Sweet escape: Sialic acids in tumor immune evasion

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1846, Issue 1, 2014, Pages 238-246

  Büll, Christian ^a   den Brok, Martijn H ^a   Adema, Gosse J ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Cancer; Immune evasion; Sialic acids; Sialoglycans; Siglecs; Tumor microenvironment

Indexed keywords

CYTOKINE; SIALIC ACID;

ANTIGEN PRESENTING CELL; BONE MARROW CELL; CANCER IMMUNOTHERAPY; CARCINOGENESIS; CELL ASSAY; COMPLEMENT SYSTEM; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE ACTIVITY; EFFECTOR CELL; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; LYMPHOCYTE FUNCTION; MALIGNANT NEOPLASTIC DISEASE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TUMOR ESCAPE;

CANCER; IMMUNE EVASION; SIALIC ACIDS; SIALOGLYCANS; SIGLECS; TUMOR MICROENVIRONMENT;

ANIMALS; COMPLEMENT SYSTEM PROTEINS; DENDRITIC CELLS; HUMANS; IMMUNE SYSTEM; IMMUNOTHERAPY; MYELOID CELLS; NEOPLASMS; SIALIC ACIDS; T-LYMPHOCYTES, CYTOTOXIC; TUMOR ESCAPE;

EID: 84905233546     PISSN: 0304419X     EISSN: 18792561     Source Type: Journal    
DOI: 10.1016/j.bbcan.2014.07.005     Document Type: Review

References (107)

1. Varki A., Lowe J.B. Biological Roles of Glycans 2009.
2. Varki A., Kannagi R., Toole B.P. Glycosylation changes in cancer. Essentials of Glycobiology, Cold Spring Harbor (NY) 2009, A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart, M.E. Etzler (Eds.).
3. Häuselmann I., Borsig L. Altered tumor-cell glycosylation promotes metastasis. Front. Oncol. 2014, 4:28.
4. Varki A., Schauer R. Sialic acids. Essentials of Glycobiology, Cold Spring Harbor (NY) 2009, A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, C.R. Bertozzi, G.W. Hart, M.E. Etzler (Eds.).
5. Harduin-Lepers A., Krzewinski-Recchi M.A., Colomb F., Foulquier F., Groux-Degroote S., Delannoy P. Sialyltransferases functions in cancers. Front. Biosci. (Elite Ed) 2012, 4:499-515.
6. Büll C., Stoel M.A., den Brok M.H., Adema G.J. Sialic acids sweeten a tumor's life. Cancer Res. 2014, 74:3199-3204.
7. Astronomo R.D., Burton D.R. Carbohydrate vaccines: developing sweet solutions to sticky situations?. Nat. Rev. Drug Discov. 2010, 9:308-324.
8. Kufe D.W. Mucins in cancer: function, prognosis and therapy. Nat. Rev. Cancer 2009, 9:874-885.
9. Mehla K., Singh P.K. MUC1: a novel metabolic master regulator. Biochim. Biophys. Acta 2014, 1845:126-135.
10. Fuster M.M., Esko J.D. The sweet and sour of cancer: glycans as novel therapeutic targets. Nat. Rev. Cancer 2005, 5:526-542.
11. Schultz M.J., Swindall A.F., Bellis S.L. Regulation of the metastatic cell phenotype by sialylated glycans. Cancer Metastasis Rev. 2012, 31:501-518.
12. Johnson J.L., Jones M.B., Ryan S.O., Cobb B.A. The regulatory power of glycans and their binding partners in immunity. Trends Immunol. 2013, 34:290-298.
13. Varki A., Gagneux P. Multifarious roles of sialic acids in immunity. Ann. N. Y. Acad. Sci. 2012, 1253:16-36.
14. Khatua B., Ghoshal A., Bhattacharya K., Mandal C., Saha B., Crocker P.R. Sialic acids acquired by Pseudomonas aeruginosa are involved in reduced complement deposition and siglec mediated host-cell recognition. FEBS Lett. 2010, 584:555-561.
15. Carlin A.F., Uchiyama S., Chang Y.C., Lewis A.L., Nizet V., Varki A. Molecular mimicry of host sialylated glycans allows a bacterial pathogen to engage neutrophil Siglec-9 and dampen the innate immune response. Blood 2009, 113:3333-3336.
16. Surolia I., Pirnie S.P., Chellappa V., Taylor K.N., Cariappa A., Moya J., Liu H., Bell D.W., Driscoll D.R., Diederichs S., Haider K., Netravali I., Le S., Elia R., Dow E., Lee A., Freudenberg J., De Jager P.L., Chretien Y., Varki A., MacDonald M.E., Gillis T., Behrens T.W., Bloch D., Collier D., Korzenik J., Podolsky D.K., Hafler D., Murali M., Sands B., Stone J.H., Gregersen P.K., Pillai S. Functionally defective germline variants of sialic acid acetylesterase in autoimmunity. Nature 2010, 466:243-247.
17. Miyazaki K., Sakuma K., Kawamura Y.I., Izawa M., Ohmori K., Mitsuki M., Yamaji T., Hashimoto Y., Suzuki A., Saito Y., Dohi T., Kannagi R. Colonic epithelial cells express specific ligands for mucosal macrophage immunosuppressive receptors Siglec-7 and -9. J. Immunol. 2012, 188:4690-4700.
18. Linnartz B., Kopatz J., Tenner A.J., Neumann H. Sialic acid on the neuronal glycocalyx prevents complement C1 binding and complement receptor-3-mediated removal by microglia. J. Neurosci. 2012, 32:946-952.
19. Varki A. Since there are PAMPs and DAMPs, there must be SAMPs? Glycan "self-associated molecular patterns" dampen innate immunity, but pathogens can mimic them. Glycobiology 2011, 21:1121-1124.
20. Pillai S., Netravali I.A., Cariappa A., Mattoo H. Siglecs and immune regulation. Annu. Rev. Immunol. 2012, 30:357-392.
21. Stamenkovic I., Sgroi D., Aruffo A., Sy M.S., Anderson T. The B lymphocyte adhesion molecule CD22 interacts with leukocyte common antigen CD45RO on T cells and alpha 2-6 sialyltransferase, CD75, on B cells. Cell 1991, 66:1133-1144.
22. Crocker P.R., Kelm S., Dubois C., Martin B., McWilliam A.S., Shotton D.M., Paulson J.C., Gordon S. Purification and properties of sialoadhesin, a sialic acid-binding receptor of murine tissue macrophages. EMBO J. 1991, 10:1661-1669.
23. Crocker P.R., Paulson J.C., Varki A. Siglecs and their roles in the immune system. Nat. Rev. Immunol. 2007, 7:255-266.
24. Chen G.Y., Tang J., Zheng P., Liu Y. CD24 and Siglec-10 selectively repress tissue damage-induced immune responses. Science 2009, 323:1722-1725.
25. Liu Y., Chen G.Y., Zheng P. CD24-Siglec G/10 discriminates danger - from pathogen-associated molecular patterns. Trends Immunol. 2009, 30:557-561.
26. Chen G.Y., Chen X., King S., Cavassani K.A., Cheng J., Zheng X., Cao H., Yu H., Qu J., Fang D., Wu W., Bai X.F., Liu J.Q., Woodiga S.A., Chen C., Sun L., Hogaboam C.M., Kunkel S.L., Zheng P., Liu Y. Amelioration of sepsis by inhibiting sialidase-mediated disruption of the CD24-SiglecG interaction. Nat. Biotechnol. 2011, 29:428-435.
27. Chen W., Han C., Xie B., Hu X., Yu Q., Shi L., Wang Q., Li D., Wang J., Zheng P., Liu Y., Cao X. Induction of Siglec-G by RNA viruses Inhibits the innate immune response by promoting RIG-I degradation. Cell 2013, 152:467-478.
28. Sanford B.H. An alteration in tumor histocompatibility induced by neuraminidase. Transplantation 1967, 5:1273-1279.
29. Bagshawe K.D., Currie G.A. Immunogenicity of L 1210 murine leukaemia cells after treatment with neuraminidase. Nature 1968, 218:1254-1255.
30. Sedlacek H.H., Seiler F.R., Schwick H.G. Neuraminidase and tumor immunotherapy. Klin. Wochenschr. 1977, 55:199-214.
31. Sedlacek H.H., Seiler F.R. Immunotherapy of neoplastic diseases with neuraminidase - contradictions, new aspects, and revised concepts. Cancer Immunol. Immunother. 1978, 5:153-163.
32. Currie G.A. Masking of antigens on the Landschutz ascites tumour. Lancet 1967, 2:1336-1338.
33. Currie G.A., Bagshawe K.D. The role of sialic acid in antigenic expression: further studies of the Landschutz ascites tumour. Br. J. Cancer 1968, 22:843-853.
34. Sanford B.H., Codington J.F. Further studies on the effect of neuraminidase on tumor cell transplantability. Tissue Antigens 1971, 1:153-161.
35. Powell L.D., Whiteheart S.W., Hart G.W. Cell surface sialic acid influences tumor cell recognition in the mixed lymphocyte reaction. J. Immunol. 1987, 139:262-270.
36. Lundgren G., Simmons R.L. Effect of neuraminidase on the stimulatory capacity of cells in human mixed lymphocyte cultures. Clin. Exp. Immunol. 1971, 9:915-926.
37. Watkins E., Ogata Y., Anderson L.L., Watkins E., Waters M.F. Activation of host lymphocytes cultured with cancer cells treated with neuraminidase. Nat. New Biol. 1971, 231:83-85.
38. Watkins E., Gray B.N., Anderson L.L., Baralt O.L., Nebril L.R., Waters M.F., Connery C.K. Neuraminidase-mediated augmentation of in vitro immune response of patients with solid tumors. Int. J. Cancer 1974, 14:799-807.
39. Seigler H.F., Ww Shinglet, Fetter B.F., Miller D.S., Metzgar R.S., Bergoc P.M., Buckley C.E., Phaup M.B. Nonspecific and specific immunotherapy in patients with melanoma. Surgery 1972, 72:162-174.
40. Rosato F.E., Brown A.S., Miller E.E., Rosato E.F., Mullis W.F., Johnson J., Moskovit A. Neuraminidase immunotherapy of tumors in man. Surg. Gynaecol. Obstet. 1974, 139:675-682.
41. Rosato F.E. Active specific immunotherapy of human solid tumors. Ann. N. Y. Acad. Sci. 1976, 277:332-338.
42. Bekesi J.G., Holland J.F. Impact of specific immunotherapy in acute myelocytic leukemia. Hematol. Blood Transfus. 1979, 23:79-87.
43. Urbanitz D., Buchner T., Pielken H., Koch P., Ludwig W.D., Maschmeier G., Heinecke A., van de Loo J. Neuraminidase-treated allogeneic blasts for maintenance in acute myelogenous leukemia: results of a prospective randomized trial. Hematol. Blood Transfus. 1987, 30:64-68.
44. Gray B.N., Walker C., Andrewartha L., Freeman S., Bennett R.C. Controlled clinical trial of adjuvant immunotherapy with BCG and neuraminidase-treated autologous tumour cells in large bowel cancer. J. Surg. Oncol. 1989, 40:34-37.
45. Figdor C.G., de Vries I.J., Lesterhuis W.J., Melief C.J. Dendritic cell immunotherapy: mapping the way. Nat. Med. 2004, 10:475-480.
46. Mcquiddy P., Lilien J.E. Binding of exogenously added neuraminidase to cells and tissues in culture. Biochim. Biophys. Acta 1973, 291:774-779.
47. Ferreira V.P., Pangburn M.K., Cortes C. Complement control protein factor H: the good, the bad, and the inadequate. Mol. Immunol. 2010, 47:2187-2197.
48. Lewis L.A., Carter M., Ram S. The relative roles of factor H binding protein, neisserial surface protein A, and lipooligosaccharide sialylation in regulation of the alternative pathway of complement on meningococci. J. Immunol. 2012, 188:5063-5072.
49. Ram S., Sharma A.K., Simpson S.D., Gulati S., McQuillen D.P., Pangburn M.K., Rice P.A. A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. J. Exp. Med. 1998, 187:743-752.
50. Severi E., Hood D.W., Thomas G.H. Sialic acid utilization by bacterial pathogens. Microbiology 2007, 153:2817-2822.
51. Gancz D., Fishelson Z. Cancer resistance to complement-dependent cytotoxicity (CDC): problem-oriented research and development. Mol. Immunol. 2009, 46:2794-2800.
52. Pio R., Ajona D., Lambris J.D. Complement inhibition in cancer therapy. Semin. Immunol. 2013, 25:54-64.
53. Donin N., Jurianz K., Ziporen L., Schultz S., Kirschfink M., Fishelson Z. Complement resistance of human carcinoma cells depends on membrane regulatory proteins, protein kinases and sialic acid. Clin. Exp. Immunol. 2003, 131:254-263.
54. Junnikkala S., Jokiranta T.S., Friese M.A., Jarva H., Zipfel P.F., Meri S. Exceptional resistance of human H2 glioblastoma cells to complement-mediated killing by expression and utilization of factor H and factor H-like protein 1. J. Immunol. 2000, 164:6075-6081.
55. Ajona D., Hsu Y.F., Corrales L., Montuenga L.M., Pio R. Down-regulation of human complement factor H sensitizes non-small cell lung cancer cells to complement attack and reduces in vivo tumor growth. J. Immunol. 2007, 178:5991-5998.
56. Cheng M., Chen Y., Xiao W., Sun R., Tian Z. NK cell-based immunotherapy for malignant diseases. Cell. Mol. Immunol. 2013, 10:230-252.
57. Cohen M., Elkabets M., Perlmutter M., Porgador A., Voronov E., Apte R.N., Lichtenstein R.G. Sialylation of 3-methylcholanthrene-induced fibrosarcoma determines antitumor immune responses during immunoediting. J. Immunol. 2010, 185:5869-5878.
58. Belisle J.A., Horibata S., Jennifer G.A., Petrie S., Kapur A., Andre S., Gabius H.J., Rancourt C., Connor J., Paulson J.C., Patankar M.S. Identification of Siglec-9 as the receptor for MUC16 on human NK cells, B cells, and monocytes. Mol. Cancer 2010, 9:118.
59. Jandus C., Boligan K.F., Chijioke O., Liu H., Dahlhaus M., Demoulins T., Schneider C., Wehrli M., Hunger R.E., Baerlocher G.M., Simon H.U., Romero P., Munz C., von Gunten S. Interactions between Siglec-7/9 receptors and ligands influence NK cell-dependent tumor immunosurveillance. J. Clin. Invest. 2014, 124:1810-1820.
60. Drake P.M., Nathan J.K., Stock C.M., Chang P.V., Muench M.O., Nakata D., Reader J.R., Gip P., Golden K.P., Weinhold B., Gerardy-Schahn R., Troy F.A., Bertozzi C.R. Polysialic acid, a glycan with highly restricted expression, is found on human and murine leukocytes and modulates immune responses. J. Immunol. 2008, 181:6850-6858.
61. Nicoll G., Avril T., Lock K., Furukawa K., Bovin N., Crocker P.R. Ganglioside GD3 expression on target cells can modulate NK cell cytotoxicity via Siglec-7-dependent and -independent mechanisms. Eur. J. Immunol. 2003, 33:1642-1648.
62. Yamaji T., Mitsuki M., Teranishi T., Hashimoto Y. Characterization of inhibitory signaling motifs of the natural killer cell receptor Siglec-7: attenuated recruitment of phosphatases by the receptor is attributed to two amino acids in the motifs. Glycobiology 2005, 15:667-676.
63. Macauley M.S., Paulson J.C. IMMUNOLOGY glyco-engineering 'super-self'. Nat. Chem. Biol. 2014, 10:7-8.
64. Hudak J.E., Canham S.M., Bertozzi C.R. Glycocalyx engineering reveals a Siglec-based mechanism for NK cell immunoevasion. Nat. Chem. Biol. 2014, 10:69-75.
65. Gubbels J.A., Felder M., Horibata S., Belisle J.A., Kapur A., Holden H., Petrie S., Migneault M., Rancourt C., Connor J.P., Patankar M.S. MUC16 provides immune protection by inhibiting synapse formation between NK and ovarian tumor cells. Mol. Cancer 2010, 9:11.
66. Park J.E., Wu D.Y., Prendes M., Lu S.X., Ragupathi G., Schrantz N., Chapman P.B. Fine specificity of natural killer T cells against GD3 ganglioside and identification of GM3 as an inhibitory natural killer T-cell ligand. Immunology 2008, 123:145-155.
67. Webb T.J., Li X., Giuntoli R.L., Lopez P.H., Heuser C., Schnaar R.L., Tsuji M., Kurts C., Oelke M., Schneck J.P. Molecular identification of GD3 as a suppressor of the innate immune response in ovarian cancer. Cancer Res. 2012, 72:3744-3752.
68. Lee H.C., Wondimu A., Liu Y., Ma J.S., Radoja S., Ladisch S. Ganglioside inhibition of CD8+ T cell cytotoxicity: interference with lytic granule trafficking and exocytosis. J. Immunol. 2012, 189:3521-3527.
69. Lee K.H., Feig C., Tchikov V., Schickel R., Hallas C., Schutze S., Peter M.E., Chan A.C. The role of receptor internalization in CD95 signaling. EMBO J 2006, 25:1009-1023.
70. Swindall A.F., Bellis S.L. Sialylation of the Fas death receptor by ST6Gal-I provides protection against Fas-mediated apoptosis in colon carcinoma cells. J. Biol. Chem. 2011, 286:22982-22990.
71. Nguyen D.H., Hurtado-Ziola N., Gagneux P., Varki A. Loss of Siglec expression on T lymphocytes during human evolution. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:7765-7770.
72. Ikehara Y., Ikehara S.K., Paulson J.C. Negative regulation of T cell receptor signaling by Siglec-7 (p70/AIRM) and Siglec-9. J. Biol. Chem. 2004, 279:43117-43125.
73. Bandala-Sanchez E., Zhang Y., Reinwald S., Dromey J.A., Lee B.H., Qian J., Bohmer R.M., Harrison L.C. T cell regulation mediated by interaction of soluble CD52 with the inhibitory receptor Siglec-10. Nat. Immunol. 2013, 14:741-748.
74. Saito Y., Nakahata S., Yamakawa N., Kaneda K., Ichihara E., Suekane A., Morishita K. CD52 as a molecular target for immunotherapy to treat acute myeloid leukemia with high EVI1 expression. Leukemia 2011, 25:921-931.
75. Bi S., Baum L.G. Sialic acids in T cell development and function. Biochim. Biophys. Acta 2009, 1790:1599-1610.
76. Nagafuku M., Okuyama K., Onimaru Y., Suzuki A., Odagiri Y., Yamashita T., Iwasaki K., Fujiwara M., Takayanagi M., Ohno I., Inokuchi J. CD4 and CD8 T cells require different membrane gangliosides for activation. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E336-E342.
77. De Palma M., Lewis C.E. Macrophage regulation of tumor responses to anticancer therapies. Cancer Cell 2013, 23:277-286.
78. Klaas M., Crocker P.R. Sialoadhesin in recognition of self and non-self. Semin. Immunopathol. 2012, 34:353-364.
79. O'Neill A.S., van den Berg T.K., Mullen G.E. Sialoadhesin - a macrophage-restricted marker of immunoregulation and inflammation. Immunology 2013, 138:198-207.
80. Asano K., Nabeyama A., Miyake Y., Qiu C.H., Kurita A., Tomura M., Kanagawa O., Fujii S., Tanaka M. CD169-positive macrophages dominate antitumor immunity by crosspresenting dead cell-associated antigens. Immunity 2011, 34:85-95.
81. Takamiya R., Ohtsubo K., Takamatsu S., Taniguchi N., Angata T. The interaction between Siglec-15 and tumor-associated sialyl-Tn antigen enhances TGF-beta secretion from monocytes/macrophages through the DAP12-Syk pathway. Glycobiology 2013, 23:178-187.
82. Ando M., Tu W., Nishijima K., Iijima S. Siglec-9 enhances IL-10 production in macrophages via tyrosine-based motifs. Biochem. Biophys. Res. Commun. 2008, 369:878-883.
83. Chen X., Eksioglu E.A., Zhou J., Zhang L., Djeu J., Fortenbery N., Epling-Burnette P., Van Bijnen S., Dolstra H., Cannon J., Youn J.I., Donatelli S.S., Qin D., De Witte T., Tao J., Wang H., Cheng P., Gabrilovich D.I., List A., Wei S. Induction of myelodysplasia by myeloid-derived suppressor cells. J. Clin. Invest. 2013, 123:4595-4611.
84. Lindau D., Gielen P., Kroesen M., Wesseling P., Adema G.J. The immunosuppressive tumour network: myeloid-derived suppressor cells, regulatory T cells and natural killer T cells. Immunology 2013, 138:105-115.
85. Jales A., Falahati R., Mari E., Stemmy E.J., Shen W., Southammakosane C., Herzog D., Ladisch S., Leitenberg D. Ganglioside-exposed dendritic cells inhibit T-cell effector function by promoting regulatory cell activity. Immunology 2011, 132:134-143.
86. Peguet-Navarro J., Sportouch M., Popa I., Berthier O., Schmitt D., Portoukalian J. Gangliosides from human melanoma tumors impair dendritic cell differentiation from monocytes and induce their apoptosis. J. Immunol. 2003, 170:3488-3494.
87. Shurin G.V., Shurin M.R., Bykovskaia S., Shogan J., Lotze M.T., Barksdale E.M. Neuroblastoma-derived gangliosides inhibit dendritic cell generation and function. Cancer Res. 2001, 61:363-369.
88. Bennaceur K., Popa I., Portoukalian J., Berthier-Vergnes O., Peguet-Navarro J. Melanoma-derived gangliosides impair migratory and antigen-presenting function of human epidermal Langerhans cells and induce their apoptosis. Int. Immunol. 2006, 18:879-886.
89. Ishida A., Ohta M., Toda M., Murata T., Usui T., Akita K., Inoue M., Nakada H. Mucin-induced apoptosis of monocyte-derived dendritic cells during maturation. Proteomics 2008, 8:3342-3349.
90. Ohta M., Ishida A., Toda M., Akita K., Inoue M., Yamashita K., Watanabe M., Murata T., Usui T., Nakada H. Immunomodulation of monocyte-derived dendritic cells through ligation of tumor-produced mucins to Siglec-9. Biochem. Biophys. Res. Commun. 2010, 402:663-669.
91. Carlos C.A., Dong H.F., Howard O.M., Oppenheim J.J., Hanisch F.G., Finn O.J. Human tumor antigen MUC1 is chemotactic for immature dendritic cells and elicits maturation but does not promote Th1 type immunity. J. Immunol. 2005, 175:1628-1635.
92. Crespo H.J., Lau J.T., Videira P.A. Dendritic cells: a spot on sialic acid. Front. Immunol. 2013, 4:491.
93. Büll C., Boltje T.J., Wassink M., de Graaf A.M., van Delft F.L., den Brok M.H., Adema G.J. Targeting aberrant sialylation in cancer cells using a fluorinated sialic acid analogue impairs adhesion, migration and in vivo tumor growth. Mol. Cancer Ther. 2013, 12:1935-1946.
94. Rillahan C.D., Antonopoulos A., Lefort C.T., Sonon R., Azadi P., Ley K., Dell A., Haslam S.M., Paulson J.C. Global metabolic inhibitors of sialyl- and fucosyltransferases remodel the glycome. Nat. Chem. Biol. 2012, 8:661-668.
95. Dube D.H., Bertozzi C.R. Glycans in cancer and inflammation-potential for therapeutics and diagnostics. Nat. Rev. Drug Discov. 2005, 4:477-488.
96. Koo H., Lee S., Na J.H., Kim S.H., Hahn S.K., Choi K., Kwon I.C., Jeong S.Y., Kim K. Bioorthogonal copper-free click chemistry in vivo for tumor-targeted delivery of nanoparticles. Angew. Chem. Int. Ed. Engl. 2012, 51:11836-11840.
97. Tangvoranuntakul P., Gagneux P., Diaz S., Bardor M., Varki N., Varki A., Muchmore E. Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:12045-12050.
98. Samraj A.N., Laubli H., Varki N., Varki A. Involvement of a non-human sialic acid in human cancer. Front. Oncol. 2014, 4:33.
99. Heimburg-Molinaro J., Lum M., Vijay G., Jain M., Almogren A., Rittenhouse-Olson K. Cancer vaccines and carbohydrate epitopes. Vaccine 2011, 29:8802-8826.
100. Wu X., Ragupathi G., Panageas K., Hong F., Livingston P.O. Accelerated tumor growth mediated by sublytic levels of antibody-induced complement activation is associated with activation of the PI3K/AKT survival pathway. Clin. Cancer Res. 2013, 19:4728-4739.
101. Livingston P.O., Hood C., Krug L.M., Warren N., Kris M.G., Brezicka T., Ragupathi G. Selection of GM2, fucosyl GM1, globo H and polysialic acid as targets on small cell lung cancers for antibody mediated immunotherapy. Cancer Immunol. Immunother. 2005, 54:1018-1025.
102. Cai H., Sun Z.Y., Chen M.S., Zhao Y.F., Kunz H., Li Y.M. Synthetic multivalent glycopeptide-lipopeptide antitumor vaccines: impact of the cluster effect on the killing of tumor cells. Angew. Chem. Int. Ed. Engl. 2014, 53:1699-1703.
103. Ju T., Wang Y., Aryal R.P., Lehoux S.D., Ding X., Kudelka M.R., Cutler C., Zeng J., Wang J., Sun X., Heimburg-Molinaro J., Smith D.F., Cummings R.D. Tn and sialyl-Tn antigens, aberrant O-glycomics as human disease markers. Proteomics Clin. Appl. 2013, 7:618-631.
104. Zhu J., Warren J.D., Danishefsky S.J. Synthetic carbohydrate-based anticancer vaccines: the Memorial Sloan-Kettering experience. Expert Rev. Vaccines 2009, 8:1399-1413.
105. 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.
106. Lou Y.W., Wang P.Y., Yeh S.C., Chuang P.K., Li S.T., Wu C.Y., Khoo K.H., Hsiao M., Hsu T.L., Wong C.H. Stage-specific embryonic antigen-4 as a potential therapeutic target in glioblastoma multiforme and other cancers. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:2482-2487.
107. Cohen M., Varki A. The sialome-far more than the sum of its parts. Omics 2010, 14:455-464.