Minimizing immunogenicity of the SDR-grafted humanized antibody CC49 by genetic manipulation of the framework residues

Molecular Immunology

Volumn 40, Issue 6, 2003, Pages 337-349

  Gonzales, Noreen R ^a   Padlan, Eduardo A ^b,d   De Pascalis, Roberto ^a   Schuck, Peter ^c   Schlom, Jeffrey ^a   Kashmiri, S V S ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d University of the Philippines Diliman   (Philippines)

Author keywords

Antigen binding affinity; CDRs; Frameworks; HAMA response; Humanized antibody; Immunogenicity; Molecular biology; Specificity determining residues

Indexed keywords

GLYCOPROTEIN; HUMAN MONOCLONAL ANTIBODY CC49 V10; HUMAN MONOCLONAL ANTIBODY CC49 V35; HUMAN MONOCLONAL ANTIBODY CC49 V37; HUMAN MONOCLONAL ANTIBODY CC49 V40; HUMAN MONOCLONAL ANTIBODY CC49 V41; HUMAN MONOCLONAL ANTIBODY CC49 V47; HUMAN MONOCLONAL ANTIBODY CC49 V48; HUMAN MONOCLONAL ANTIBODY CC49 V58; HUMAN MONOCLONAL ANTIBODY CC49 V59; MONOCLONAL ANTIBODY CC49; TAG 72 ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBODY AFFINITY; ANTIBODY RESPONSE; ANTIGEN BINDING; ARTICLE; BINDING SITE; CHO CELL; COMPLEMENTARITY DETERMINING REGION; CONTROLLED STUDY; GENETIC MANIPULATION; HUMAN; IMMUNOGENICITY; IMMUNOGLOBULIN STRUCTURE; NONHUMAN; PRIORITY JOURNAL; SERUM; SITE DIRECTED MUTAGENESIS; SPECIFICITY DETERMINING RESIDUE; VALIDATION PROCESS;

ANIMALIA; MURINAE;

EID: 0141756310     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0161-5890(03)00166-4     Document Type: Article

References (59)

1. Abola E.E., Sussman J.L., Prilusky J., Manning N.O. Protein data bank archives of three-dimensional macromolecular structures. Methods Enzymol. 277:1997;556-571.
2. Abrantes M., Magone M.T., Boyd L.F., Schuck P. Adaptation of a surface plasmon resonance biosensor with microfluidics for use with small sample volumes and long contact times. Anal. Chem. 73:2001;2828-2835.
3. 177Lu -CC49: a phase I/II study Gynecol. Oncol. 65:1997;94-101.
4. Amit A.G., Mariuzza R.A., Phillips S.E., Poljak R.J. Three-dimensional structure of an antigen-antibody complex at 2.8 A resolution. Science. 233:1986;747-753.
5. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
6. Carter P. Improving the efficacy of antibody-based cancer therapies. Nat. Rev. Cancer. 1:2001;118-129.
7. Chothia C., Lesk A.M. Canonical structures for the hypervariable regions of immunoglobulins. J. Mol. Biol. 196:1987;901-917.
8. Chothia C., Lesk A.M., Tramontano A., Levitt M., Smith-Gill S.J., Air G., Sheriff S., Padlan E.A., Davies D., Tulip W.R.et al. Conformations of immunoglobulin hypervariable regions. Nature. 342:1989;877-883.
9. Chothia C., Gelfand I., Kister A. Structural determinants in the sequences of immunoglobulin variable domain. J. Mol. Biol. 278:1998;457-479.
10. Colman P.M., Laver W.G., Varghese J.N., Baker A.T., Tulloch P.A., Air G.M., Webster R.G. Three-dimensional structure of a complex of antibody with influenza virus neuraminidase. Nature. 326:1987;358-363.
11. Cote R.J., Houchens D.P., Hitchcock C.L., Saad A.D., Nines R.G., Greenson J.K., Schneebaum S., Arnold M.W., Martin E.W. Jr. Intraoperative detection of occult colon cancer micrometastases using 125 I-radiolabled monoclonal antibody CC49. Cancer. 77:1996;613-620.
12. Divgi C.R., Scott A.M., Dantis L., Capitelli P., Siler K., Hilton S., Finn R.D., Kemeny N., Kelsen D., Kostakoglu L.et al. Phase I radioimmunotherapy trial with iodine-131-CC49 in metastatic colon carcinoma. J. Nucl. Med. 36:1995a;586-592.
13. Divgi C.R., Scott A.M., Gulec S., Broussard E.K., Levy N., Young C., Capitelli P., Daghighian F., Williams J.M., Finn R.D.et al. Pilot radioimmunotherapy trial with 131I-labeled murine monoclonal antibody CC49 and deoxyspergualin in metastatic colon carcinoma. Clin. Cancer Res. 1:1995b;1503-1510.
14. Farah R.A., Clinchy B., Herrera L., Vitetta E.S. The development of monoclonal antibodies for the therapy of cancer. Crit. Rev. Eukaryot Gene Exp. 8:1998;321-356.
15. Fischmann T.O., Bentley G.A., Bhat T.N., Boulot G., Mariuzza R.A., Phillips S.E., Tello D., Poljak R.J. Crystallographic refinement of the three-dimensional structure of the FabD1.3-lysozyme complex at 2.5-A resolution. J. Biol. Chem. 266:1991;12915-12920.
16. Frankel M.E., Gerhard W. The rapid determination of binding constants for antiviral antibodies by a radioimmunoassay. An analysis of the interaction between hybridoma proteins and influenza virus. Mol. Immunol. 16:1979;101-106.
17. Gonzales N.R., Schuck P., Schlom J., Kashmiri S.V. Surface plasmon resonance-based competition assay to assess the sera reactivity of variants of humanized antibodies. J. Immunol. Methods. 268:2002;197-210.
18. Haddad R., Avital S., Troitsa A., Chen J., Baratz M., Brazovsky E., Gitstein G., Kashtan H., Skornick Y., Schneebaum S. Benefits of radioimmunoguided surgery for pelvic recurrence. Eur. J. Surg. Oncol. 27:2001;298-301.
19. Hanisch F.G., Uhlenbruck G., Egge H., Peter-Katalinic J. A B72.3 second-generation-monoclonal antibody (CC49) defines the mucin-carried carbohydrate epitope Gal beta(1-3) [NeuAc alpha(2-6)]GalNAc. Biol. Chem. Hoppe Seyler. 370:1989;21-26.
20. Hearn M.T., Bethell G.S., Ayers J.S., Hancock W.S. Application of 1-1′-carbonyldiimidazole-activated agarose for the purification of proteins. II. The use of an activated matrix devoid of additional charged groups for the purification of thyroid proteins. J. Chromatogr. 185:1979;463-470.
21. Higuchi R., Krummel B., Saiki R.K. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res. 16:1988;7351-7367.
22. Ho S.N., Hunt H.D., Horton R.M., Pullen J.K., Pease L.R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 77:1989;51-59.
23. Holmes M.A., Buss T.N., Foote J. Structural effects of framework mutations on a humanized anti-lysozyme antibody. J. Immunol. 167:2001;296-301.
24. Huston J.S., George A.J. Engineered antibodies take center stage. Hum. Antibodies. 10:2001;127-142.
25. Iwahashi M., Milenic D.E., Padlan E.A., Bei R., Schlom J., Kashmiri S.V. CDR substitutions of a humanized monoclonal antibody (CC49): contributions of individual CDRs to antigen binding and immunogenicity. Mol. Immunol. 36:1999;1079-1091.
26. Johnsson B., Lofas S., Lindquist G. Immobilization of proteins to a carboxymethyldextran-modified gold surface for biospecific interaction analysis in surface plasmon resonance sensors. Anal. Biochem. 198:1991;268-277.
27. Kabat, E.A., Wu, T., Perry, H.M., Gottesman, K.S., Foeller, C., 1991. Sequence of proteins of immunological interests, fifth ed. NIH Publication No. 91-3242. US Department of Health and Human Services, National Institutes of Health, Bethesda, MD.
28. Kashmiri S.V., Shu L., Padlan E.A., Milenic D.E., Schlom J., Hand P.H. Generation, characterization, and in vivo studies of humanized anticarcinoma antibody CC49. Hybridoma. 14:1995;461-473.
29. Kashmiri S.V., Iwahashi M., Tamura M., Padlan E.A., Milenic D.E., Schlom J. Development of a minimally immunogenic variant of humanized anti-carcinoma monoclonal antibody CC49. Crit. Rev. Oncol. Hematol. 38:2001;3-16.
30. Kuroki M., Fernsten P.D., Wunderlich D., Colcher D., Simpson J.F., Poole D.J., Schlom J. Serological mapping of the TAG-72 tumor-associated antigen using 19 distinct monoclonal antibodies. Cancer Res. 50:1990;4872-4879.
31. Landt O., Grunert H.P., Hahn U. A general method for rapid site-directed mutagenesis using the polymerase chain reaction. Gene. 96:1990;125-128.
32. LaValle G.J., Martinez D.A., Sobel D., DeYoung B., Martin E.W. Jr. Assessment of disseminated pancreatic cancer: a comparison of traditional exploratory laparotomy and radioimmunoguided surgery. Surgery. 122:1997;867-871. (Discussion 871-3).
33. Liu T., Meredith R.F., Saleh M.N., Wheeler R.H., Khazaeli M.B., Plott W.E., Schlom J., LoBuglio A.F. Correlation of toxicity with treatment parameters for 131I-CC49 radioimmunotherapy in three phase II clinical trials. Cancer Biother. Radiopharm. 12:1997;79-87.
34. Macey D.J., Grant E.J., Kasi L., Rosenblum M.G., Zhang H.Z., Katz R.L., Rieger P.T., LeBherz D., South M., Greiner J.W., Schlom J., Podoloff D.A., Murray J.L. Effect of recombinant alpha-interferon on pharmacokinetics, biodistribution, toxicity, and efficacy of 131I-labeled monoclonal antibody CC49 in breast cancer: a phase II trial. Clin. Cancer Res. 3:1997;1547-1555.
35. McIntosh D.G., Colcher D., Seemayer T., Smith M.L. The intraoperative detection of ovarian adenocarcinoma using radiolabeled CC49 monoclonal antibody and a hand-held gamma-detecting probe. Cancer Biother. Radiopharm. 12:1997;287-294.
36. Meredith R.F., Khazaeli M.B., Plott W.E., Grizzle W.E., Liu T., Schlom J., Russell C.D., Wheeler R.H., LoBuglio A.F. Phase II study of dual 131I-labeled monoclonal antibody therapy with interferon in patients with metastatic colorectal cancer. Clin. Cancer Res. 2:1996a;1811-1818.
37. Meredith R.F., Partridge E.E., Alvarez R.D., Khazaeli M.B., Plott G., Russell C.D., Wheeler R.H., Liu T., Grizzle W.E., Schlom J., LoBuglio A.F. Intraperitoneal radioimmunotherapy of ovarian cancer with lutetium-177-CC49. J. Nucl. Med. 37:1996b;1491-1496.
38. Meredith R.F., Khazaeli M.B., Macey D.J., Grizzle W.E., Mayo M., Schlom J., Russell C.D., LoBuglio A.F. Phase II study of interferon-enhanced 131I-labeled high affinity CC49 monoclonal antibody therapy in patients with metastatic prostate cancer. Clin. Cancer Res. 5:1999;3254s-3258s.
39. Meredith R.F., Alvarez R.D., Partridge E.E., Khazaeli M.B., Lin C.Y., Macey D.J., Austin J.M. Jr., Kilgore L.C., Grizzle W.E., Schlom J., LoBuglio A.F. Intraperitoneal radioimmunochemotherapy of ovarian cancer: a phase I study. Cancer Biother. Radiopharm. 16:2001;305-315.
40. Morrison, S.L., Schlom, J., 1990. Recombinant chimeric monoclonal antibodies. Imp. Adv. Oncol. 3-18.
41. Mulligan T., Carrasquillo J.A., Chung Y., Milenic D.E., Schlom J., Feuerstein I., Paik C., Perentesis P., Reynolds J., Curt G.et al. Phase I study of intravenous Lu-labeled CC49 murine monoclonal antibody in patients with advanced adenocarcinoma. Clin. Cancer Res. 1:1995;1447-1454.
42. Muraro R., Kuroki M., Wunderlich D., Poole D.J., Colcher D., Thor A., Greiner J.W., Simpson J.F., Molinolo A., Noguchi P.et al. Generation and characterization of B72.3 second generation monoclonal antibodies reactive with the tumor-associated glycoprotein 72 antigen. Cancer Res. 48:1988;4588-4596.
43. Murray J.L., Macey D.J., Grant E.J., Rosenblum M.G., Kasi L.P., Zhang H.Z., Katz R.L., Riger P.T., LeBherz D., Bhadkamkar V.et al. Enhanced TAG-72 expression and tumor uptake of radiolabeled monoclonal antibody CC49 in metastatic breast cancer patients following alpha-interferon treatment. Cancer Res. 55:1995;5925s-5928s.
44. Nicolet C.M., Siegel D.H., Surfus J.E., Sondel P.M. TAG-72-reactive antibody CC49 recognizes molecules expressed by hematopoietic cell lines. Tumor Biol. 18:1997;356-366.
45. Padlan E.A. Anatomy of the antibody molecule. Mol. Immunol. 31:1994;169-217.
46. Padlan E.A., Abergel C., Tipper J.P. Identification of specificity-determining residues in antibodies. FASEB J. 9:1995;133-139.
47. Padlan E.A., Silverton E.W., Sheriff S., Cohen G.H., Smith-Gill S.J., Davies D.R. Structure of an antibody-antigen complex: crystal structure of the HyHEL-10 Fab-lysozyme complex. Proc. Natl. Acad. Sci. U.S.A. 86:1989;5938-5942.
48. Rucker R., Bresler H.S., Heffelfinger M., Kim J.A., Martin E.W. Jr., Triozzi P.L. Low-dose monoclonal antibody CC49 administered sequentially with granulocyte-macrophage colony-stimulating factor in patients with metastatic colorectal cancer. J. Immunother. 22:1999;80-84.
49. Ryu C.J., Padlan E.A., Jin B.R., Yoo O.J., Hong H.J. A humanized antibody with specificity for hepatitis B surface antigen. Hum. Antibodies Hybridomas. 7:1996;113-122.
50. Schneebaum S., Troitsa A., Avital S., Haddad R., Kashtan H., Gitstein G., Baratz M., Brazovsky E., Papo J., Skornick Y. Identification of lymph node metastases in recurrent colorectal cancer. Recent Results Cancer Res. 157:2000;281-292.
51. Schuck P. Use of surface plasmon resonance to probe the equilibrium and dynamic aspects of interactions between biological macromolecules. Annu. Rev. Biophys. Biomol. Struct. 26:1997;541-566.
52. Schuck, P., Boyd, L., Andersen, P., 1999. Measuring protein interactions by optical biosensor. Curr. Protocols Protein Sci. 2, 20.2.1-21.
53. Sheriff S., Silverton E.W., Padlan E.A., Cohen G.H., Smith-Gill S.J., Finzel B.C., Davies D.R. Three-dimensional structure of an antibody-antigen complex. Proc. Natl. Acad. Sci. U.S.A. 84:1987;8075-8079.
54. Slovin S.F., Scher H.I., Divgi C.R., Reuter V., Sgouros G., Moore M., Weingard K., Pettengall R., Imbriaco M., El-Shirbiny A., Finn R., Bronstein J., Brett C., Milenic D., Dnistrian A., Shapiro L., Schlom J., Larson S.M. Interferon-gamma and monoclonal antibody 131I-labeled CC49: outcomes in patients with androgen-independent prostate cancer. Clin. Cancer. Res. 4:1998;643-651.
55. Tamura M., Milenic D.E., Iwahashi M., Padlan E., Schlom J., Kashmiri S.V. Structural correlates of an anticarcinoma antibody: identification of specificity-determining residues (SDRs) and development of a minimally immunogenic antibody variant by retention of SDRs only. J. Immunol. 164:2000;1432-1441.
56. Tempero M., Leichner P., Dalrymple G., Harrison K., Augustine S., Schlam J., Anderson J., Wisecarver J., Colcher D. High-dose therapy with iodine-131-labeled monoclonal antibody CC49 in patients with gastrointestinal cancers: a phase I trial. J. Clin. Oncol. 15:1997;1518-1528.
57. Tramontano A., Chothia C., Lesk A.M. Framework residue 71 is a major determinant of the position and conformation of the second hypervariable region in the VH domains of immunoglobulins. J. Mol. Biol. 215:1990;175-182.
58. Tulip W.R., Varghese J.N., Laver W.G., Webster R.G., Colman P.M. Refined crystal structure of the influenza virus N9 neuraminidase-NC41 Fab complex. J. Mol. Biol. 227:1992;122-148.
59. Winter G., Harris W.J. Humanized antibodies. Immunol. Today. 14:1993;243-246.