Single cycle structure-based humanization of an anti-nerve growth factor therapeutic antibody

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Covaceuszach, Sonia ^a,b   Marinelli, Sara ^c   Krastanova, Ivet ^d   Ugolini, Gabriele ^a,g   Pavone, Flaminia ^b   Lamba, Doriano ^b   Cattaneo, Antonino ^e,f  

^a Lay Line Genomics SpA   (Italy)

^b CNR   (Italy)

^c CNR   (Italy)

^d SINCROTRONE TRIESTE   (Italy)

^e EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^f SCUOLA NORMALE SUPERIORE   (Italy)

^g Rotta Research Laboratorium   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY ALPHAD11; NERVE GROWTH FACTOR; UNCLASSIFIED DRUG; ANALGESIC AGENT; FORMALDEHYDE;

ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; CHRONIC PAIN; CONTROLLED STUDY; CRYSTAL STRUCTURE; DOSE RESPONSE; DRUG DETERMINATION; DRUG EFFECT; DRUG MECHANISM; DRUG POTENCY; DRUG STRUCTURE; IN VITRO STUDY; IN VIVO STUDY; NEUROPATHIC PAIN; NONHUMAN; RAT; SINGLE DRUG DOSE; AMINO ACID SEQUENCE; ANIMAL; ANTIBODY SPECIFICITY; CHEMICAL STRUCTURE; CHEMICALLY INDUCED DISORDER; CHEMISTRY; DRUG DESIGN; HUMAN; IMMUNOLOGY; MOLECULAR GENETICS; MOUSE; NEURALGIA; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

MUS; RATTUS; RODENTIA;

AMINO ACID SEQUENCE; ANALGESICS; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIBODY SPECIFICITY; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; FORMALDEHYDE; HUMANS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NERVE GROWTH FACTOR; NEURALGIA; PROTEIN CONFORMATION; RATS;

EID: 84857778236     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032212     Document Type: Article

References (78)

1. Levi-Montalcini R, (1987) The nerve growth factor 35 years later. Science 237: 1154-1162.
2. Bibel M, Barde YA, (2000) Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev 14: 2919-2937.
3. Chao MV, (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4: 299-309.
4. Levi-Montalcini R, Skaper SD, Dal Toso R, Petrelli L, Leon A, (1996) Nerve growth factor: from neurotrophin to neurokine. Trends Neurosci 19: 514-520.
5. Lewin GR, Rueff A, Mendell LM, (1994) Peripheral and central mechanisms of NGF-induced hyperalgesia. Eur J Neurosci 6: 1903-1912.
6. Pezet S, McMahon SB, (2006) Neurotrophins: mediators and modulators of pain. Annu Rev Neurosci 29: 507-538.
7. Krüttgen A, Schneider I, Weis J, (2006) The dark side of the NGF family: neurotrophins in neoplasias. Brain Pathol 16: 304-310.
8. Watson JJ, Allen SJ, Dawbarn D, (2008) Targeting nerve growth factor in pain: what is the therapeutic potential? BioDrugs 22: 349-359.
9. Aloe L, Tuveri MA, Carcassi U, Levi-Montalcini R, (1992) Nerve growth factor in the synovial fluid of patients with chronic arthritis. Arthritis Rheum 35: 351-355.
10. Miller LJ, Fischer KA, Goralnick SJ, Litt M, Burleson JA, et al. (2002) Nerve growth factor and chronic prostatitis/chronic pelvic pain syndrome. Urology 59: 603-608.
11. Svensson P, Cairns BE, Wang K, Arendt-Nielsen L, (2003) Injection of nerve growth factor into human masseter muscle evokes long-lasting mechanical allodynia and hyperalgesia. Pain 104: 241-247.
12. Einarsdottir E, Carlsson A, Minde J, Toolanen G, Svensson O, et al. (2004) A mutation in the nerve growth factor beta gene (NGFB) causes loss of pain perception. Hum Mol Genet 13: 799-805.
13. Carvalho OP, Thornton GK, Hertecant J, Houlden H, Nicholas AK, et al. (2011) A novel NGF mutation clarifies the molecular mechanism and extends the phenotypic spectrum of the HSAN5 neuropathy. J Med Genet 48: 131-135.
14. Indo Y, (2001) Molecular basis of congenital insensitivity to pain with anhidrosis (CIPA): mutations and polymorphisms in TRKA (NTRK1) gene encoding the receptor tyrosine kinase for nerve growth factor. Hum Mutat 18: 462-471.
15. Hefti FF, Rosenthal A, Walicke PA, Wyatt S, Vergara G, et al. (2006) Novel class of pain drugs based on antagonism of NGF. Trends Pharmacol Sci 27: 85-91.
16. Wood JN, (2010) Nerve growth factor and pain. N Engl J Med 363: 1572-1573.
17. Levi-Montalcini R, (1964) Growth control of nerve cells by a protein factor and its antiserum. Science 143: 105-110.
18. Cattaneo A, Rapposelli B, Calissano P, (1988) Three distinct types of monoclonal antibodies after long-term immunization of rats with mouse nerve growth factor. J Neurochem 50: 1003-1010.
19. Paoletti F, Covaceuszach S, Konarev PV, Gonfloni S, Malerba F, et al. (2009) Intrinsic structural disorder of mouse proNGF. Proteins 75: 990-1009.
20. Molnar M, Tongiorgi E, Avignone E, Gonfloni S, Ruberti F, et al. (1998) The effects of anti-nerve growth factor monoclonal antibodies on developing basal forebrain neurons are transient and reversible. Eur J Neurosci 10: 3127-3140.
21. Molnar M, Ruberti F, Cozzari C, Domenici L, Cattaneo A, (1997) A critical period in the sensitivity of basal forebrain cholinergic neurones to NGF deprivation. Neuroreport 8: 575-579.
22. Ruberti F, Bradbury A, Cattaneo A, (1993) Cloning and expression of an anti-nerve growth factor (NGF) antibody for studies using the neuroantibody approach. Cell Mol Neurobiol 13: 559-568.
23. Berardi N, Celerino A, Domenici L, Fagiolini M, Pizzorusso T, et al. (1994) Monoclonal antibodies to nerve growth factor affect the postnatal development of the visual system. Proc Natl Acad Sci USA 91: 684-688.
24. Garaci E, Aquaro S, Lamenta C, Amendola A, Spada M, et al. (2003) Anti-nerve growth factor antibody abrogates macrophage-mediated HIV-1 infection and depletion of CD4+ T lymphocytes in hu-SCID mice. Proc Natl Acad Sci USA 100: 8927-8932.
25. Capsoni S, Tiveron C, Vignone D, Amato G, Cattaneo A, (2010) Dissecting the involvement of tropomyosin-related kinase A and p75 neurotrophin receptor signaling in NGF deficit-induced neurodegeneration. Proc Natl Acad Sci USA 107: 12299-12304.
26. Covaceuszach S, Cassetta A, Cattaneo A, Lamba D, (2004) Purification, crystallization, X-ray diffraction analysis and phasing of a Fab fragment of monoclonal neuroantibody áD11 against nerve growth factor. Acta Crystallogr Sect D Biol Crystallogr 60: 1323-1327.
27. Covaceuszach S, Cassetta A, Koranev PV, Gonfloni S, Rudolph R, et al. (2008) Dissecting NGF interactions with TrkA and p75 receptors by structural and functional studies of an anti-NGF neutralizing antibody. J Mol Biol 381: 881-889.
28. Holland DR, Cousens LS, Meng W, Matthews BW, (1994) Nerve growth factor in different crystal forms displays structural flexibility and reveals zinc binding sites. J Mol Biol 239: 385-400.
29. Wiesmann C, Ultsch MH, Bass SH, de Vos AM, (1999) Crystal structure of nerve growth factor in complex with the ligand-binding domain of the TrkA receptor. Nature 401: 184-188.
30. Prlić A, Bliven S, Rose PW, Bluhm WF, Bizon C, et al. (2010) Pre-calculated protein structure alignments at the RCSB PDB website. Bioinformatics 26: 2983-2985.
31. Ye Y, Godzik A, (2003) Flexible structure alignment by chaining aligned fragment pairs allowing twists. Bioinformatics 19: 246-255.
32. DeLano WL, (2002) The PyMOL Molecular Graphics System Palo Alto, CA, USA DeLano Scientific LLC.
33. Chevalier S, Praloran V, Smith C, MacGrogan D, Ip NY, et al. (1994) Expression and functionality of the trkA proto-oncogene product/NGF receptor in undifferentiated hematopoietic cells. Blood 83: 1479-1485.
34. Bennett GJ, Xie YK, (1988) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33: 87-107.
35. Cattaneo A, Covaceuszach S, Lamba D, (2005) Methods for the humanization of antibodies and humanized antibodies thereby obtained. Patent WO/2005/061540.
36. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28: 235-242.
37. Diederichs K, (1995) Structural superposition of proteins with unknown alignment and detection of topological similarity using a six-dimensional search algorithm. Proteins 23: 187-195.
38. Faelber K, Kirchhofer D, Presta L, Kelley RF, Muller YA, (2001) The 1.85 Å resolution crystal structures of tissue factor in complex with humanized Fab D3H44 and of free humanized Fab D3H44: revisiting the solvation of antigen combining sites. J Mol Biol 313: 83-97.
39. Kabat EA, Wu TT, Perry HM, Gottesman KS, Foeller C, (1991) Sequences of Proteins of Immunological Interest. 5th Ed., United States Department of Health and Human Services, Public Health Service, National Institutes of Health, NIH Publication No. 91: 3242.
40. Makabe K, Nakanishi T, Tsumoto K, Tanaka Y, Kondo H, et al. (2008) Thermodynamic consequences of mutations in Vernier zone residues of a humanized anti-human epidermal growth factor receptor murine antibody, 528. J Biol Chem 283: 1156-1166.
41. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr Sect D Biol Crystallogr 54: 905-921.
42. Persic L, Roberts A, Wilton J, Cattaneo A, Bradbury A, et al. (1997) An integrated vector system for the eukaryotic expression of antibodies or their fragments after selection from phage display libraries. Gene 187: 9-18.
43. Greene LA, Tischler AS, (1976) Establishment of a noradrenergic clonal line of rat adrenal phaeochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA 73: 2424-2428.
44. Jones PT, Dear PH, Foote J, Neuberger MS, Winter G, (1986) Replacing the complementarity-determining regions in a human antibody with those from a mouse. Nature 321: 522-525.
45. Riechmann L, Clark M, Waldmann G, Winter G, (1988) Reshaping human antibodies for therapy. Nature 332: 323-327.
46. Verhoeyen M, Milstein C, Winter G, (1988) Reshaping human antibodies: grafting an antilysozyme activity. Science 239: 1534-1536.
47. Gorman SD, Clark MR, Routledge EG, Cobbold SP, Waldmann H, (1991) Reshaping a therapeutic CD4 antibody. Proc Natl Acad Sci USA 88: 4181-4185.
48. Tempest PR, Bremner P, Lambert M, Taylor G, Furze JM, et al. (1991) Reshaping a human monoclonal antibody to inhibit human respiratory syncytial virus infection in vivo. Biotechnology 9: 266-271.
49. Carter P, Presta L, Gorman CM, Ridgway JB, Henner D, et al. (1992) Humanization of an anti-p185HER2 antibody for human cancer therapy. Proc Natl Acad Sci USA 89: 4285-4289.
50. Foote J, Winter G, (1992) Antibody framework residues affecting the conformation of the hypervariable loops. J Mo Biol 224: 487-499.
51. Queen C, Schneider WP, Selick HE, Payne PW, Landolfi NF, et al. (1989) A humanized antibody that binds to the interleukin 2 receptor. Proc Natl Acad Sci USA 86: 10029-10033.
52. Co MS, Deschamps M, Whitley RJ, Queen C, (1991) Humanized antibodies for antiviral therapy. Proc Natl Acad Sci USA 88: 2869-2873.
53. Fan ZC, Shan L, Goldsteen BZ, Guddat LW, Thakur A, et al. (1999) Comparison of the three-dimensional structures of a humanized and a chimeric Fab of an anti-gamma-interferon antibody. J Mol Recognit 12: 19-32.
54. Sleiman-Haidar JN, Yuan Q-A, Zeng L, Snavely M, Luna X, et al. (2011) A universal combinatorial design of antibody framework to graft distinct CDR sequences; a bioinformatics approach. Proteins DOI:10.1002/prot.23246.
55. Riechmann L, Weill M, Cavanagh J, (1992) Improving the antigen affinity of an antibody Fv-fragment by protein design. J Mol Biol 224: 913-918.
56. Morea V, Tramontano A, Rustici M, Chothia C, Lesk AM, (1998) Conformations of the third hypervariable region in the VH domain of immunoglobulins. J Mol Biol 275: 269-294.
57. Shirai H, Kidera A, Nakamura H, (1996) Structural classification of CDR-H3 in antibodies. FEBS Lett 399: 1-8.
58. Shirai H, Kidera A, Nakamura H, (1999) H3-rules: identification of CDR-H3 structures in antibodies. FEBS Lett 455: 188-197.
59. Zemlin M, Klinger M, Link J, Zemlin C, Bauer K, et al. (2003) Expressed murine and human CDR-H3 intervals of equal length exhibit distinct repertoires that differ in their amino acid composition and predicted range of structures. J Mol Biol 334: 733-749.
60. Chothia C, Lesk AM, Tramontano A, Levitt M, Smith-Gill SJ, et al. (1989) Conformations of immunoglobulin hypervariable regions. Nature 342: 877-883.
61. Chothia C, Lesk AM, Gherardi E, Tomlinson IM, Walter G, et al. (1992) Structural repertoire of the human VH segments. J Mol Biol 227: 799-817.
62. Kuroda D, Shirai H, Kobori M, Nakamura H, (2008) Structural classification of CDR-H3 revisited: a lesson in antibody modeling. Proteins 73: 608-20.
63. Banfield MJ, King DJ, Mountain A, Brady RL, (1997) VL:VH domain rotations in engineered antibodies: crystal structures of the Fab fragments from two murine antitumor antibodies and their engineered human constructs. Proteins 29: 161-171.
64. Pedersen JT, Henry AH, Searle SJ, Guild BC, Roguska M, et al. (1994) Comparison of surface accessible residues in human and murine immunoglobulin Fv domains. Implication for humanization of murine antibodies. J Mol Biol 235: 959-973.
65. Roguska MA, Pedersen JT, Keddy CA, Henry AH, Searle SJ, et al. (1994) Humanization of murine monoclonal antibodies through variable domain resurfacing. Proc Natl Acad Sci USA 91: 969-973.
66. Roguska MA, Pedersen JT, Henry AH, Searle SM, Roja CM, et al. (1996) A comparison of two murine monoclonal antibodies humanized by CDR-grafting and variable domain resurfacing. Protein Eng 9: 895-904.
67. Nicol GD, Vasko MR, (2007) Unraveling the story of NGF-mediated sensitization of nociceptive sensory neurons: ON or OFF the Trks? Mol Interv 7: 26-41.
68. He X, Garcia KC, (2004) Structure of nerve growth factor complexed with the shared neurotrophin receptor p75. Science 304: 870-875.
69. Wehrman T, He X, Raab B, Dukipatti A, Blau H, et al. (2007) Structural and mechanistic insights into nerve growth factor interactions with the TrkA and p75 receptors. Neuron 53: 25-38.
70. Abdiche YN, Malashock DS, Pons J, (2008) Probing the binding mechanism and affinity of tanezumab, a recombinant humanized anti-NGF monoclonal antibody, using a repertoire of biosensors. Protein Sci 17: 1326-1335.
71. Cattaneo A, Capsoni S, Margotti E, Righi M, Kontsekova E, et al. (1999) Functional blockade of tyrosine kinase A in the rat basal forebrain by a novel antagonistic anti-receptor monoclonal antibody. J Neurosci 19: 9687-9697.
72. Covaceuszach S, Cattaneo A, Lamba D, (2005) Neutralization of NGF-TrkA receptor interaction by the novel antagonistic anti-TrkA monoclonal antibody MNAC13: a structural insight. Proteins 58: 717-727.
73. Ugolini G, Marinelli S, Covaceuszach S, Cattaneo A, Pavone F, (2007) The function neutralizing anti-TrkA antibody MNAC13 reduces inflammatory and neuropathic pain. Proc Natl Acad Sci USA 104: 2985-2990.
74. Cattaneo A, (2010) Tanezumab, a recombinant humanized mAb against nerve growth factor for the treatment of acute and chronic pain. Curr Opin Mol Ther 12: 94-106.
75. Lane NE, Schnitzer TJ, Birbara CA, Mokhtarani M, Shelton DL, et al. (2010) Tanezumab for the treatment of pain from osteoarthritis of the knee. N Engl J Med 363: 1521-1531.
76. Kolbinger F, Saldanha J, Hardman N, Bendig MM, (1993) Humanization of a mouse anti-human IgE antibody: a potential therapeutic for IgE-mediated allergies. Protein Eng 6: 971-980.
77. Covaceuszach S, Capsoni S, Ugolini G, Spirito F, Vignone D, et al. (2009) Development of a non invasive NGF-based therapy for Alzheimer's disease. Curr Alzheimer Res 6: 158-170.
78. Zimmermann M, (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16: 109-110.