Structural biology of antibody recognition of carbohydrate epitopes and potential uses for targeted cancer immunotherapies

Molecular Immunology

Volumn 67, Issue 2, 2015, Pages 75-88

  Dingjan, Tamir ^a   Spendlove, Ian ^b   Durrant, Lindy G ^b   Scott, Andrew M ^c,d,e   Yuriev, Elizabeth ^a   Ramsland, Paul A ^a,d,f,g  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c OLIVIA NEWTON JOHN CANCER RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e LA TROBE UNIVERSITY   (Australia)

^f BURNET INSTITUTE   (Australia)

^g CURTIN UNIVERSITY   (Australia)

Author keywords

Antibody tumor targeting; Blood group carbohydrates; Cancer immunotherapy; Carbohydrate conformations; Carbohydrate recognition; Protein carbohydrate interactions

Indexed keywords

ANTIBODY; CARBOHYDRATE; CARBOHYDRATE ANTIGEN; EPITOPE; GLYCOLIPID; GLYCOPROTEIN; MONOCLONAL ANTIBODY; BLOOD GROUP LEWIS SYSTEM; LEWIS Y ANTIGEN;

ANTIBODY RECOGNITION; BINDING SITE; CANCER IMMUNOTHERAPY; CHEMICAL STRUCTURE; CONFORMATION; GLYCOSYLATION; HUMAN; IMMUNOLOGICAL PARAMETERS; NONHUMAN; PRIORITY JOURNAL; REVIEW; THREE DIMENSIONAL IMAGING; BLOOD GROUP LEWIS SYSTEM; CARBOHYDRATE ANALYSIS; CHEMISTRY; IMMUNOLOGY; IMMUNOTHERAPY; METABOLISM; MOLECULAR GENETICS; NEOPLASMS; PROCEDURES;

ANTIBODIES; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CARBOHYDRATES; EPITOPES; HUMANS; IMMUNOTHERAPY; LEWIS BLOOD-GROUP SYSTEM; MOLECULAR SEQUENCE DATA; NEOPLASMS;

EID: 84935084960     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2015.02.028     Document Type: Review

References (102)

1. Agostino M., Farrugia W., Sandrin M.S., Scott A.M., Yuriev E., Ramsland P.A. Structural Glycobiology of Antibody Recognition in Xenotransplantation and Cancer Immunotherapy 2012, 203-228. Springer, Wein, (Chapter 9). P. Kosma, S. Muller-Loennies (Eds.).
2. Agostino M., Yuriev E., Ramsland P.A. Antibody recognition of cancer-related gangliosides and their mimics investigated using in silico site mapping. PLoS ONE 2012, 7:e35457.
3. Agrawal P., Kurcon T., Pilobello K.T., Rakus J.F., Koppolu S., Liu Z., Batista B.S., Eng W.S., Hsu K.L., Liang Y., Mahal L.K. Mapping posttranscriptional regulation of the human glycome uncovers microRNA defining the glycocode. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:4338-4343.
4. Ahmed M., Goldgur Y., Hu J., Guo H.F., Cheung N.K. In silico driven redesign of a clinically relevant antibody for the treatment of GD2 positive tumors. PLoS ONE 2013, 8:e63359.
5. Ahmed M., Hu J., Cheung N.K. Structure based refinement of a humanized monoclonal antibody that targets tumor antigen disialoganglioside GD2. Front. Immunol. 2014, 5:372.
6. Ajani J.A., Kelsen D.P., Haller D., Hargraves K., Healey D. A multi-institutional phase II study of BMS-182248-01 (BR96-doxorubicin conjugate) administered every 21 days in patients with advanced gastric adenocarcinoma. Cancer J. 2000, 6:78-81.
7. Aziz F., Qiu Y. The role of anti-LeY antibody in the downregulation of MAPKs/COX-2 pathway in gastric cancer. Curr. Drug Targets 2014, 15:469-476.
8. Baker H.M., Basu I., Chung M.C., Caradoc-Davies T., Fraser J.D., Baker E.N. Crystal structures of the staphylococcal toxin SSL5 in complex with sialyl Lewis X reveal a conserved binding site that shares common features with viral and bacterial sialic acid binding proteins. J. Mol. Biol. 2007, 374:1298-1308.
9. Bara J., Gautier R., Daher N., Zaghouani H., Decaens C. Monoclonal antibodies against oncofetal mucin M1 antigens associated with precancerous colonic mucosae. Cancer Res. 1986, 46:3983-3989.
10. Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., Shindyalov I.N., Bourne P.E. The protein data bank. Nucleic Acids Res. 2000, 28:235-242.
11. Brockhausen I. Mucin-type O-glycans in human colon and breast cancer: glycodynamics and functions. EMBO Rep. 2006, 7:599-604.
12. Brockhausen I., Gao Y. Structural Glycobiology: Applications in Cancer Research 2012, 177-213. Taylor and Francis/CRC Press, London, (Chapter 8). E. Yuriev, P.A. Ramsland (Eds.).
13. Brodzik R., Glogowska M., Bandurska K., Okulicz M., Deka D., Ko K., van der Linden J., Leusen J.H., Pogrebnyak N., Golovkin M., Steplewski Z., Koprowski H. Plant-derived anti-Lewis Y mAb exhibits biological activities for efficient immunotherapy against human cancer cells. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:8804-8809.
14. Brooks C.L., Schietinger A., Borisova S.N., Kufer P., Okon M., Hirama T., Mackenzie C.R., Wang L.X., Schreiber H., Evans S.V. Antibody recognition of a unique tumor-specific glycopeptide antigen. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:10056-10061.
15. Buskas T., Thompson P., Boons G.J. Immunotherapy for cancer: synthetic carbohydrate-based vaccines. Chem. Commun. (Camb.) 2009, 5335-5349.
16. Cazet A., Julien S., Bobowski M., Burchell J., Delannoy P. Tumour-associated carbohydrate antigens in breast cancer. Breast Cancer Res. 2010, 12:204.
17. Cazet A., Julien S., Bobowski M., Krzewinski-Recchi M.A., Harduin-Lepers A., Groux-Degroote S., Delannoy P. Consequences of the expression of sialylated antigens in breast cancer. Carbohydr. Res. 2010, 345:1377-1383.
18. Chen Y., Tan M., Xia M., Hao N., Zhang X.C., Huang P., Jiang X., Li X., Rao Z. Crystallography of a Lewis-binding norovirus, elucidation of strain-specificity to the polymorphic human histo-blood group antigens. PLoS Pathog. 2011, 7:e1002152.
19. Chung M.C., Wines B.D., Baker H., Langley R.J., Baker E.N., Fraser J.D. The crystal structure of staphylococcal superantigen-like protein 11 in complex with sialyl Lewis X reveals the mechanism for cell binding and immune inhibition. Mol. Microbiol. 2007, 66:1342-1355.
20. Clarke K., Lee F.T., Brechbiel M.W., Smyth F.E., Old L.J., Scott A.M. Therapeutic efficacy of anti-Lewis(y) humanized 3S193 radioimmunotherapy in a breast cancer model: enhanced activity when combined with taxol chemotherapy. Clin. Cancer Res. 2000, 6:3621-3628.
21. Delbaere L.T., Vandonselaar M., Prasad L., Quail J.W., Wilson K.S., Dauter Z. Structures of the lectin IV of Griffonia simplicifolia and its complex with the Lewis b human blood group determinant at 2.0 A resolution. J. Mol. Biol. 1993, 230:950-965.
22. Devine P.L., McKenzie I.F. Mucins: structure, function, and associations with malignancy. Bioessays 1992, 14:619-625.
23. Dube V.E. The structural relationship of blood group-related oligosaccharides in human carcinoma to biological function: a perspective. Cancer Metast. Rev. 1987, 6:541-557.
24. Durrant L.G., Harding S.J., Green N.H., Buckberry L.D., Parsons T. A new anticancer glycolipid monoclonal antibody, SC104, which directly induces tumor cell apoptosis. Cancer Res. 2006, 66:5901-5909.
25. Durrant L.G., Noble P., Spendlove I. Immunology in the clinic review series; focus on cancer: glycolipids as targets for tumour immunotherapy. Clin. Exp. Immunol. 2012, 167:206-215.
26. Farhan H., Schuster C., Klinger M., Weisz E., Waxenecker G., Schuster M., Sexl V., Mudde G.C., Freissmuth M., Kircheis R. Inhibition of xenograft tumor growth and down-regulation of ErbB receptors by an antibody directed against Lewis Y antigen. J. Pharmacol. Exp. Ther. 2006, 319:1459-1466.
27. Farrugia W., Scott A.M., Ramsland P.A. A possible role for metallic ions in the carbohydrate cluster recognition displayed by a Lewis Y specific antibody. PLoS ONE 2009, 4:e7777.
28. Feil S.C., Lawrence S., Mulhern T.D., Holien J.K., Hotze E.M., Farrand S., Tweten R.K., Parker M.W. Structure of the lectin regulatory domain of the cholesterol-dependent cytolysin lectinolysin reveals the basis for its lewis antigen specificity. Structure 2012, 20:248-258.
29. Feinberg H., Taylor M.E., Weis W.I. Scavenger receptor C-type lectin binds to the leukocyte cell surface glycan Lewis(x) by a novel mechanism. J. Biol. Chem. 2007, 282:17250-17258.
30. Feizi T. Carbohydrate antigens in human cancer. Cancer Surv. 1985, 4:245-269.
31. Feridani A.H., Holmqvist B., Sjogren H.O., Strand S.E., Tennvall J., Baldetorp B. Combined flow cytometry and confocal laser scanning microscopy for evaluation of BR96 antibody cancer cell targeting and internalization. Cytometry A 2007, 71:361-370.
32. Guo Y., Feinberg H., Conroy E., Mitchell D.A., Alvarez R., Blixt O., Taylor M.E., Weis W.I., Drickamer K. Structural basis for distinct ligand-binding and targeting properties of the receptors DC-SIGN and DC-SIGNR. Nat. Struct. Mol. Biol. 2004, 11:591-598.
33. Hakomori S. Tumor-associated carbohydrate antigens defining tumor malignancy: basis for development of anti-cancer vaccines. Adv. Exp. Med. Biol. 2001, 491:369-402.
34. Hanai N., Nakamura K., Shitara K. Recombinant antibodies against ganglioside expressed on tumor cells. Cancer Chemother. Pharmacol. 2000, 46(Suppl):S13-S17.
35. Heimburg-Molinaro J., Lum M., Vijay G., Jain M.T., Almogren A., Rittenhouse-Olson K. Cancer vaccines and carbohydrate epitopes. Vaccine 2011, 29:8802-8826.
36. Hellstrom I., Garrigues H.J., Garrigues U., Hellstrom K.E. Highly tumor-reactive, internalizing, mouse monoclonal antibodies to Le(y)-related cell surface antigens. Cancer Res. 1990, 50:2183-2190.
37. Herbertson R.A., Tebbutt N.C., Lee F.T., MacFarlane D.J., Chappell B., Micallef N., Lee S.T., Saunder T., Hopkins W., Smyth F.E., Wyld D.K., Bellen J., Sonnichsen D.S., Brechbiel M.W., Murone C., Scott A.M. Phase I biodistribution and pharmacokinetic study of Lewis Y-targeting immunoconjugate CMD-193 in patients with advanced epithelial cancers. Clin. Cancer Res. 2009, 15:6709-6715.
38. Hermans S.J., Baker H.M., Sequeira R.P., Langley R.J., Baker E.N., Fraser J.D. Structural and functional properties of staphylococcal superantigen-like protein 4. Infect. Immun. 2012, 80:4004-4013.
39. Izawa M., Kumamoto K., Mitsuoka C., Kanamori C., Kanamori A., Ohmori K., Ishida H., Nakamura S., Kurata-Miura K., Sasaki K., Nishi T., Kannagi R. Expression of sialyl 6-sulfo Lewis X is inversely correlated with conventional sialyl Lewis X expression in human colorectal cancer. Cancer Res. 2000, 60:1410-1416.
40. Jeffrey P.D., Bajorath J., Chang C.Y., Yelton D., Hellstrom I., Hellstrom K.E., Sheriff S. The X-ray structure of an anti-tumour antibody in complex with antigen. Nat. Struct. Biol. 1995, 2:466-471.
41. Ju T., Otto V.I., Cummings R.D. The Tn antigen-structural simplicity and biological complexity. Angew. Chem. Int. Ed. Engl. 2011, 50:1770-1791.
42. Kaminski M.J., MacKenzie C.R., Mooibroek M.J., Dahms T.E., Hirama T., Houghton A.N., Chapman P.B., Evans S.V. The role of homophilic binding in anti-tumor antibody R24 recognition of molecular surfaces. Demonstration of an intermolecular beta-sheet interaction between vh domains. J. Biol. Chem. 1999, 274:5597-5604.
43. Kanazawa J., Ohta S., Shitara K., Fujita F., Fujita M., Hanai N., Akinaga S., Okabe M. Therapeutic potential of chimeric anti-(ganglioside GD3) antibody KM871: antitumor activity in xenograft model of melanoma and effector function analysis. Cancer Immunol. Immunother. 2000, 49:253-258.
44. Kannagi R. Carbohydrate antigen sialyl Lewis a - its pathophysiological significance and induction mechanism in cancer progression. Chang Gung Med. J. 2007, 30:189-209.
45. Kelly M.P., Lee F.T., Tahtis K., Smyth F.E., Brechbiel M.W., Scott A.M. Radioimmunotherapy with alpha-particle emitting 213Bi-C-functionalized trans-cyclohexyl-diethylenetriaminepentaacetic acid-humanized 3S193 is enhanced by combination with paclitaxel chemotherapy. Clin. Cancer Res. 2007, 13:5604s-5612s.
46. Kelly M.P., Lee S.T., Lee F.T., Smyth F.E., Davis I.D., Brechbiel M.W., Scott A.M. Therapeutic efficacy of 177Lu-CHX-A″-DTPA-hu3S193 radioimmunotherapy in prostate cancer is enhanced by EGFR inhibition or docetaxel chemotherapy. Prostate 2009, 69:92-104.
47. Kircheis R., Halanek N., Koller I., Jost W., Schuster M., Gorr G., Hajszan K., Nechansky A. Correlation of ADCC activity with cytokine release induced by the stably expressed, glyco-engineered humanized Lewis Y-specific monoclonal antibody MB314. MAbs 2012, 4:532-541.
48. Kitamura K., Stockert E., Garin-Chesa P., Welt S., Lloyd K.O., Armour K.L., Wallace T.P., Harris W.J., Carr F.J., Old L.J. Specificity analysis of blood group Lewis-y (Le(y)) antibodies generatedagainst synthetic and natural Le(y) determinants. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:12957-12961.
49. Kobata A., Amano J. Altered glycosylation of proteins produced by malignant cells, and application for the diagnosis and immunotherapy of tumours. Immunol. Cell Biol. 2005, 83:429-439.
50. Krengel U., Olsson L.L., Martinez C., Talavera A., Rojas G., Mier E., Angstrom J., Moreno E. Structure and molecular interactions of a unique antitumor antibody specific for N-glycolyl GM3. J. Biol. Chem. 2004, 279:5597-5603.
51. Krug L.M., Milton D.T., Jungbluth A.A., Chen L.C., Quaia E., Pandit-Taskar N., Nagel A., Jones J., Kris M.G., Finn R., Smith-Jones P., Scott A.M., Old L., Divgi C. Targeting Lewis Y (Le(y)) in small cell lung cancer with a humanized monoclonal antibody, hu3S193: a pilot trial testing two dose levels. J. Thorac. Oncol. 2007, 2:947-952.
52. Kubota T., Kumagai A., Ito H., Furukawa S., Someya Y., Takeda N., Ishii K., Wakita T., Narimatsu H., Shirato H. Structural basis for the recognition of Lewis antigens by genogroup I norovirus. J. Virol. 2012, 86:11138-11150.
53. Laskowski R.A., Swindells M.B. LigPlot+: multiple ligand-protein interaction diagrams for drug discovery. J. Chem. Inf. Model. 2011, 51:2778-2786.
54. Lawrence S.L., Feil S.C., Holien J.K., Kuiper M.J., Doughty L., Dolezal O., Mulhern T.D., Tweten R.K., Parker M.W. Manipulating the Lewis antigen specificity of the cholesterol-dependent cytolysin lectinolysin. Front. Immunol. 2012, 3:330.
55. Liu J., Lin B., Hao Y., Qi Y., Zhu L., Li F., Liu D., Cong J., Zhang S., Iwamori M. Lewis y antigen promotes the proliferation of ovarian carcinoma-derived RMG-I cells through the PI3K/Akt signaling pathway. J. Exp. Clin. Cancer Res. 2009, 28:154.
56. Liu Y., Misulovin Z., Bjorkman P.J. The molecular mechanism of sulfated carbohydrate recognition by the cysteine-rich domain of mannose receptor. J. Mol. Biol. 2001, 305:481-490.
57. Loo D., Pryer N., Young P., Liang T., Coberly S., King K.L., Kang K., Roberts P., Tsao M., Xu X., Potts B., Mather J.P. The glycotope-specific RAV12 monoclonal antibody induces oncosis in vitro and has antitumor activity against gastrointestinal adenocarcinoma tumor xenografts in vivo. Mol. Cancer Ther. 2007, 6:856-865.
58. Ma Y., Kowolik C.M., Swiderski P.M., Kortylewski M., Yu H., Horne D.A., Jove R., Caballero O.L., Simpson A.J., Lee F.T., Pillay V., Scott A.M. Humanized Lewis-Y specific antibody based delivery of STAT3 siRNA. ACS Chem. Biol. 2011, 6:962-970.
59. Manimala J.C., Roach T.A., Li Z., Gildersleeve J.C. High-throughput carbohydrate microarray profiling of 27 antibodies demonstrates widespread specificity problems. Glycobiology 2007, 17:17C-23C.
60. Milde-Langosch K., Karn T., Schmidt M., zu Eulenburg C., Oliveira-Ferrer L., Wirtz R.M., Schumacher U., Witzel I., Schutze D., Muller V. Prognostic relevance of glycosylation-associated genes in breast cancer. Breast Cancer Res. Treat. 2014, 145:295-305.
61. Miyoshi E., Moriwaki K., Nakagawa T. Biological function of fucosylation in cancer biology. J. Biochem. 2008, 143:725-729.
62. Mollicone R., Cailleau A., Imberty A., Gane P., Perez S., Oriol R. Recognition of the blood group H type 2 trisaccharide epitope by 28 monoclonal antibodies and three lectins. Glycoconj. J. 1996, 13:263-271.
63. Moore C.J., Auzanneau F.I. Understanding the recognition of Lewis X by anti-Le(x) monoclonal antibodies. J. Med. Chem. 2013, 56:8183-8190.
64. Noble P., Spendlove I., Harding S., Parsons T., Durrant L.G. Therapeutic targeting of Lewis(y) and Lewis(b) with a novel monoclonal antibody 692/29. PLoS ONE 2013, 8:e54892.
65. Orbom A., Eriksson S.E., Elgstrom E., Ohlsson T., Nilsson R., Tennvall J., Strand S.E. The intratumoral distribution of radiolabeled 177Lu-BR96 monoclonal antibodies changes in relation to tumor histology over time in a syngeneic rat colon carcinoma model. J. Nucl. Med. 2013, 54:1404-1410.
66. Pai L.H., Batra J.K., FitzGerald D.J., Willingham M.C., Pastan I. Anti-tumor activities of immunotoxins made of monoclonal antibody B3 and various forms of Pseudomonas exotoxin. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:3358-3362.
67. Pai L.H., Wittes R., Setser A., Willingham M.C., Pastan I. Treatment of advanced solid tumors with immunotoxin LMB-1: an antibody linked to Pseudomonas exotoxin. Nat. Med. 1996, 2:350-353.
68. Pastan I., Lovelace E.T., Gallo M.G., Rutherford A.V., Magnani J.L., Willingham M.C. Characterization of monoclonal antibodies B1 and B3 that react with mucinous adenocarcinomas. Cancer Res. 1991, 51:3781-3787.
69. Perret S., Sabin C., Dumon C., Pokorna M., Gautier C., Galanina O., Ilia S., Bovin N., Nicaise M., Desmadril M., Gilboa-Garber N., Wimmerova M., Mitchell E.P., Imberty A. Structural basis for the interaction between human milk oligosaccharides and the bacterial lectin PA-IIL of Pseudomonas aeruginosa. Biochem. J. 2005, 389:325-332.
70. Pichla S.L., Murali R., Burnett R.M. The crystal structure of a Fab fragment to the melanoma-associated GD2 ganglioside. J. Struct. Biol. 1997, 119:6-16.
71. Rabu C., McIntosh R., Jurasova Z., Durrant L. Glycans as targets for therapeutic antitumor antibodies. Future Oncol. 2012, 8:943-960.
72. Ramsland P.A., Farrugia W., Bradford T.M., Mark Hogarth P., Scott A.M. Structural convergence of antibody binding of carbohydrate determinants in Lewis Y tumor antigens. J. Mol. Biol. 2004, 340:809-818.
73. Reynolds M., Fuchs A., Lindhorst T.K., Perez S. The hydration features of carbohydrate determinants of Lewis antigens. Mol. Simul. 2008, 34:447-460.
74. Ritchie D.S., Neeson P.J., Khot A., Peinert S., Tai T., Tainton K., Chen K., Shin M., Wall D.M., Honemann D., Gambell P., Westerman D.A., Haurat J., Westwood J.A., Scott A.M., Kravets L., Dickinson M., Trapani J.A., Smyth M.J., Darcy P.K., Kershaw M.H., Prince H.M. Persistence and efficacy of second generation CAR T cell against the LeY antigen in acute myeloid leukemia. Mol. Ther. 2013, 21:2122-2129.
75. Roque-Navarro L., Chakrabandhu K., de Leon J., Rodriguez S., Toledo C., Carr A., de Acosta C.M., Hueber A.O., Perez R. Anti-ganglioside antibody-induced tumor cell death by loss of membrane integrity. Mol. Cancer Ther. 2008, 7:2033-2041.
76. Ross H.J., Hart L.L., Swanson P.M., Rarick M.U., Figlin R.A., Jacobs A.D., McCune D.E., Rosenberg A.H., Baron A.D., Grove L.E., Thorn M.D., Miller D.M., Drachman J.G., Rudin C.M. A randomized, multicenter study to determine the safety and efficacy of the immunoconjugate SGN-15 plus docetaxel for the treatment of non-small cell lung carcinoma. Lung Cancer 2006, 54:69-77.
77. Saha S., Pashov A., Siegel E.R., Murali R., Kieber-Emmons T. Defining the recognition elements of Lewis Y-reactive antibodies. PLoS ONE 2014, 9:e104208.
78. Saleh M.N., Sugarman S., Murray J., Ostroff J.B., Healey D., Jones D., Daniel C.R., LeBherz D., Brewer H., Onetto N., LoBuglio A.F. Phase I trial of the anti-Lewis Y drug immunoconjugate BR96-doxorubicin in patients with lewis Y-expressing epithelial tumors. J. Clin. Oncol. 2000, 18:2282-2292.
79. Sawada R., Sun S.M., Wu X., Hong F., Ragupathi G., Livingston P.O., Scholz W.W. Human monoclonal antibodies to sialyl-Lewis (CA19.9) with potent CDC, ADCC, and antitumor activity. Clin. Cancer Res. 2011, 17:1024-1032.
80. Schlimok G., Pantel K., Loibner H., Fackler-Schwalbe I., Riethmuller G. Reduction of metastatic carcinoma cells in bone marrow by intravenously administered monoclonal antibody: towards a novel surrogate test to monitor adjuvant therapies of solid tumours. Eur. J. Cancer 1995, 31A:1799-1803.
81. Scott A.M., Geleick D., Rubira M., Clarke K., Nice E.C., Smyth F.E., Stockert E., Richards E.C., Carr F.J., Harris W.J., Armour K.L., Rood J., Kypridis A., Kronina V., Murphy R., Lee F.T., Liu Z., Kitamura K., Ritter G., Laughton K., Hoffman E., Burgess A.W., Old L.J. Construction, production, and characterization of humanized anti-Lewis Y monoclonal antibody 3S193 for targeted immunotherapy of solid tumors. Cancer Res. 2000, 60:3254-3261.
82. Scott A.M., Renner C. Tumour Antigens Recognized by Antibodies 2001, John Wiley & Sons, Ltd. 10.1038/npg.els.0001433.
83. Scott A.M., Tebbutt N., Lee F.T., Cavicchiolo T., Liu Z., Gill S., Poon A.M., Hopkins W., Smyth F.E., Murone C., MacGregor D., Papenfuss A.T., Chappell B., Saunder T.H., Brechbiel M.W., Davis I.D., Murphy R., Chong G., Hoffman E.W., Old L.J. A phase I biodistribution and pharmacokinetic trial of humanized monoclonal antibody Hu3s193 in patients with advanced epithelial cancers that express the Lewis-Y antigen. Clin. Cancer Res. 2007, 13:3286-3292.
84. Scott A.M., Wolchok J.D., Old L.J. Antibody therapy of cancer. Nat. Rev. Cancer 2012, 12:278-287.
85. Shanker S., Choi J.M., Sankaran B., Atmar R.L., Estes M.K., Prasad B.V. Structural analysis of histo-blood group antigen binding specificity in a norovirus GII.4 epidemic variant: implications for epochal evolution. J. Virol. 2011, 85:8635-8645.
86. Shanker S., Czako R., Sankaran B., Atmar R.L., Estes M.K., Prasad B.V. Structural analysis of determinants of histo-blood group antigen binding specificity in genogroup I noroviruses. J. Virol. 2014, 88:6168-6180.
87. Sheriff S., Chang C.Y., Jeffrey P.D., Bajorath J. X-ray structure of the uncomplexed anti-tumor antibody BR96 and comparison with its antigen-bound form. J. Mol. Biol. 1996, 259:938-946.
88. Singhal A., Hakomori S. Molecular changes in carbohydrate antigens associated with cancer. Bioessays 1990, 12:223-230.
89. Sliwkowski M.X., Mellman I. Antibody therapeutics in cancer. Science 2013, 341:1192-1198.
90. Talavera A., Eriksson A., Okvist M., Lopez-Requena A., Fernandez-Marrero Y., Perez R., Moreno E., Krengel U. Crystal structure of an anti-ganglioside antibody, and modelling of the functional mimicry of its NeuGc-GM3 antigen by an anti-idiotypic antibody. Mol. Immunol. 2009, 46:3466-3475.
91. Tempero M.A., Uchida E., Takasaki H., Burnett D.A., Steplewski Z., Pour P.M. Relationship of carbohydrate antigen 19-9 and Lewis antigens in pancreatic cancer. Cancer Res. 1987, 47:5501-5503.
92. Tessier M.B., Grant O.C., Heimburg-Molinaro J., Smith D., Jadey S., Gulick A.M., Glushka J., Deutscher S.L., Rittenhouse-Olson K., Woods R.J. Computational screening of the human TF-glycome provides a structural definition for the specificity of anti-tumor antibody JAA-F11. PLoS ONE 2013, 8:e54874.
93. Tolcher A.W., Sugarman S., Gelmon K.A., Cohen R., Saleh M., Isaacs C., Young L., Healey D., Onetto N., Slichenmyer W. Randomized phase II study of BR96-doxorubicin conjugate in patients with metastatic breast cancer. J. Clin. Oncol. 1999, 17:478-484.
94. Trail P.A., Willner D., Bianchi A.B., Henderson A.J., TrailSmith M.D., Girit E., Lasch S., Hellstrom I., Hellstrom K.E. Enhanced antitumor activity of paclitaxel in combination with the anticarcinoma immunoconjugate BR96-doxorubicin. Clin. Cancer Res. 1999, 5:3632-3638.
95. van Roon A.M., Pannu N.S., de Vrind J.P., van der Marel G.A., van Boom J.H., Hokke C.H., Deelder A.M., Abrahams J.P. Structure of an anti-Lewis X Fab fragment in complex with its Lewis X antigen. Structure 2004, 12:1227-1236.
96. Wallace A.C., Laskowski R.A., Thornton J.M. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 1995, 8:127-134.
97. Wang C.C., Huang Y.L., Ren C.T., Lin C.W., Hung J.T., Yu J.C., Yu A.L., Wu C.Y., Wong C.H. Glycan microarray of Globo H and related structures for quantitative analysis of breast cancer. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:11661-11666.
98. Wilson R.M., Danishefsky S.J. A vision for vaccines built from fully synthetic tumor-associated antigens: from the laboratory to the clinic. J. Am. Chem. Soc. 2013, 135:14462-14472.
99. Xiong X., Tuzikov A., Coombs P.J., Martin S.R., Walker P.A., Gamblin S.J., Bovin N., Skehel J.J. Recognition of sulphated and fucosylated receptor sialosides by A/Vietnam/1194/2004 (H5N1) influenza virus. Virus Res. 2013, 178:12-14.
100. Yuan M., Itzkowitz S.H., Palekar A., Shamsuddin A.M., Phelps P.C., Trump B.F., Kim Y.S. Distribution of blood group antigens A, B, H, Lewis a, and Lewis b in human normal, fetal, and malignant colonic tissue. Cancer Res. 1985, 45:4499-4511.
101. Yuriev E., Farrugia W., Scott A.M., Ramsland P.A. Three-dimensional structures of carbohydrate determinants of Lewis system antigens: implications for effective antibody targeting of cancer. Immunol. Cell Biol. 2005, 83:709-717.
102. Zhang S., Cordon-Cardo C., Zhang H.S., Reuter V.E., Adluri S., Hamilton W.B., Lloyd K.O., Livingston P.O. Selection of tumor antigens as targets for immune attack using immunohistochemistry: I. Focus on gangliosides. Int. J. Cancer 1997, 73:42-49.