Antibody targeting of cell-bound MUC1 SEA domain kills tumor cells

Cancer Research

Volumn 72, Issue 13, 2012, Pages 3324-3336

  Pichinuk, Edward ^a   Benhar, Itai ^a   Jacobi, Oded ^a   Chalik, Michael ^a   Weiss, Lotem ^a   Ziv, Ravit ^a   Sympson, Carolyn ^b   Karwa, Amolkumar ^b   Smorodinsky, Nechama I ^a   Rubinstein, Daniel B ^c   Wreschner, Daniel H ^a,d  

^a TEL AVIV UNIVERSITY   (Israel)

^b MEDTRONIC INC   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d Biomodifying Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR 2; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY DMB5F3; MUCIN 1; TRASTUZUMAB; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BREAST CANCER; BREAST CARCINOMA; CANCER CELL; CANCER CELL CULTURE; CELL KILLING; CELL POPULATION; CELL SURFACE; CHO CELL; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG TARGETING; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNIZATION; INTERNALIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; TEMPERATURE; TUMOR CELL;

ANTIBODIES, MONOCLONAL; BLOTTING, WESTERN; CELL LINE, TUMOR; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; MUCIN-1;

EID: 84863570663     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-0067     Document Type: Article

References (48)

1. Baruch A, Hartmann M, Zrihan-Licht S, Greenstein S, Burstein M, Keydar I, et al. Preferential expression of novel MUC1 tumor antigen isoforms in human epithelial tumors and their tumor-potentiating function. Int J Cancer 1997;71:741-9. (Pubitemid 27237193)
2. Gendler SJ, Lancaster CA, Taylor-Papadimitriou J, Duhig T, Peat N, Burchell J, et al. Molecular cloning and expression of human tumor-associated polymorphic epithelial mucin. J Biol Chem 1990;265:15286-93.
3. Ligtenberg MJ, Vos HL, Gennissen AM, Hilkens J. Episialin, a carcinoma-associated mucin, is generated by a polymorphic gene encoding splice variants with alternative amino termini. J Biol Chem 1990;265:5573-8. (Pubitemid 20127185)
4. Levitin F, Stern O, Weiss M, Gil-Henn C, Ziv R, Prokocimer Z, et al. The MUC1 SEA module is a self-cleaving domain. J Biol Chem 2005;280:33374-86. (Pubitemid 41397135)
5. Lillehoj EP, Han F, Kim KC. Mutagenesis of a Gly-Ser cleavage site in MUC1 inhibits ectodomain shedding. Biochem Biophys Res Commun 2003;307:743-9. (Pubitemid 36944995)
6. Macao B, Johansson DG, Hansson GC, Hard T. Autoproteolysis coupled to protein folding in the SEA domain of the membrane-bound MUC1 mucin. Nat Struct Mol Biol 2006;13:71-6. (Pubitemid 43049405)
7. Ligtenberg MJ, Kruijshaar L, Buijs F, van Meijer M, Litvinov SV, Hilkens J. Cell-associated episialin is a complex containing two proteins derived from a common precursor. J Biol Chem 1992;267:6171-7.
8. O'Connor JC, Julian J, Lim SD, Carson DD. MUC1 expression in human prostate cancer cell lines and primary tumors. Prostate Cancer Prostatic Dis 2005;8:36-44.
9. Yonezawa S, Byrd JC, Dahiya R, Ho JJ, Gum JR, Griffiths B, et al. Differential mucin gene expression in human pancreatic and colon cancer cells. Biochem J 1991;276(Pt 3): 599-605.
10. Lapointe J, Li C, Higgins JP, van de Rijn M, Bair E, Montgomery K, et al. Gene expression profiling identifies clinically relevant subtypes of prostate cancer. Proc Natl Acad Sci U S A 2004;101:811-6. (Pubitemid 38121040)
11. Joshi MD, Ahmad R, Yin L, Raina D, Rajabi H, Bubley G, et al. MUC1 oncoprotein is a druggable target in human prostate cancer cells. Mol Cancer Ther 2009;8:3056-65.
12. Gold DV, Karanjawala Z, Modrak DE, Goldenberg DM, Hruban RH. PAM4-reactive MUC1 is a biomarker for early pancreatic adenocarcinoma. Clin Cancer Res 2007;13:7380-7.
13. Kawano T, Ahmad R, Nogi H, Agata N, Anderson K, Kufe D. MUC1 oncoprotein promotes growth and survival of human multiple myeloma cells. Int J Oncol 2008;33:153-9.
14. Cheever MA, Allison JP, Ferris AS, Finn OJ, Hastings BM, Hecht TT, et al. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin Cancer Res 2009;15:5323-37.
15. Prinssen HM, Molthoff CF, Verheijen RH, Broadhead TJ, Kenemans P, Roos JC, et al. Biodistribution of 111In-labelled engineered human antibody CTM01 (hCTM01) in ovarian cancer patients: influence of prior administration of unlabelled hCTM01. Cancer Immunol Immunother 1998;47:39-46. (Pubitemid 28430529)
16. Gillespie AM, Broadhead TJ, Chan SY, Owen J, Farnsworth AP, Sopwith M, et al. Phase I open study of the effects of ascending doses of the cytotoxic immunoconjugate CMB-401 (hCTMO1-calicheamicin) in patients with epithelial ovarian cancer. Ann Oncol 2000;11:735-41.
17. Pegram MD, Borges VF, Ibrahim N, Fuloria J, Shapiro C, Perez S, et al. Phase I dose escalation pharmacokinetic assessment of intravenous humanized anti-MUC1 antibody AS1402 in patients with advanced breast cancer. Breast Cancer Res 2009;11:R73.
18. Rubinstein DB, Karmely M, Ziv R, Benhar I, Leitner O, Baron S, et al. MUC1/X protein immunization enhances cDNA immunization in generating anti-MUC1 alpha/beta junction antibodies that target malignant cells. Cancer Res 2006;66:11247-53. (Pubitemid 46009953)
19. Mazor Y, Keydar I, Benhar I. Humanization and epitope mapping of the H23 anti-MUC1 monoclonal antibody reveals a dual epitope specificity. Mol Immunol 2005;42:55-69. (Pubitemid 39360927)
20. Keydar I, Chou CS, Hareuveni M, Tsarfaty I, Sahar E, Selzer G, et al. Production and characterization of monoclonal antibodies identifying breast tumor-associated antigens. Proc Natl Acad Sci U S A 1989;86:1362-6. (Pubitemid 19061546)
21. Rubinstein DB, Karmely M, Pichinuk E, Ziv R, Benhar I, Feng N, et al. The MUC1 oncoprotein as a functional target: immunotoxin binding to alpha/beta junction mediates cell killing. Int J Cancer 2009;124:46-54.
22. Engelmann K, Shen H, Finn OJ. MCF7 side population cells with characteristics of cancer stem/progenitor cells express the tumor antigen MUC1. Cancer Res 2008;68:2419-26. (Pubitemid 351521817)
23. Mazor Y, Barnea I, Keydar I, Benhar I. Antibody internalization studied using a novel IgG binding toxin fusion. J Immunol Methods 2007;321:41-59. (Pubitemid 46441195)
24. Ali HR, Dawson SJ, Blows FM, Provenzano E, Pharoah PD, Caldas C. Cancer stem cell markers in breast cancer: pathological, clinical and prognostic significance. Breast Cancer Res 2011;13:R118.
25. Kok M, Koornstra RH, Margarido TC, Fles R, Armstrong NJ, Linn SC, et al. Mammosphere-derived gene set predicts outcome in patients with ER-positive breast cancer. J Pathol 2009;218:316-26.
26. Hartman M, Baruch A, Ron I, Aderet Y, Yoeli M, Sagi-Assif O, et al. MUC1 isoform specific monoclonal antibody 6E6/2 detects preferential expression of the novel MUC1/Y protein in breast and ovarian cancer. Int J Cancer 1999;82:256-67. (Pubitemid 29293786)
27. Kufe DW. Mucins in cancer: function, prognosis and therapy. Nat Rev Cancer 2009;9:874-85.
28. Hamann PR, Hinman LM, Beyer CF, Lindh D, Upeslacis J, Shochat D, et al. A calicheamicin conjugate with a fully humanized anti-MUC1 antibody shows potent antitumor effects in breast and ovarian tumor xenografts. Bioconjug Chem 2005;16:354-60. (Pubitemid 40388211)
29. Koumarianou AA, Hudson M, Williams R, Epenetos AA, Stamp GW. Development of a novel bi-specific monoclonal antibody approach for tumour targeting. Br J Cancer 1999;81:431-9. (Pubitemid 29458796)
30. Snijdewint FG, von Mensdorff-Pouilly S, Karuntu-Wanamarta AH, Verstraeten AA, Livingston PO, Hilgers J, et al. Antibody-dependent cell-mediated cytotoxicity can be induced by MUC1 peptide vaccination of breast cancer patients. Int J Cancer 2001;93:97-106. (Pubitemid 32539508)
31. Troise F, Cafaro V, Giancola C, D'Alessio G, De Lorenzo C. Differential binding of human immunoagents and Herceptin to the ErbB2 receptor. FEBS J 2008;275:4967-79.
32. Thomas SM, Grandis JR. Pharmacokinetic and pharmacodynamic properties of EGFR inhibitors under clinical investigation. Cancer Treat Rev 2004;30:255-68. (Pubitemid 38477271)
33. Du X, Xiang L, Mackall C, Pastan I. Killing of resistant cancer cells with low Bak by a combination of an antimesothelin immunotoxin and a TRAIL Receptor 2 agonist antibody. Clin Cancer Res 2011;17:5926-34.
34. Kreitman RJ, Pastan I. Antibody fusion proteins: anti-CD22 recombinant immunotoxin moxetumomab pasudotox. Clin Cancer Res 2011;17:6398-405.
35. Vincenzi B, Santini D, Tonini G. New issues on cetuximab mechanism of action in epidermal growth factor receptor-negative colorectal cancer: the role of vascular endothelial growth factor. J Clin Oncol 2006;24:1957; author reply 1957-1958.
36. Hudis CA. Trastuzumab-mechanism of action and use in clinical practice. N Engl J Med 2007;357:39-51. (Pubitemid 47026733)
37. Gualberto A. Brentuximab Vedotin (SGN-35), an antibody-drug conjugate for the treatment of CD30-positive malignancies. Expert Opin Investig Drugs 2012;21:205-16.
38. Lievre A, Bachet JB, Boige V, Cayre A, Le Corre D, Buc E, et al. KRAS mutations as an independent prognostic factor in patients with advanced colorectal cancer treated with cetuximab. J Clin Oncol 2008;26:374-9. (Pubitemid 351171687)
39. Di Fiore F, Blanchard F, Charbonnier F, Le Pessot F, Lamy A, Galais MP, et al. Clinical relevance of KRAS mutation detection in metastatic colorectal cancer treated by Cetuximab plus chemotherapy. Br J Cancer 2007;96:1166-9. (Pubitemid 46625066)
40. Modi S, D'Andrea G, Norton L, Yao TJ, Caravelli J, Rosen PP, et al. A phase I study of cetuximab/paclitaxel in patients with advanced-stage breast cancer. Clin Breast Cancer 2006;7:270-7. (Pubitemid 44445741)
41. Okines AF, Cunningham D. Trastuzumab in gastric cancer. Eur J Cancer 2010;46:1949-59.
42. Clynes R, Takechi Y, Moroi Y, Houghton A, Ravetch JV. Fc receptors are required in passive and active immunity to melanoma. Proc Natl Acad Sci U S A 1998;95:652-6. (Pubitemid 28083798)
43. Ragupathi G, Liu NX, Musselli C, Powell S, Lloyd K, Livingston PO. Antibodies against tumor cell glycolipids and proteins, but not mucins, mediate complement-dependent cytotoxicity. J Immunol 2005;174:5706-12. (Pubitemid 40593213)
44. Gilewski T, Adluri S, Ragupathi G, Zhang S, Yao TJ, Panageas K, et al. Vaccination of high-risk breast cancer patients with mucin-1 (MUC1) keyhole limpet hemocyanin conjugate plus QS-21. Clin Cancer Res 2000;6:1693-701. (Pubitemid 30305061)
45. Ding C, Wang L, Marroquin J, Yan J. Targeting of antigens to B cells augments antigen-specific T-cell responses and breaks immune tolerance to tumor-associated antigen MUC1. Blood 2008;112:2817-25.
46. Ramanathan RK, Lee KM, McKolanis J, Hitbold E, Schraut W, Moser AJ, et al. Phase I study of aMUC1vaccine composed of different doses of MUC1 peptide with SB-AS2 adjuvant in resected and locally advanced pancreatic cancer. Cancer Immunol Immunother 2005;54:254-64. (Pubitemid 40174243)
47. Lepisto AJ, Moser AJ, Zeh H, Lee K, Bartlett D, McKolanis JR, et al. A phase I/II study of a MUC1 peptide pulsed autologous dendritic cell vaccine as adjuvant therapy in patients with resected pancreatic and biliary tumors. Cancer Ther 2008;6:955-64.
48. Karanikas V, Hwang LA, Pearson J, Ong CS, Apostolopoulos V, Vaughan H, et al. Antibody and T cell responses of patients with adenocarcinoma immunized with mannan-MUC1 fusion protein. J Clin Invest 1997;100:2783-92. (Pubitemid 28007547)