T cells recognize PD(N/T)R motif common in a variable number of tandem repeat and degenerate repeat sequences of MUC1

International Immunopharmacology

Volumn 5, Issue 2, 2005, Pages 315-330

  Pisarev, Vladimir M ^a   Kinarsky, Leo ^a   Caffrey, Thomas ^a   Hanisch, Franz George ^b   Sanderson, Sam ^c   Hollingsworth, Michael A ^a   Sherman, Simon ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b Ctrl Bioanalytics Ctr Molec M   (Germany)

^c NEBRASKA MEDICAL CENTER   (United States)

Author keywords

C5a derived peptide; Class I MHC binding; Cross reactive T cell epitopes; Degenerate tandem repeat MUC1; ELISPOT; Mucin

Indexed keywords

COMPLEMENT COMPONENT C5A; EPITOPE; HLA A2 ANTIGEN; MUCIN 1; PEPTIDE DERIVATIVE; PHENYLALANYLALANYLPROLYLGLYCYLASPARAGINYLTYROSYLPROLYLALANYLLEUCINE; SERYLALANYLPROLYLASPARTYLASPARAGINYLARGINYLPROLYLALANYLLEUCINE; SERYLALANYLPROLYLASPARTYLTHREONYLARGINYLPROLYLALANYLPROLINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBODY SPECIFICITY; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CROSS REACTION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; FEMALE; IMMUNE RESPONSE; MOLECULAR MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN STRUCTURE; T LYMPHOCYTE; VARIABLE NUMBER OF TANDEM REPEAT;

ANIMALS; ANTIBODIES, MONOCLONAL; BINDING SITES, ANTIBODY; CA-15-3 ANTIGEN; CANCER VACCINES; CELL LINE; EPITOPES, T-LYMPHOCYTE; FEMALE; GENES, MHC CLASS I; H-2 ANTIGENS; HLA-A2 ANTIGEN; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; SPLEEN; T-LYMPHOCYTES; TANDEM REPEAT SEQUENCES;

EID: 12344255938     PISSN: 15675769     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.intimp.2004.10.004     Document Type: Article

References (72)

1. J. Fontenot, S. Mariappan, P. Catasti, N. Domenech, and O. Finn Structure of a tumor associated antigen containing a tandemly repeated immunodominant epitope J. Biomol. Struct. Dyn. 13 1995 245 260
2. S. Muller, K. Alving, J. Peter-Katalinic, N. Zachara, A. Gooley, and F.G. Hanisch High density O-glycosylation on tandem repeat peptide from secretory MUC1 of T47D breast cancer cells J. Biol. Chem. 274 1999 18165 18172
3. F. Hanisch, and S. Muller MUC1: the polymorphic appearance of a human mucin Glycobiology 10 2000 439 449
4. M. Hollingsworth, and B. Swanson Mucins in cancer: protection and control of the cell surface Nat. Rev. Cancer 4 2004 45 60
5. K. Nakagawa, J. Akagi, E. Takai, Y. Tamori, T. Okino, and H. Kako Prognostic values of MUC-1 molecule expressing cytokine receptor-like epitope and DF3 in patients with gastric carcinoma Int. J. Oncol. 14 1999 425 435
6. S. Treon, J. Mollick, M. Urashima, G. Teoh, D. Chauhan, and A. Ogata Muc-1 core protein is expressed on multiple myeloma cells and is induced by dexamethasone Blood 93 1999 1287 1298
7. T. Tanimoto, S. Tanaka, K. Haruma, M. Yoshihara, K. Sumii, and G. Kajiyama MUC1 expression in intramucosal colorectal neoplasms. Possible involvement in histogenesis and progression Oncology 56 1999 223 231
8. V. Dyomin, N. Palanisamy, K. Lloyd, K. Dyomina, S. Jhanwar, and J. Houldsworth MUC1 is activated in a B-cell lymphoma by the t(1;14)(q21;q32) translocation and is rearranged and amplified in B-cell lymphoma subsets Blood 95 2000 2666 2671
9. J. Taylor-Papadimitriou, J. Burchell, T. Plunkett, R. Graham, I. Correa, and D. Miles J. Mammary Gland Biol. Neoplasia 7 2002 209 221
10. M. Croce, A. Colussi, M. Price, and A. Segal-Eiras Expression of tumour associated antigens in normal, benign and malignant human mammary epithelial tissue: a comparative immunohistochemical study Anticancer Res. 17 1997 4287 4297
11. Y. Dong, M. Walsh, C. Cummings, R. Wright, and S. Khoo Expression of MUC1 and MUC2 mucins in epithelial ovarian tumours J. Pathol. 183 1997 311 317
12. O. Finn, K. Jerome, R. Henderson, G. Pecher, and N. Domenech MUC-1 epithelial tumor mucin-based immunity and cancer vaccines Immunol. Rev. 145 1995 61 89
13. V. Apostolopoulos, G. Pietersz, P. Xing, C.J. Lees, M. Michael, and J. Bishop The immunogenicity of MUC1 peptides and fusion protein Cancer Lett. 90 1995 21 26
14. R. Graham, J. Burchell, and J. Taylor-Papadimitriou The polymorphic epithelial mucin: potential as an immunogen for a cancer vaccine Cancer Immunol. Immunother. 42 1996 71 80
15. T. Gilewski, S. Adluri, G. Ragupathi, S. Zhang, T. Yao, and K. Panageas Vaccination of high-risk breast cancer patients with mucin-1 (MUC1) keyhole limpet hemocyanin conjugate plus QS-21 Clin. Cancer Res. 6 2000 1693 1701
16. G. Pecher, A. Haring, L. Kaiser, and E. Thiel Mucin gene (MUC1) transfected dendritic cells as vaccine: results of a phase I/II clinical trial Cancer Immunol. Immunother. 51 2002 669 673
17. J. Samuel, W.A. Budzynski, M.A. Reddish, L. Ding, G.L. Zimmermann, and M.J. Krantz Immunogenicity and antitumor activity of a liposomal MUC1 peptide-based vaccine Int. J. Cancer 75 1998 295 302
18. S. Zhang, L. Graeber, F. Helling, G. Ragupathi, S. Adluri, and K. Lloyd Augmenting the immunogenicity of synthetic MUC1 peptide vaccines in mice Cancer Res. 56 1996 3315 3319
19. D. Gold, T. Cardillo, Y. Vardi, and R. Blumenthal Radioimmunotherapy of experimental pancreatic cancer with 131I-labeled monoclonal antibody PAM4 Int. J. Cancer 71 1997 660 667
20. T. Cardillo, R. Blumenthal, Z. Ying, and D. Gold Combined gemcitabine and radioimmunotherapy for the treatment of pancreatic cancer Int. J. Cancer 97 2002 386 392
21. D. Goldenberg Targeted therapy of cancer with radiolabeled antibodies J. Nucl. Med. 43 2002 693 713
22. C. Richman, and S. DeNardo Systemic radiotherapy in metastatic breast cancer using 90Y-linked monoclonal MUC-1 antibodies Crit. Rev. Oncol. Hematol. 38 2001 25 35
23. C. Heuser, M. Ganser, A. Hombach, H. Brand, G. Denton, and F. Hanisch An anti-MUC1-antibody-interleukin-2 fusion protein that activates resting NK cells to lysis of MUC1-positive tumour cells Br. J. Cancer 89 2003 1130 1139
24. J. Akagi, J.W. Hodge, J.P. McLaughlin, L. Gritz, G. Mazzara, and D. Kufe Therapeutic antitumor response after immunization with an admixture of recombinant vaccinia viruses expressing a modified MUC1 gene and the murine T-cell costimulatory molecule B7 J. Immunother. 20 1997 38 47
25. R. Graham, J. Burchell, P. Beverley, and J. Taylor-Papadimitriou Intramuscular immunisation with MUC1 cDNA can protect C57 mice challenged with MUC1-expressing syngeneic mouse tumour cells Int. J. Cancer 65 1996 664 670
26. H. Guan, W. Budzynski, R. Koganty, M. Krantz, M. Reddish, and J. Rogers Liposomal formulations of synthetic MUC1 peptides: effects of encapsulation versus surface display of peptides on immune responses Bioconjug. Chem. 9 1998 451 458
27. H. Johnen, H. Kulbe, and G. Pecher Long-term tumor growth suppression in mice immunized with naked DNA of the human tumor antigen mucin (MUC1) Cancer Immunol. Immunother. 50 2001 356 3560
28. M. Kamata, K. Denda-Nagai, N. Kubota, S. Aida, K. Takeda, and T. Irimura Vaccination of mice with MUC1 cDNA suppresses the development of lung metastases Clin. Exp. Metastasis 19 2002 689 696
29. K. Kontani, O. Taguchi, Y. Ozaki, J. Hanaoka, and N. Tezuka Novel vaccination protocol consisting of injecting MUC1 DNA and nonprimed dendritic cells at the same region greatly enhanced MUC1-specific antitumor immunity in a murine model Cancer Gene Ther. 9 2002 330 337
30. K. Kontani, O. Taguchi, Y. Ozaki, J. Hanaoka, S. Sawai, and S. Inoue Dendritic cell vaccine immunotherapy of cancer targeting MUC1 mucin Int. J. Mol. Med. 12 2003 493 502
31. F. Snijdewint, S. von Mensdorff-Pouilly, A. Karuntu-Wanamarta, A. Verstraeten, P.O. Livingston, and J. Hilgers Antibody-dependent cell-mediated cytotoxicity can be induced by MUC1 peptide vaccination of breast cancer patients Int. J. Cancer 93 2001 97 106
32. V. Apostolopoulos, J. Haurum, and I. McKenzie MUC1 peptide epitopes associated with five different H-2 class I molecules Eur. J. Immunol. 27 1997 2579 2587
33. P. Brossart, K. Heinrich, G. Stuhler, L. Behnke, V. Reichardt, and S. Stevanovic Identification of HLA-A2-restricted T-cell epitopes derived from the MUC1 tumor antigen for broadly applicable vaccine therapies Blood 93 1999 4309 4317
34. A. Vlad, J. Kettel, N. Alajez, C. Carlos, and O. Finn MUC1 immunobiology: from discovery to clinical applications Adv. Immunol. 82 2004 249 293
35. L. Ding, E. Lalani, M. Reddish, R. Koganty, T. Wong, and J. Samuel Immunogenicity of synthetic peptides related to the core peptide sequence encoded by the human MUC1 mucin gene: effect of immunization on the growth of murine mammary adenocarcinoma cells transfected with the human MUC1 gene Cancer Immunol. Immunother. 36 1993 9 17
36. N. Domenech, R. Henderson, and O. Finn Identification of an HLA-A11-restricted epitope from the tandem repeat domain of the epithelial tumor antigen mucin J. Immunol. 155 1995 4766 4774
37. L. Heukamp, T. van Hall, F. Ossendorp, J. Burchell, C. Melief, and J. Taylor-Papadimitriou Effective immunotherapy of cancer in MUC1-transgenic mice using clonal cytotoxic T lymphocytes directed against an immunodominant MUC1 epitope J. Immunother. 25 2002 46 56
38. S. von Mensdorff-Pouilly, E. Petrakou, P. Kenemans, K. van Uffelen, A.A. Verstraeten, and F.G. Snijdewint Reactivity of natural and induced human antibodies to MUC1 mucin with MUC1 peptides and n-acetylgalactosamine (GalNAc) peptides Int. J. Cancer 86 2002 702 712
39. P. Xing, C. Lees, J. Lodding, J. Prenzoska, and G. Poulos Mouse mucin 1 (MUC1) defined by monoclonal antibodies Int. J. Cancer 76 1998 875 883
40. M.R. Price, P.D. Rye, E. Petrakou, A. Murray, K. Brady, and S. Imai Summary report on the ISOBM TD-4 Workshop: analysis of 56 monoclonal antibodies against the MUC1 mucin. San Diego, Calif., November 17-23, 1996 Tumour Biol. 19 Suppl. 1 1998 1 20
41. L. Carmon, K.M. El-Shami, A. Paz, S. Pascolo, E. Tzehoval, and B. Tirosh Novel breast-tumor-associated MUC1-derived peptides: characterization in Db-/- x beta2 microglobulin (beta2m) null mice transgenic for a chimeric HLA-A2.1/Db-beta2 microglobulin single chain Int. J. Cancer 85 2000 391 397
42. L.C. Heukamp, S.H. van der Burg, J.W. Drijfhout, C.J. Melief, J. Taylor-Papadimitriou, and R. Offringa Identification of three non-VNTR MUC1-derived HLA-A*0201-restricted T-cell epitopes that induce protective anti-tumor immunity in HLA-A2/K(b)-transgenic mice Int. J. Cancer 91 2001 385 392
43. T. Plunkett, R. Graham, I. Correa, R. Sewell, D. Miles, and J. Burchell Protection against MUC1 expressing mouse tumours by intra-muscular injection of MUC1 cDNA requires functional CD8+ and CD4+ T cells but does not require the MUC1 tandem repeat domain Int. J. Cancer 109 2004 691 697
44. K. Tsang, C. Palena, J. Gulley, P. Arlen, and J. Schlom A human cytotoxic T-lymphocyte epitope and its agonist epitope from the nonvariable number of tandem repeat sequence of MUC-1 Clin. Cancer Res. 10 2004 2139 2149
45. C. Lees, V. Apostolopoulos, and I. McKenzie Cytokine production from murine CD4 and CD8 cells after mannan-MUC1 immunization J. Interferon Cytokine Res. 19 1999 1373 1379
46. P. Mukherjee, C.S. Madsen, A.R. Ginardi, T.L. Tinder, F. Jacobs, and J. Parker Mucin 1-specific immunotherapy in a mouse model of spontaneous breast cancer J. Immunother. 26 2003 47 62
47. V. Karanikas, J. Lodding, V. Maino, and I. McKenzie Flow cytometric measurement of intracellular cytokines detects immune responses in MUC1 immunotherapy Clin. Cancer Res. 6 2000 829 837
48. J. Sandberg, P. Grufman, E. Wolpert, L. Franksson, B. Chambers, and K. Karre Superdominance among immunodominant H-2Kb-restricted epitopes and reversal by dendritic cell-mediated antigen delivery J. Immunol. 160 1998 3163 3169
49. S. Sanderson, L. Kirnarsky, S. Sherman, J. Ember, and Finch Agonists of human C5a: the relationship between conformation and spasmogenic and platelet aggregatory activities J. Med. Chem. 37 1994 3171 3180
50. S. Vogen, O. Prakash, L. Kirnarsky, S. Sanderson, and S. Sherman Determination of structural elements related to the biological activities of a potent decapeptide agonist of human C5a anaphylatoxin J. Pept. Res. 54 1999 74 84
51. S. Taylor, S. Sherman, L. Kirnarsky, and S. Sanderson Development of response-selective agonists of human C5a anaphylatoxin: conformational, biological, and therapeutic considerations Curr. Med. Chem. 8 2001 675 684
52. R.M. Tempero, M.A. Hollingsworth, M.D. Burdick, A.M. Finch, S.M. Taylor, and S.M. Vogen Molecular adjuvant effects of a conformationally biased agonist of human C5a anaphylatoxin J. Immunol. 158 1997 1377 1382
53. J. Ulrich, W. Cieplak, N. Paczkowski, S. Taylor, and S. Sanderson Induction of an antigen-specific CTL response by a conformationally biased agonist of human C5a anaphylatoxin as a molecular adjuvant J. Immunol. 164 2000 5492 5498
54. S.D. Sanderson, S.R. Cheruku, M.P. Padmanilayam, J.L. Vennerstrom, G.M. Thiele, and M.I. Palmatier Immunization to nicotine with a peptide-based vaccine composed of a conformationally biased agonist of C5a as a molecular adjuvant Int. Immunopharmacol. 3 2003 137 146
55. M.L. Andersen, M. Ruhwald, M. Thorn, A.E. Pedersen, S. Mathiassen, and S. Buus Tumor-associated antigens identified by mRNA expression profiling as tumor rejection epitopes J. Immune 2003 Based Ther. Vaccines 1 2003 1 9
56. V. Pisarev, B. Yu, R. Salup, S. Sherman, D.C. Altieri, and D.I. Gabrilovich Full-length dominant-negative survivin for cancer immunotherapy Clin. Cancer Res. 9 2003 6523 6533
57. V.M. Pisarev, P. Parajuli, R.L. Mosley, J. Chavez, D. Zimmerman, and D. Winship Flt3 ligand and conjugation to IL-1beta peptide as adjuvants for a type 1, T-cell response to an HIV p17 gag vaccine Vaccine 20 2002 2358 2368
58. B. Yu, S. Kusmartsev, F. Cheng, M. Paolini, Y. Nefedova, and E. Sotomayor Effective combination of chemotherapy and dendritic cell administration for the treatment of advanced-stage experimental breast cancer Clin. Cancer Res. 9 2003 285 294
59. V.M. Pisarev, P. Parajuli, R.L. Mosley, J. Sublet, L. Kelsey, and P.S. Sarin Flt3 ligand enhances the immunogenicity of a gag-based HIV-1 vaccine Int. J. Immunopharmacol. 22 2000 865 876
60. M. Saper, P. Bjorkman, and D. Wiley Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 A resolution J. Mol. Biol. 219 1991 277 319
61. W. Zhang, A. Young, M. Imarai, S. Nathenson, and J. Sacchettini Crystal structure of the major histocompatibility complex class I H-2Kb molecule containing a single viral peptide: implications for peptide binding and T-cell receptor recognition Proc. Natl. Acad. Sci. 89 1992 8403 8407
62. A. Young, W. Zhang, J. Sacchettini, and S. Nathenson The three-dimensional structure of H-2Db at 2.4 A resolution: implications for antigen-determinant selection Cell 76 1994 39 50
63. V. Apostolopoulos, V. Karanikas, J. Haurum, and I. McKenzie Induction of HLA-A2-restricted CTLs to the mucin 1 human breast cancer antigen J. Immunol. 159 1997 5211 5218
64. V. Apostolopoulos, G. Chelvanayagam, P. Xing, and I. McKenzie Anti-MUC1 antibodies react directly with MUC1 peptides presented by class I H-2 and HLA molecules J. Immunol. 161 1998 767 775
65. P. Dokurno, P. Bates, H. Band, L. Stewart, and J. Lally Crystal structure at 1.95 A resolution of the breast tumour-specific antibody SM3 complexed with its peptide epitope reveals novel hypervariable loop recognition J. Mol. Biol. 284 1998 713 728
66. S. Briggs, M. Price, and S. Tendler Fine specificity of antibody recognition of carcinoma-associated epithelial mucins: antibody binding to synthetic peptide epitopes Eur. J. Cancer 29A 1993 230 237
67. A. Morelli, A. Larregina, I. Chuluyan, E. Kolkowski, and L. Fainboim Expression and modulation of C5a receptor (CD88) on skin dendritic cells. Chemotactic effect of C5a on skin migratory dendritic cells Immunology 89 1996 126 134
68. A. Morelli, A. Larregina, E. Chuluyan, E. Kolkowski, and L. Fainboim Functional expression and modulation of C5a receptor (CD88) on skin dendritic cells Adv. Exp. Med. Biol. 417 1997 133 138
69. K. Kirchhoff, O. Weinmann, J. Zwirner, G. Begemann, O. Gotze, and A. Kapp Detection of anaphylatoxin receptors on CD83+ dendritic cells derived from human skin Immunology 103 2001 210 217
70. O. Weinmann, R. Gutzmer, J. Zwirner, M. Wittmann, K. Langer, and M. Lisewski Up-regulation of C5a receptor expression and function on human monocyte derived dendritic cells by prostaglandin E2 Immunology 110 2003 458 465
71. A. Soruri, J. Riggert, T. Schlott, Z. Kiafard, C. Dettmer, and J. Zwirner Anaphylatoxin C5a induces monocyte recruitment and differentiation into dendritic cells by TNF-alpha and prostaglandin E2-dependent mechanisms J. Immunol. 171 2003 2631 2636
72. S. Joshi, P. Wang, and S. Sanderson Enhanced antitumor immunostimulatory effects of human dendritic cells primed with conformationally biased response-selective C5a agonist decapeptide Proc. AACR. vol. 44 2003 American Association for Cancer Research Inc. Washington, DC 557