bartek J., Hilvert D., Wilson I.A. Evolution of shape complementary and catalytic efficiency from a primordial antibody template. Science 1999, 286:2345-2348.
73. Xu Y., Yamamoto N., Janda K.D. Catalytic antibodies: hapten design strategies and screening methods. Bioorg. Med. Chem. 2004, 12:5247-5268.
74. Yang P.L., Schultz P.G. Mutational analysis of the affinity maturation of antibody 48G7. J. Mol. Biol. 1999, 294:1191-1201.
75. Zein H.S., Teixeira da Silva J.A., Miyatake K. Structure-function analysis and molecular modeling of DNase catalytic antibodies. Immunol. Lett. 2010, 129:13-22.
76. Zein H.S., Teixeira da Silva J.A., Miyatake K. Molecular analysis of multicatalytic monoclonal antibodies. Mol. Immunol. 2010, 47:1747-1756.
77. Zheng L., Goddard J.P., Baumann U., Reymond J.L. Expression improvement and mechanistic study of the retro-Diels-Alderase catalytic antibody 10F11 by site-directed mutagenesis. J. Mol. Biol. 2004, 341:807-814.
78. Zhou G.W., Guo J., Huang W., Fletterick R.J., Scanlan T.S. Crystal structure of a catalytic antibody with a serine protease active site. Science 1994, 265:1059-1064.
79. Zhou Z.H., Tzioufas A.G., Notkins A.L. Properties and function of polyreactive antibodies and polyreactive antigen-binding B cells. J. Autoimmun. 2007, 29:219-228.
80. Zhu X., Wentworth P., Wentworth A.D., Eschenmoser A., Lerner R.A., Wilson I.A. Probing the antibody-catalyzed water-oxidation pathway at atomic resolution. Proc. Natl. Acad. Sci. U.S.A. 2004, 110:2247-2252.