Glycan Elongation Beyond the Mucin Associated Tn Antigen Protects Tumor Cells from Immune-Mediated Killing

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Madsen, Caroline B ^a   Lavrsen, Kirstine ^a   Steentoft, Catharina ^a   Vester Christensen, Malene B ^a   Clausen, Henrik ^a   Wandall, Hans H ^a   Pedersen, Anders Elm ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

GALACTOSE; GLYCAN; GLYCOPROTEIN; MUCIN; MUCIN 1; MUCIN 16; SERINE; THREONINE; UNCLASSIFIED DRUG;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; BREAST ADENOCARCINOMA; CANCER CELL; CELL SURFACE; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; GLYCOSYLATION; HUMAN; HUMAN CELL; IMMUNE MEDIATED INJURY; IMMUNE SYSTEM; MALIGNANT TRANSFORMATION; NATURAL KILLER CELL; PANCREAS ADENOCARCINOMA; TUMOR CELL; UPREGULATION;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; ANTINEOPLASTIC AGENTS; CA-125 ANTIGEN; CELL LINE, TUMOR; CELL SURVIVAL; GENE KNOCKOUT TECHNIQUES; GLYCOSYLATION; HUMANS; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; MUCIN-1; POLYSACCHARIDES; RECEPTOR, EPIDERMAL GROWTH FACTOR; T-LYMPHOCYTES, CYTOTOXIC; TUMOR ESCAPE;

EID: 84883613105     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072413     Document Type: Article

References (58)

1. Hanahan D, Weinberg RA, (2000) The hallmarks of cancer. Cell 100: 57-70 S0092-8674(00)81683-9 [pii].
2. Hanahan D, Weinberg RA, (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674 S0092-8674(11)00127-9 [pii];10.1016/j.cell.2011.02.013 [doi].
3. Sledge GW Jr, Miller KD, (2003) Exploiting the hallmarks of cancer: the future conquest of breast cancer. Eur J Cancer 39: 1668-1675 S0959804903002739 [pii].
4. Bauer K, Michel S, Reuschenbach M, Nelius N, von Knebel DM, et al. (2011) Dendritic cell and macrophage infiltration in microsatellite-unstable and microsatellite-stable colorectal cancer. Fam Cancer 10: 557-565 10.1007/s10689-011-9449-7 [doi].
5. Ladanyi A, Kiss J, Mohos A, Somlai B, Liszkay G, et al. (2011) Prognostic impact of B-cell density in cutaneous melanoma. Cancer Immunol Immunother 60: 1729-1738 10.1007/s00262-011-1071-x [doi].
6. Liu S, Lachapelle J, Leung S, Gao D, Foulkes WD, et al. (2012) CD8+ lymphocyte infiltration is an independent favorable prognostic indicator in basal-like breast cancer. Breast Cancer Res 14: R48 bcr3148 [pii];10.1186/bcr3148 [doi].
7. Sznurkowski JJ, Zawrocki A, Emerich J, Biernat W, (2011) Prognostic significance of CD4+ and CD8+ T cell infiltration within cancer cell nests in vulvar squamous cell carcinoma. Int J Gynecol Cancer 21: 717-721 10.1097/IGC.0b013e3182131f36 [doi];00009577-201105000-00021 [pii].
8. Emens LA, Silverstein SC, Khleif S, Marincola FM, Galon J, (2012) Toward integrative cancer immunotherapy: targeting the tumor microenvironment. J Transl Med 10: 70 1479-5876-10-70 [pii];10.1186/1479-5876-10-70 [doi].
9. Fridman WH, Galon J, Dieu-Nosjean MC, Cremer I, Fisson S, et al. (2011) Immune infiltration in human cancer: prognostic significance and disease control. Curr Top Microbiol Immunol 344: 1-24 10.1007/82_2010_46 [doi].
10. Galon J, Pages F, Marincola FM, Thurin M, Trinchieri G, et al. (2012) The immune score as a new possible approach for the classification of cancer. J Transl Med 10: 1 1479-5876-10-1 [pii];10.1186/1479-5876-10-1 [doi].
11. Pages F, Berger A, Camus M, Sanchez-Cabo F, Costes A, et al. (2005) Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 353: 2654-2666 353/25/2654 [pii];10.1056/NEJMoa051424 [doi].
12. Wright SE, (2012) Immunotherapy of breast cancer. Expert Opin Biol Ther 12: 479-490 10.1517/14712598.2012.665445 [doi].
13. Lee WC, Wu TJ, Chou HS, Yu MC, Hsu PY, et al. (2012) The impact of CD4+ CD25+ T cells in the tumor microenvironment of hepatocellular carcinoma. Surgery 151: 213-222 S0039-6060(11)00380-1 [pii];10.1016/j.surg.2011.07.029 [doi].
14. Montero AJ, Diaz-Montero CM, Kyriakopoulos CE, Bronte V, Mandruzzato S, (2012) Myeloid-derived suppressor cells in cancer patients: a clinical perspective. J Immunother 35: 107-115 10.1097/CJI.0b013e318242169f [doi];00002371-201202000-00001 [pii].
15. Hollingsworth MA, Swanson BJ, (2004) Mucins in cancer: protection and control of the cell surface. Nat Rev Cancer 4: 45-60 10.1038/nrc1251 [doi];nrc1251 [pii].
16. Taylor-Papadimitriou J, Burchell J, Miles DW, Dalziel M, (1999) MUC1 and cancer. Biochim Biophys Acta 1455: 301-313 S0925-4439(99)00055-1 [pii].
17. Gendler SJ, Spicer AP, Lalani EN, Duhig T, Peat N, et al. (1991) Structure and biology of a carcinoma-associated mucin, MUC1. Am Rev Respir Dis 144: S42-S47.
18. O'Brien TJ, Beard JB, Underwood LJ, Dennis RA, Santin AD, et al. (2001) The CA 125 gene: an extracellular superstructure dominated by repeat sequences. Tumour Biol 22: 348-366 tbi22348 [pii].
19. Brockhausen I, (2006) Mucin-type O-glycans in human colon and breast cancer: glycodynamics and functions. EMBO Rep 7: 599-604 7400705 [pii];10.1038/sj.embor.7400705 [doi].
20. Hanisch FG, (2001) O-glycosylation of the mucin type. Biol Chem 382: 143-149 10.1515/BC.2001.022 [doi].
21. Cazet A, Julien S, Bobowski M, Burchell J, Delannoy P, (2010) Tumour-associated carbohydrate antigens in breast cancer. Breast Cancer Res 12: 204 bcr2577 [pii];10.1186/bcr2577 [doi].
22. Wandall HH, Blixt O, Tarp MA, Pedersen JW, Bennett EP, et al. (2010) Cancer biomarkers defined by autoantibody signatures to aberrant o-glycopeptide epitopes. Cancer Res 70: 1306-1313.
23. Lakshminarayanan V, Thompson P, Wolfert MA, Buskas T, Bradley JM, et al. (2012) Immune recognition of tumor-associated mucin MUC1 is achieved by a fully synthetic aberrantly glycosylated MUC1 tripartite vaccine. Proc Natl Acad Sci U S A 109: 261-266 1115166109 [pii];10.1073/pnas.1115166109 [doi].
24. Gubbels JA, Felder M, Horibata S, Belisle JA, Kapur A, et al. (2010) MUC16 provides immune protection by inhibiting synapse formation between NK and ovarian tumor cells. Mol Cancer 9: 11 1476-4598-9-11 [pii];10.1186/1476-4598-9-11 [doi].
25. Suzuki Y, Sutoh M, Hatakeyama S, Mori K, Yamamoto H, et al. (2012) MUC1 carrying core 2 O-glycans functions as a molecular shield against NK cell attack, promoting bladder tumor metastasis. Int J Oncol 40: 1831-1838 10.3892/ijo.2012.1411 [doi].
26. Jentoft N, (1990) Why are proteins O-glycosylated? Trends Biochem Sci 15: 291-294 0968-0004(90)90014-3 [pii].
27. Beum PV, Kennedy AD, Williams ME, Lindorfer MA, Taylor RP, (2006) The shaving reaction: rituximab/CD20 complexes are removed from mantle cell lymphoma and chronic lymphocytic leukemia cells by THP-1 monocytes. J Immunol 176: 2600-2609 176/4/2600 [pii].
28. Pedersen AE, Jungersen MB, Pedersen CD, (2011) Monocytes mediate shaving of B-cell-bound anti-CD20 antibodies. Immunology 133: 239-245 10.1111/j.1365-2567.2011.03434.x [doi].
29. Beum PV, Mack DA, Pawluczkowycz AW, Lindorfer MA, Taylor RP, (2008) Binding of rituximab, trastuzumab, cetuximab, or mAb T101 to cancer cells promotes trogocytosis mediated by THP-1 cells and monocytes. J Immunol 181: 8120-8132 181/11/8120 [pii].
30. Keydar I, Chen L, Karby S, Weiss FR, Delarea J, et al. (1979) Establishment and characterization of a cell line of human breast carcinoma origin. Eur J Cancer 15: 659-670.
31. Tarp MA, Sorensen AL, Mandel U, Paulsen H, Burchell J, et al. (2007) Identification of a novel cancer-specific immunodominant glycopeptide epitope in the MUC1 tandem repeat. Glycobiology 17: 197-209.
32. Bohm CM, Mulder MC, Zennadi R, Notter M, Schmitt-Graff A, et al. (1997) Carbohydrate recognition on MUC1-expressing targets enhances cytotoxicity of a T cell subpopulation. Scand J Immunol 46: 27-34.
33. Thurnher M, Clausen H, Sharon N, Berger EG, (1993) Use of O-glycosylation-defective human lymphoid cell lines and flow cytometry to delineate the specificity of Moluccella laevis lectin and monoclonal antibody 5F4 for the Tn antigen (GalNAc alpha 1-O-Ser/Thr). Immunol Lett 36: 239-243.
34. Burchell J, Gendler S, Taylor-Papadimitriou J, Girling A, Lewis A, 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.
35. Steentoft C, Vakhrushev SY, Vester-Christensen MB, Schjoldager KT, Kong Y, et al. (2011) Mining the O-glycoproteome using zinc-finger nuclease-glycoengineered SimpleCell lines. Nat Methods 8: 977-982 nmeth.1731 [pii];10.1038/nmeth.1731 [doi].
36. Meissner M, Reichert TE, Kunkel M, Gooding W, Whiteside TL, et al. (2005) Defects in the human leukocyte antigen class I antigen processing machinery in head and neck squamous cell carcinoma: association with clinical outcome. Clin Cancer Res 11: 2552-2560 11/7/2552 [pii];10.1158/1078-0432.CCR-04-2146 [doi].
37. Shields JD, Kourtis IC, Tomei AA, Roberts JM, Swartz MA, (2010) Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21. Science 328: 749-752 science.1185837 [pii];10.1126/science.1185837 [doi].
38. Shevach EM, (2004) Fatal attraction: tumors beckon regulatory T cells. Nat Med 10: 900-901 10.1038/nm0904-900 [doi];nm0904-900 [pii].
39. Nagaraj S, Gabrilovich DI, (2008) Tumor escape mechanism governed by myeloid-derived suppressor cells. Cancer Res 68: 2561-2563 68/8/2561 [pii];10.1158/0008-5472.CAN-07-6229 [doi].
40. Julien S, Adriaenssens E, Ottenberg K, Furlan A, Courtand G, et al. (2006) ST6GalNAc I expression in MDA-MB-231 breast cancer cells greatly modifies their O-glycosylation pattern and enhances their tumourigenicity. Glycobiology 16: 54-64 cwj033 [pii];10.1093/glycob/cwj033 [doi].
41. Chiricolo M, Malagolini N, Bonfiglioli S, Dall'Olio F, (2006) Phenotypic changes induced by expression of beta-galactoside alpha2,6 sialyltransferase I in the human colon cancer cell line SW948. Glycobiology 16: 146-154 cwj045 [pii];10.1093/glycob/cwj045 [doi].
42. Sorensen AL, Rumjantseva V, Nayeb-Hashemi S, Clausen H, Hartwig JH, et al. (2009) Role of sialic acid for platelet life span: exposure of beta-galactose results in the rapid clearance of platelets from the circulation by asialoglycoprotein receptor-expressing liver macrophages and hepatocytes. Blood 114: 1645-1654 blood-2009-01-199414 [pii];10.1182/blood-2009-01-199414 [doi].
43. Schauer R, (2009) Sialic acids as regulators of molecular and cellular interactions. Curr Opin Struct Biol 19: 507-514 S0959-440X(09)00095-5 [pii];10.1016/j.sbi.2009.06.003 [doi].
44. Avril T, Floyd H, Lopez F, Vivier E, Crocker PR, (2004) The membrane-proximal immunoreceptor tyrosine-based inhibitory motif is critical for the inhibitory signaling mediated by Siglecs-7 and-9, CD33-related Siglecs expressed on human monocytes and NK cells. J Immunol 173: 6841-6849 173/11/6841 [pii].
45. Kawasaki Y, Ito A, Withers DA, Taima T, Kakoi N, et al. (2010) Ganglioside DSGb5, preferred ligand for Siglec-7, inhibits NK cell cytotoxicity against renal cell carcinoma cells. Glycobiology 20: 1373-1379 cwq116 [pii];10.1093/glycob/cwq116 [doi].
46. Strilic B, Eglinger J, Krieg M, Zeeb M, Axnick J, et al. (2010) Electrostatic cell-surface repulsion initiates lumen formation in developing blood vessels. Curr Biol 20: 2003-2009 S0960-9822(10)01218-2 [pii];10.1016/j.cub.2010.09.061 [doi].
47. Johnson CP, Fujimoto I, Rutishauser U, Leckband DE, (2005) Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J Biol Chem 280: 137-145 M410216200 [pii];10.1074/jbc.M410216200 [doi].
48. Huppa JB, Davis MM, (2003) T-cell-antigen recognition and the immunological synapse. Nat Rev Immunol 3: 973-983 10.1038/nri1245 [doi];nri1245 [pii].
49. Hubert P, Heitzmann A, Viel S, Nicolas A, Sastre-Garau X, et al. (2011) Antibody-dependent cell cytotoxicity synapses form in mice during tumor-specific antibody immunotherapy. Cancer Res 71: 5134-5143 0008-5472.CAN-10-4222 [pii];10.1158/0008-5472.CAN-10-4222 [doi].
50. Liu D, Bryceson YT, Meckel T, Vasiliver-Shamis G, Dustin ML, et al. (2009) Integrin-dependent organization and bidirectional vesicular traffic at cytotoxic immune synapses. Immunity 31: 99-109 S1074-7613(09)00275-1 [pii];10.1016/j.immuni.2009.05.009 [doi].
51. Vakhrushev SY, Steentoft C, Vester-Christensen MB, Bennett EP, Clausen H, et al. (2013) Enhanced mass spectrometric mapping of the human GalNAc-type O-glycoproteome with SimpleCells. Mol Cell Proteomics 12: 932-944 O112.021972 [pii];10.1074/mcp.O112.021972 [doi].
52. Komatsu M, Yee L, Carraway KL, (1999) Overexpression of sialomucin complex, a rat homologue of MUC4, inhibits tumor killing by lymphokine-activated killer cells. Cancer Res 59: 2229-2236.
53. Komatsu M, Tatum L, Altman NH, Carothers Carraway CA, Carraway KL, (2000) Potentiation of metastasis by cell surface sialomucin complex (rat MUC4), a multifunctional anti-adhesive glycoprotein. Int J Cancer 87: 480-486 10.1002/1097-0215(20000815)87:4<480::AID-IJC4>3.0.CO;2-6 [pii].
54. Belisle JA, Horibata S, Jennifer GA, Petrie S, Kapur A, et al. (2010) Identification of Siglec-9 as the receptor for MUC16 on human NK cells, B cells, and monocytes. Mol Cancer 9: 118 1476-4598-9-118 [pii];10.1186/1476-4598-9-118 [doi].
55. McCann FE, Vanherberghen B, Eleme K, Carlin LM, Newsam RJ, et al. (2003) The size of the synaptic cleft and distinct distributions of filamentous actin, ezrin, CD43, and CD45 at activating and inhibitory human NK cell immune synapses. J Immunol 170: 2862-2870.
56. Vasir B, Avigan D, Wu Z, Crawford K, Turnquist S, et al. (2005) Dendritic cells induce MUC1 expression and polarization on human T cells by an IL-7-dependent mechanism. J Immunol 174: 2376-2386 174/4/2376 [pii].
57. Zhang QJ, Li XL, Wang D, Huang XC, Mathis JM, et al. (2008) Trogocytosis of MHC-I/peptide complexes derived from tumors and infected cells enhances dendritic cell cross-priming and promotes adaptive T cell responses. PLoS One 3: e3097 10.1371/journal.pone.0003097 [doi].
58. Beum PV, Peek EM, Lindorfer MA, Beurskens FJ, Engelberts PJ, et al. (2011) Loss of CD20 and bound CD20 antibody from opsonized B cells occurs more rapidly because of trogocytosis mediated by Fc receptor-expressing effector cells than direct internalization by the B cells. J Immunol 187: 3438-3447 jimmunol.1101189 [pii];10.4049/jimmunol.1101189 [doi].