Antibody recognition of a unique tumor-specific glycopeptide antigen

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 22, 2010, Pages 10056-10061

  Brooks, Cory L ^a   Schietinger, Andrea ^b,c   Borisova, Svetlana N ^a   Kufer, Peter ^d   Okon, Mark ^e   Hirama, Tomoko ^f   MacKenzie, C Roger ^f   Wang, Lai Xi ^g   Schreiber, Hans ^b   Evansa, Stephen V ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF MUNICH   (Germany)

^d MICROMET AG   (Germany)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^f NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^g UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Affinity maturation; Crystal structure; X ray crystallography

Indexed keywords

EPITOPE; GLYCOPEPTIDE; MONOCLONAL ANTIBODY; TUMOR ANTIGEN;

ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; ANTIBODY STRUCTURE; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ARTICLE; CARBOHYDRATE ANALYSIS; CONTROLLED STUDY; CROSS REACTION; GERM LINE; GLYCOSYLATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; ANTIGEN-ANTIBODY COMPLEX; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; CRYSTALLOGRAPHY, X-RAY; EPITOPES; GLYCOPEPTIDES; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; MICE; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; STATIC ELECTRICITY; SURFACE PLASMON RESONANCE;

EID: 77953384504     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0915176107     Document Type: Article

References (54)

1. Schietinger A, Philip M, Schreiber H (2008) Specificity in cancer immunotherapy. Semin Immunol 20:276-285.
2. Kim YJ, Varki A (1997) Perspectives on the significance of altered glycosylation of glycoproteins in cancer. Glycoconjugate J 14:569-576.
3. Livingston PO (1995) Augmenting the immunogenicity of carbohydrate tumor antigens. Semin Cancer Biol 6:357-366.
4. Carbone FR, Gleeson PA (1997) Carbohydrates and antigen recognition by T cells. Glycobiology 7:725-730.
5. Hanisch FG, Ninkovic T (2006) Immunology of O-glycosylated proteins: approaches to the design of a MUC1 glycopeptide-based tumor vaccine. Curr Protein Pept Sci 7:307-315. (Pubitemid 44237140)
6. Freire T, Bay S, von Mensdorff-Pouilly S, Osinaga E (2005) Molecular basis of incomplete O-glycan synthesis in MCF-7 breast cancer cells: Putative role of MUC6 in Tn antigen expression. Cancer Res 65:7880-7887. (Pubitemid 41297265)
7. Ohshio G, et al. (1995) Distribution of Tn antigen recognized by an anti-Tn monoclonal antibody (MLS128) in normal and malignant tissues of the digestive tract. J Cancer Res Clin Oncol 121:247-252.
8. Kanitakis J, al-Rifai I, Faure M, Claudy A (1998) Differential expression of the cancer associated antigens T (Thomsen-Friedenreich) and Tn to the skin in primary and metastatic carcinomas. J Clin Pathol 51:588-592.
9. Lo-Man R, et al. (2004) A fully synthetic therapeutic vaccine candidate targeting carcinoma-associated Tn carbohydrate antigen induces tumor-specific antibodies in nonhuman primates. Cancer Res 64:4987-4994. (Pubitemid 38924547)
10. Stepensky D, Tzehoval E, Vadai E, Eisenbach L (2006) O-glycosylated versus nonglycosylated MUC1-derived peptides as potential targets for cytotoxic immunotherapy of carcinoma. Clin Exp Immunol 143:139-149.
11. Babino A, et al. (1997) Molecular cloning of a monoclonal anti-tumor antibody specific for the Tn antigen and expression of an active single-chain Fv fragment. Hybridoma 16:317-324. (Pubitemid 27410600)
12. Duk M, Lisowska E (1998) Purification of human anti-TF (Thomsen-Friedenreich) and anti-Tn antibodies by affinity chromatography on glycophorin A derivatives and characterization of the antibodies by microtiter plate ELISA. Arch Immunol Ther Ex 46:69-77. (Pubitemid 128516980)
13. Jansson B, Borrebaeck CA (1992) The human repertoire of antibody specificities against Thomsen-Friedenreich and Tn-carcinoma-associated antigens as defined by human monoclonal antibodies. Cancer Immunol Immunother 34:294-298.
14. Oppezzo P, et al. (2000) Production and functional characterization of two mouse/human chimeric antibodies with specificity for the tumor-associated Tn-antigen. Hybridoma 19:229-239. (Pubitemid 30622624)
15. Springer GF, Chandrasekaran EV, Desai PR, Tegtmeyer H (1988) Blood group Tn-active macromolecules from human carcinomas and erythrocytes: Characterization of and specific reactivity with mono- and poly-clonal anti-Tn antibodies induced by various immunogens. Carbohydr Res 178:271-292.
16. Springer GF, Desai PR (1985) Tn epitopes, immunoreactive with ordinary anti-Tn antibodies, on normal, desialylated human erythrocytes and on Thomsen-Friedenreich antigen isolated therefrom. Mol Immunol 22:1303-1310.
17. Zanetti M, Lenert G, Springer GF (1993) Idiotypes of pre-existing human anticarcinoma anti-T and anti-Tn antibodies. Int Immunol 5:113-119. (Pubitemid 23075513)
18. Babino A, et al. (2003) The crystal structure of a plant lectin in complex with the Tn antigen. FEBS Lett 536:106-110. (Pubitemid 36206415)
19. Yoshida T, et al. (2003) SRCL/CL-P1 recognizes GalNAc and a carcinoma-associated antigen, Tn antigen. J Biochem 133:271-277. (Pubitemid 36504393)
20. Dokurno P, et al. (1998) Crystal structure at 1.95 A resolution of the breast tumour-specific antibody SM3 complexed with its peptide epitope reveals novel hypervariable loop recognition. J Mol Biol 284:713-728. (Pubitemid 28550017)
21. Sorensen AL, et al. (2006) Chemoenzymatically synthesized multimeric Tn/STn MUC1 glycopeptides elicit cancer-specific anti-MUC1 antibody responses and override tolerance. Glycobiology 16:96-107.
22. Ward PL, Koeppen H, Hurteau T, Schreiber H (1989) Tumor antigens defined by cloned immunological probes are highly polymorphic and are not detected on autologous normal cells. J Exp Med 170:217-232. (Pubitemid 19179706)
23. Schietinger A, et al. (2006) A mutant chaperone converts a wild-type protein into a tumor-specific antigen. Science 314:304-308. (Pubitemid 44571976)
24. Raica M, Cimpean AM, Ribatti D (2008) The role of podoplanin in tumor progression and metastasis. Anticancer Res 28:2997-3006.
25. MacKenzie CR, et al. (1996) Analysis by surface plasmon resonance of the influence of valence on the ligand binding affinity and kinetics of an anti-carbohydrate antibody. J Biol Chem 271:1527-1533.
26. Okarvi SM, Jammaz IA (2009) Design, synthesis, radiolabeling and in vitro and in vivo characterization of tumor-antigen- and antibody-derived peptides for the detection of breast cancer. Anticancer Res 29:1399-1409.
27. Wuthrich K, Billeter M, Braun W (1984) Polypeptide secondary structure determination by nuclear magnetic resonance observation of short proton-proton distances. J Mol Biol 180:715-740.
28. Davies DR, Cohen GH (1996) Interactions of protein antigens with antibodies. Proc Natl Acad Sci USA 93:7-12.
29. Slovin SF, Keding SJ, Ragupathi G (2005) Carbohydrate vaccines as immunotherapy for cancer. Immunol Cell Biol 83:418-428.
30. Burchell J, et al. (1987) Development and characterization of breast cancer reactive monoclonal antibodies directed to the core protein of the human milk mucin. Cancer Res 47:5476-5482. (Pubitemid 17152966)
31. Blumenfeld OO, Adamany AM (1978) Structural polymorphism within the aminoterminal region of MM, NN, and MN glycoproteins (glycophorins) of the human erythrocyte membrane. Proc Natl Acad Sci USA 75:2727-2731.
32. Hirohashi S, Clausen H, Yamada T, Shimosato Y, Hakomori S (1985) Blood group A cross-reacting epitope defined by monoclonal antibodies NCC-LU-35 and -81 expressed in cancer of blood group O or B individuals: Its identification as Tn antigen. Proc Natl Acad Sci USA 82:7039-7043. (Pubitemid 16209687)
33. Taylor-Papadimitriou J, Epenetos AA (1994) Exploiting altered glycosylation patterns in cancer: Progress and challenges in diagnosis and therapy. Trends Biotechnol 12:227-233. (Pubitemid 24190550)
34. Moller H, Serttas N, Paulsen H, Burchell JM, Taylor-Papadimitriou J (2002) NMR-based determination of the binding epitope and conformational analysis of MUC-1 glycopeptides and peptides bound to the breast cancer-selective monoclonal antibody SM3. Eur J Biochem 269:1444-1455. (Pubitemid 34227085)
35. Spencer DI, et al. (1999) Structure/activity studies of the anti-MUC1 monoclonal antibody C595 and synthetic MUC1 mucin-core-related peptides and glycopeptides. Biospectroscopy 5:79-91.
36. Daugherty PS, Chen G, Iverson BL, Georgiou G (2000) Quantitative analysis of the effect of the mutation frequency on the affinity maturation of single chain Fv antibodies. Proc Natl Acad Sci USA 97:2029-2034. (Pubitemid 30134016)
37. England P, Nageotte R, Renard M, Page AL, Bedouelle H (1999) Functional characterization of the somatic hypermutation process leading to antibody D1.3, a high affinity antibody directed against lysozyme. J Immunol 162:2129-2136. (Pubitemid 29288834)
38. Zahnd C, et al. (2004) Directed in vitro evolution and crystallographic analysis of a peptide-binding single chain antibody fragment (scFv) with low picomolar affinity. J Biol Chem 279:18870-18877. (Pubitemid 38623314)
39. Acierno JP, Braden BC, Klinke S, Goldbaum FA, Cauerhff A (2007) Affinity maturation increases the stability and plasticity of the Fv domain of anti-protein antibodies. J Mol Biol 374:130-146. (Pubitemid 47600230)
40. Wedemayer GJ, Patten PA, Wang LH, Schultz PG, Stevens RC (1997) Structural insights into the evolution of an antibody combining site. Science 276(5319):1665-1669.
41. Yang PL, Schultz PG (1999) Mutational analysis of the affinity maturation of antibody 48G7. J Mol Biol 294:1191-1201.
42. Springer GF (1997) Immunoreactive T and Tn epitopes in cancer diagnosis, prognosis, and immunotherapy. J Mol Med 75:594-602.
43. Reed W, Bryne M, Clausen H, Dabelsteen E, Nesland JM (1994) Simple mucins (T, sialosyl-T, Tn and sialosyl-Tn) are not diagnostic for malignant breast lesions. Anticancer Res 14:609-615. (Pubitemid 24172180)
44. Schmitt FC, Figueiredo P, Lacerda M (1995) Simple mucin-type carbohydrate antigens (T, sialosyl-T, Tn and sialosyl-Tn) in breast carcinogenesis. Virchows Arch 427:251-258.
45. Manimala JC, Li Z, Jain A, VedBrat S, Gildersleeve JC (2005) Carbohydrate array analysis of anti-Tn antibodies and lectins reveals unexpected specificities: implications for diagnostic and vaccine development. Chembiochem 6:2229-2241. (Pubitemid 46259999)
46. Nakada H, et al. (1993) Epitopic structure of Tn glycophorin A for an anti-Tn antibody (MLS 128). Proc Natl Acad Sci USA 90:2495-2499. (Pubitemid 23078654)
47. Hakomori S (2001) Tumor-associated carbohydrate antigens defining tumor malignancy: Basis for development of anti-cancer vaccines. Adv Exp Med Biol 491:369-402.
48. Lorimer IA (2002) Mutant epidermal growth factor receptors as targets for cancer therapy. Curr Cancer Drug Tar 2:91-102. (Pubitemid 34625478)
49. Kobata A, Amano J (2005) Altered glycosylation of proteins produced by malignant cells, and application for the diagnosis and immunotherapy of tumours. Immunol Cell Biol 83:429-439. (Pubitemid 41044621)
50. Ju T, et al. (2008) Human tumor antigens Tn and sialyl Tn arise from mutations in Cosmc. Cancer Res 68:1636-1646. (Pubitemid 351416547)
51. Ju T, Cummings RD (2005) Protein glycosylation: Chaperone mutation in Tn syndrome. Nature 437:1252.
52. McCoy AJ, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40:658-674.
53. CCP4 (1994) The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D 50:760-763.
54. Adams PD, et al. (2002) PHENIX: Building new software for automated crystallographic structure determination. Acta Crystallogr D 58:1948-1954.