Engineered CAR T Cells Targeting the Cancer-Associated Tn-Glycoform of the Membrane Mucin MUC1 Control Adenocarcinoma

Immunity

Volumn 44, Issue 6, 2016, Pages 1444-1454

  Posey, Avery D ^a   Schwab, Robert D ^a   Boesteanu, Alina C ^a   Steentoft, Catharina ^b   Mandel, Ulla ^b   Engels, Boris ^c,e   Stone, Jennifer D ^d   Madsen, Thomas D ^b   Schreiber, Karin ^c   Haines, Kathleen M ^a   Cogdill, Alexandria P ^a   Chen, Taylor J ^a   Song, Decheng ^a   Scholler, John ^a   Kranz, David M ^d   Feldman, Michael D ^a   Young, Regina ^a   Keith, Brian ^a   Schreiber, Hans ^c   Clausen, Henrik ^b   Johnson, Laura A ^a   June, Carl H ^a   more..

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF CHICAGO   (United States)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^e NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; CHIMERIC ANTIGEN RECEPTOR; EPITOPE; GLYCOPROTEIN; MUCIN 1; TN ANTIGEN; HYBRID PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR;

ADENOCARCINOMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER THERAPY; CELL ENGINEERING; CELL THERAPY; CONTROLLED STUDY; CYTOTOXICITY; GLYCOSYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOLOGICAL TOLERANCE; JURKAT CELL LINE; K562 CELL LINE; MOLECULAR PATHOLOGY; MOUSE; MULTIPLE CANCER; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOLID TUMOR; T CELL LEUKEMIA; T LYMPHOCYTE; TUMOR REJECTION; ANIMAL; CHEMISTRY; DRUG SCREENING; GENETIC ENGINEERING; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; INBRED MOUSE STRAIN; METABOLISM; PHYSIOLOGY; PROCEDURES; TUMOR CELL LINE;

ADENOCARCINOMA; ANIMALS; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; EPITOPES, T-LYMPHOCYTE; GENETIC ENGINEERING; GLYCOSYLATION; HUMANS; IMMUNOTHERAPY; JURKAT CELLS; MICE; MICE, INBRED STRAINS; MUCIN-1; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84975028839     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.05.014     Document Type: Article

References (51)

1. Andrulis M., Ellert E., Mandel U., Clausen H., Lehners N., Raab M.S., Goldschmidt H., Schwartz-Albiez R. Expression of Mucin-1 in multiple myeloma and its precursors: correlation with glycosylation and subcellular localization. Histopathology 2014, 64:799-806.
2. Bennett E.P., Mandel U., Clausen H., Gerken T.A., Fritz T.A., Tabak L.A. Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology 2012, 22:736-756.
3. Berger E.G. Tn-syndrome. Biochim. Biophys. Acta 1999, 1455:255-268.
4. Borgert A., Heimburg-Molinaro J., Song X., Lasanajak Y., Ju T., Liu M., Thompson P., Ragupathi G., Barany G., Smith D.F., et al. Deciphering structural elements of mucin glycoprotein recognition. ACS Chem. Biol. 2012, 7:1031-1039.
5. Brentjens R.J., Davila M.L., Riviere I., Park J., Wang X., Cowell L.G., Bartido S., Stefanski J., Taylor C., Olszewska M., et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci. Transl. Med. 2013, 5:177ra38.
6. Carpenito C., Milone M.C., Hassan R., Simonet J.C., Lakhal M., Suhoski M.M., Varela-Rohena A., Haines K.M., Heitjan D.F., Albelda S.M., et al. Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains. Proc. Natl. Acad. Sci. USA 2009, 106:3360-3365.
7. Cazet A., Julien S., Bobowski M., Burchell J., Delannoy P. Tumour-associated carbohydrate antigens in breast cancer. Breast Cancer Res. 2010, 12:204.
8. Cloosen S., Gratama J., van Leeuwen E.B., Senden-Gijsbers B.L., Oving E.B., von Mensdorff-Pouilly S., Tarp M.A., Mandel U., Clausen H., Germeraad W.T., Bos G.M. Cancer specific Mucin-1 glycoforms are expressed on multiple myeloma. Br. J. Haematol. 2006, 135:513-516.
9. Emens L.A., Asquith J.M., Leatherman J.M., Kobrin B.J., Petrik S., Laiko M., Levi J., Daphtary M.M., Biedrzycki B., Wolff A.C., et al. Timed sequential treatment with cyclophosphamide, doxorubicin, and an allogeneic granulocyte-macrophage colony-stimulating factor-secreting breast tumor vaccine: a chemotherapy dose-ranging factorial study of safety and immune activation. J. Clin. Oncol. 2009, 27:5911-5918.
10. Finn O.J., Gantt K.R., Lepisto A.J., Pejawar-Gaddy S., Xue J., Beatty P.L. Importance of MUC1 and spontaneous mouse tumor models for understanding the immunobiology of human adenocarcinomas. Immunol. Res. 2011, 50:261-268.
11. Gill D.J., Tham K.M., Chia J., Wang S.C., Steentoft C., Clausen H., Bard-Chapeau E.A., Bard F.A. Initiation of GalNAc-type O-glycosylation in the endoplasmic reticulum promotes cancer cell invasiveness. Proc. Natl. Acad. Sci. USA 2013, 110:E3152-E3161.
12. Graham R.A., Burchell J.M., Taylor-Papadimitriou J. The polymorphic epithelial mucin: potential as an immunogen for a cancer vaccine. Cancer Immunol. Immunother. 1996, 42:71-80.
13. Grupp S.A., Kalos M., Barrett D., Aplenc R., Porter D.L., Rheingold S.R., Teachey D.T., Chew A., Hauck B., Wright J.F., et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N. Engl. J. Med. 2013, 368:1509-1518.
14. Imai C., Mihara K., Andreansky M., Nicholson I.C., Pui C.H., Geiger T.L., Campana D. Chimeric receptors with 4-1BB signaling capacity provoke potent cytotoxicity against acute lymphoblastic leukemia. Leukemia 2004, 18:676-684.
15. Itzkowitz S. Colon carcinogenesis in inflammatory bowel disease: applying molecular genetics to clinical practice. J Clin Gastroenterol 2003, 36:S70-S74. discussion S94-76.
16. Ju T., Cummings R.D. A unique molecular chaperone Cosmc required for activity of the mammalian core 1 beta 3-galactosyltransferase. Proc. Natl. Acad. Sci. USA 2002, 99:16613-16618.
17. Ju T., Cummings R.D. Protein glycosylation: chaperone mutation in Tn syndrome. Nature 2005, 437:1252.
18. Ju T., Cummings R.D., Canfield W.M. Purification, characterization, and subunit structure of rat core 1 Beta1,3-galactosyltransferase. J. Biol. Chem. 2002, 277:169-177.
19. Ju T., Lanneau G.S., Gautam T., Wang Y., Xia B., Stowell S.R., Willard M.T., Wang W., Xia J.Y., Zuna R.E., et al. Human tumor antigens Tn and sialyl Tn arise from mutations in Cosmc. Cancer Res. 2008, 68:1636-1646.
20. Ju T., Xia B., Aryal R.P., Wang W., Wang Y., Ding X., Mi R., He M., Cummings R.D. A novel fluorescent assay for T-synthase activity. Glycobiology 2011, 21:352-362.
21. June C.H., Riddell S.R., Schumacher T.N. Adoptive cellular therapy: a race to the finish line. Sci. Transl. Med. 2015, 7:280ps7.
22. Kalos M., Levine B.L., Porter D.L., Katz S., Grupp S.A., Bagg A., June C.H. T cells expressing chimeric receptors establish memory and potent antitumor effects in patients with advanced leukemia. Sci. Transl. Med. 2011, 3:95ra73.
23. Kannagi R., Sakuma K., Miyazaki K., Lim K.T., Yusa A., Yin J., Izawa M. Altered expression of glycan genes in cancers induced by epigenetic silencing and tumor hypoxia: clues in the ongoing search for new tumor markers. Cancer Sci. 2010, 101:586-593.
24. *04:05-restricted, WT1-specific TCR gene into human CD4+ T cells confers killing activity against human leukemia cells. Anticancer Res. 2015, 35:1251-1261.
25. Kochenderfer J.N., Wilson W.H., Janik J.E., Dudley M.E., Stetler-Stevenson M., Feldman S.A., Maric I., Raffeld M., Nathan D.A., Lanier B.J., et al. Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood 2010, 116:4099-4102.
26. Lamers C.H., Sleijfer S., van Steenbergen S., van Elzakker P., van Krimpen B., Groot C., Vulto A., den Bakker M., Oosterwijk E., Debets R., Gratama J.W. Treatment of metastatic renal cell carcinoma with CAIX CAR-engineered T cells: clinical evaluation and management of on-target toxicity. Mol. Ther. 2013, 21:904-912.
27. Lin C.Y., Ho J.Y., Hsieh M.T., Chiang H.L., Chuang J.M., Whang-Peng J., Chang Y.C., Tseng Y.H., Chen S.F., Nieh S., Hwang J. Reciprocal relationship of Tn/NF-κB and sTn as an indicator of the prognosis of oral squamous cell carcinoma. Histopathology 2014, 64:713-721.
28. Madsen C.B., Lavrsen K., Steentoft C., Vester-Christensen M.B., Clausen H., Wandall H.H., Pedersen A.E. Glycan elongation beyond the mucin associated Tn antigen protects tumor cells from immune-mediated killing. PLoS ONE 2013, 8:e72413.
29. Maude S.L., Frey N., Shaw P.A., Aplenc R., Barrett D.M., Bunin N.J., Chew A., Gonzalez V.E., Zheng Z., Lacey S.F., et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N. Engl. J. Med. 2014, 371:1507-1517.
30. Mi R., Song L., Wang Y., Ding X., Zeng J., Lehoux S., Aryal R.P., Wang J., Crew V.K., van Die I., et al. Epigenetic silencing of the chaperone Cosmc in human leukocytes expressing tn antigen. J. Biol. Chem. 2012, 287:41523-41533.
31. Milone M.C., Fish J.D., Carpenito C., Carroll R.G., Binder G.K., Teachey D., Samanta M., Lakhal M., Gloss B., Danet-Desnoyers G., et al. Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Molecular therapy: the journal of the American Society of Gene Therapy 2009, 17:1453-1464.
32. Morgan R.A., Yang J.C., Kitano M., Dudley M.E., Laurencot C.M., Rosenberg S.A. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol. Ther. 2010, 18:843-851.
33. Ohno S., Ohno Y., Nakada H., Suzuki N., Soma G., Inoue M. Expression of Tn and sialyl-Tn antigens in endometrial cancer: its relationship with tumor-produced cyclooxygenase-2, tumor-infiltrated lymphocytes and patient prognosis. Anticancer Res. 2006, 26(6A):4047-4053.
34. Ohtsubo K., Marth J.D. Glycosylation in cellular mechanisms of health and disease. Cell 2006, 126:855-867.
35. Parry R.V., Rumbley C.A., Vandenberghe L.H., June C.H., Riley J.L. CD28 and inducible costimulatory protein Src homology 2 binding domains show distinct regulation of phosphatidylinositol 3-kinase, Bcl-xL, and IL-2 expression in primary human CD4 T lymphocytes. J. Immunol. 2003, 171:166-174.
36. Porter D.L., Levine B.L., Kalos M., Bagg A., June C.H. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med. 2011, 365:725-733.
37. Rabinovich G.A., Croci D.O. Regulatory circuits mediated by lectin-glycan interactions in autoimmunity and cancer. Immunity 2012, 36:322-335.
38. Radhakrishnan P., Dabelsteen S., Madsen F.B., Francavilla C., Kopp K.L., Steentoft C., Vakhrushev S.Y., Olsen J.V., Hansen L., Bennett E.P., et al. Immature truncated O-glycophenotype of cancer directly induces oncogenic features. Proc. Natl. Acad. Sci. USA 2014, 111:E4066-E4075.
39. Ren D., Jia L., Li Y., Gong Y., Liu C., Zhang X., Wang N., Zhao Y. ST6GalNAcII mediates the invasive properties of breast carcinoma through PI3K/Akt/NF-κB signaling pathway. IUBMB Life 2014, 66:300-308.
40. Sabbatini P.J., Ragupathi G., Hood C., Aghajanian C.A., Juretzka M., Iasonos A., Hensley M.L., Spassova M.K., Ouerfelli O., Spriggs D.R., et al. Pilot study of a heptavalent vaccine-keyhole limpet hemocyanin conjugate plus QS21 in patients with epithelial ovarian, fallopian tube, or peritoneal cancer. Clinical cancer research: an official journal of the American Association for Cancer Research 2007, 13:4170-4177.
41. Schietinger A., Philip M., Yoshida B.A., Azadi P., Liu H., Meredith S.C., Schreiber H. A mutant chaperone converts a wild-type protein into a tumor-specific antigen. Science 2006, 314:304-308.
42. Sørensen A.L., Reis C.A., Tarp M.A., Mandel U., Ramachandran K., Sankaranarayanan V., Schwientek T., Graham R., Taylor-Papadimitriou J., Hollingsworth M.A., et al. Chemoenzymatically synthesized multimeric Tn/STn MUC1 glycopeptides elicit cancer-specific anti-MUC1 antibody responses and override tolerance. Glycobiology 2006, 16:96-107.
43. Springer G.F. T and Tn, general carcinoma autoantigens. Science 1984, 224:1198-1206.
44. Stone J.D., Aggen D.H., Schietinger A., Schreiber H., Kranz D.M. A sensitivity scale for targeting T cells with chimeric antigen receptors (CARs) and bispecific T-cell Engagers (BiTEs). OncoImmunology 2012, 1:863-873.
45. Tamura F., Sato Y., Hirakawa M., Yoshida M., Ono M., Osuga T., Okagawa Y., Uemura N., Arihara Y., Murase K., et al. RNAi-mediated gene silencing of ST6GalNAc I suppresses the metastatic potential in gastric cancer cells. Gastric cancer: official journal of the International Gastric Cancer Association and the Japanese Gastric Cancer Association 2014.
46. Tarp M.A., Clausen H. Mucin-type O-glycosylation and its potential use in drug and vaccine development. Biochim. Biophys. Acta 2008, 1780:546-563.
47. Tarp M.A., Sørensen A.L., Mandel U., Paulsen H., Burchell J., Taylor-Papadimitriou J., Clausen H. Identification of a novel cancer-specific immunodominant glycopeptide epitope in the MUC1 tandem repeat. Glycobiology 2007, 17:197-209.
48. Taylor-Papadimitriou J., Burchell J., Miles D.W., Dalziel M. MUC1 and cancer. Biochim. Biophys. Acta 1999, 1455:301-313.
49. Van Elssen C.H., Frings P.W., Bot F.J., Van de Vijver K.K., Huls M.B., Meek B., Hupperets P., Germeraad W.T., Bos G.M. Expression of aberrantly glycosylated Mucin-1 in ovarian cancer. Histopathology 2010, 57:597-606.
50. Victorzon M., Nordling S., Nilsson O., Roberts P.J., Haglund C. Sialyl Tn antigen is an independent predictor of outcome in patients with gastric cancer. International journal of cancer. Journal international du cancer 1996, 65:295-300.
51. Wandall H.H., Blixt O., Tarp M.A., Pedersen J.W., Bennett E.P., Mandel U., Ragupathi G., Livingston P.O., Hollingsworth M.A., Taylor-Papadimitriou J., et al. Cancer biomarkers defined by autoantibody signatures to aberrant O-glycopeptide epitopes. Cancer Res. 2010, 70:1306-1313.