Targeting TARP, a novel breast and prostate tumor-associated antigen, with T cell receptor-like human recombinant antibodies

European Journal of Immunology

Volumn 38, Issue 6, 2008, Pages 1706-1720

  Epel, Malka ^a   Carmi, Irit ^a   Soueid Baumgarten, Sharon ^a   Oh, SangKon ^b   Bera, Tapan ^b   Pastan, Ira ^b   Berzofsky, Jay ^b   Reiter, Yoram ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Immunotoxin; MHC; Recombinant antibody; T cell receptor

Indexed keywords

HLA A2 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN; RECOMBINANT ANTIBODY; T LYMPHOCYTE RECEPTOR GAMMA ALTERNATE READING FRAME PROTEIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; T LYMPHOCYTE RECEPTOR LIKE RECOMBINANT ANTIBODY; TUMOR ANTIGEN; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BACTERIAL TOXIN; EPITOPE; EXOTOXIN; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOTOXIN; LYMPHOCYTE ANTIGEN RECEPTOR; MONOCLONAL ANTIBODY; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NUCLEAR PROTEIN; PEPTIDE FRAGMENT; RECOMBINANT PROTEIN; TARP; TOXA PROTEIN, PSEUDOMONAS AERUGINOSA; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY COMBINING SITE; ANTIBODY DETECTION; ANTIBODY SPECIFICITY; ANTIGEN ANTIBODY COMPLEX; ANTIGEN PRESENTING CELL; ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CELL SURFACE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; GENE FUSION; HUMAN; HUMAN CELL; IMMUNOTOXICITY; MOUSE; NONHUMAN; PHAGE DISPLAY; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; AMINO ACID SUBSTITUTION; ANIMAL; BIOSYNTHESIS; BREAST TUMOR; DRUG SCREENING; EXPERIMENTAL NEOPLASM; FEMALE; GENETICS; IMMUNOLOGY; MALE; MOLECULAR GENETICS; NUDE MOUSE; PATHOLOGY; PROSTATE TUMOR; TUMOR CELL LINE;

ADP RIBOSE TRANSFERASES; AMINO ACID SUBSTITUTION; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS; BACTERIAL TOXINS; BREAST NEOPLASMS; CELL LINE, TUMOR; EPITOPES, T-LYMPHOCYTE; EXOTOXINS; FEMALE; HLA-A2 ANTIGEN; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; IMMUNOTOXINS; MALE; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, NUDE; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PEPTIDE FRAGMENTS; PROSTATIC NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT PROTEINS; VIRULENCE FACTORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 49649129991     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200737524     Document Type: Article

References (70)

1. Saffran, D. C., Reiter, R. E., Jakobovits, A. and Witte, O. N., Target antigens for prostate cancer immunotherapy. Cancer Metastasis Rev. 1999. 18: 437-449.
2. Chakraborty; N. G., Stevens, R. L., Mehrotra, S., Laska, E., Taxel, P., Sporn, J. R., Schauer, P. et al., Recognition of PSA-derived peptide antigens by T cells from prostate cancer patients without anyprior stimulation. Cancer Immunol. Immunother. 2003. 52: 497-505.
3. Schroers, R., Shen, L., Rollins, L., Xiao, Z., Sonderstrup, G., Slawin, K., Huang, X. F. et al., Identification of MHC class II-restricted T-cell epitopes in prostate-specific membrane antigen. Clin. Cancer Res. 2003. 9: 3260-3271.
4. Dannull, J., Diener, P. A., Prilder, L., Furstenberger, G., Cerny, T., Schmid, U., Ackermarm, D. K. et al., Prostate stem cell antigen is a promising candidate for immunotherapy of advanced prostate cancer. Cancer Res. 2000. 60: 5522-5528.
5. + T cells in prostate cancer patients. Int. J. Cancer 2002. 102: 390-397.
6. Inoue, Y., Takaue, Y., Takei, M., Kato, K., Kanai, S., Harada, Y., Tobisu, K. et al., Induction of tumor specific cytotoxic T lymphocytes in prostate cancer using prostatic acid phosphatase derived HLA-A2402 binding peptide. J. Urol. 2001. 166: 1508-1513.
7. Noguchi, M., Kobayashi, K., Suetsugu, N., Tomiyasu, K., Suekane, S., Yamada, A., Itoh, K. et al., Induction of cellular and humoral immune responses to tumor cells and peptides in HLA-A24 positive hormone-refractory prostate cancer patients by peptide vaccination. Prostate 2003. 57: 80-92.
8. Murphy, G. P., Tjoa, B. A., Simmons, S. J., Ragde, H., Rogers, M., Elgamal, A., Kenny, G. M. et al., Phase II prostate cancer vaccine trial: Report of a study involving 37 patients with disease recurrence following primary treatment. Prostate 1999. 39: 54-59.
9. Murphy, G. P., Tjoa, B. A., Simmons, S. J., Jarisch, J., Bowes, V. A., Ragde, H., Rogers,M. et al., Infusion of dendritic cells pulsed with HLA-A2-specific prostate-specific membrane antigen peptides: A phase II prostate cancer vaccine trial involving patients with hormone-refractory metastatic disease. Prostate 1999. 38: 73-78.
10. Pavlenko, M., Roos, A. K., Lundqvist, A., Palmborg, A., Miller, A. M., Ozenci, V., Bergman, B. et al., A phase I trial of DNA vaccination with a plasmid expressing prostate-specific antigen in patients with hormone-refractory prostate cancer. Br. J. Cancer 2004. 91: 688-694.
11. Fong, L., Brockstedt, D., Benike, C., Breen, J. K., Strang, G., Ruegg, C. L. and Engleman, E. G., Dendritic cell-based xenoantigen vaccination for prostate cancer immunotherapy. J. Immunol. 2001. 167: 7150-7156.
12. Brinkmann, U., Vasmatzis, G., Lee, B., Yerushalmi, N., Essand, M. and Pastan, I., PAGE-1, an X chromosome-linked GAGE-like gene that is expressed in normal and neoplastic prostate, testis, and uterus. Proc. Natl. Acad. Sci. USA 1998. 95: 10757-10762.
13. Olsson, P., Bera, T. K., Essand, M., Kumar, V., Duray, P., Vincent, J., Lee, B. and Pastan, I., GDEP, a new gene differentially expressed in normal prostate and prostate cancer. Prostate 2001. 48: 231-241.
14. Bera, T. K., Iavarone, C., Kumar, V., Lee, S., Lee, B. and Pastan, I., MRP9, an unusual truncated member of the ABC transporter superfamily, is highly expressed in breast cancer. Proc. Natl. Acad. Sci. USA 2002. 99: 6997-7002.
15. Essand, M., Vasmatzis, G., Brinkmann, U., Duray, P., Lee, B. and Pastan, I., High expression of a specific T-cell receptor gamma transcript in epithelial cells of the prostate. Proc. Natl. Acad. Sci. USA 1999. 96: 9287-9292.
16. Wolfgang, C. D., Essand, M., Vincent, J. J., Lee, B. and Pastan, I., TARP: A nuclear protein expressed in prostate and breast cancer cells derived from an alternate reading frame of the T cell receptor gamma chain locus. Proc. Natl. Acad. Sci. USA 2000. 97: 9437-9442.
17. Oh, S., Terabe, M., Pendleton, C. D., Bhattacharyya, A., Bera, T. K., Epel, M., Reiter, Y. et al., Human CTLs to wild-type and enhanced epitopes of a novel prostate and breast tumor-associated protein, TARP, lyse human breast cancer cells. Cancer Res. 2004. 64: 2610-2618.
18. Wulfing, C. and Pluckthun, A., Correctly folded T-cell receptor fragments in the periplasm of Escherichia coli. Influence of folding catalysts. J. Mol. Biol. 1994. 242: 655-669.
19. Corr, M., Slanetz, A. E., Boyd, L. F., Jelonek, M. T., Khilko, S., al Ramadi, B. K., Kim, Y. S. et al., T cell receptor-MHC class I peptide interactions: Affinity, kinetics, and specificity. Science 1994. 265: 946-949.
20. Matsui, K., Boniface, J. J., Steffner, P., Reay, P. A. and Davis, M. M., Kinetics of T-cell receptor binding to peptide/I-Ek complexes: Correlation of the dissociation rate with T-cell responsiveness. Proc. Natl. Acad. Sci. USA 1994. 91: 12862-12866.
21. Cohen, C. J., Denkberg, G., Lev, A., Epel, M. and Reiter, Y., Recombinant antibodies with MHC-restricted, peptide-specific, T-cell receptor-like specificity: New tools to study antigen presentation and TCR-peptide-MHC interactions. J. Mol. Recognit. 2003. 16: 324-332.
22. Cohen, C. J., Sarig, O., Yamano, Y., Tomaru, U., Jacobson, S. and Reiter, Y., Direct phenotypic analysis of human MHC class I antigen presentation: Visualization, quantitation, and in situ detection of human viral epitopes using peptide-specific, MHC-restricted human recombinant antibodies. J. Immunol. 2003. 170: 4349-4361.
23. Cohen, C. J., Hoffmann, N., Farago, M., Hoogenboom, H. R., Eisenbach, L. and Reiter, Y., Direct detection and quantitation of a distinct T-cell epitope derived from tumor-specific epithelial cell-associated mucin using human recombinant antibodies endowed with the antigen-specific, major histocompatibility complex-restricted specificity of T cells. Cancer Res. 2002. 62: 5835-5844.
24. Denkberg, G., Cohen, C. J., Lev, A., Chames, P., Hoogenboom, H. R. and Reiter, Y., Direct visualization of distinct T cell epitopes derived from a melanoma tumor-associated antigen by using human recombinant antibodies with MHC-restricted T cell receptor-like specificity. Proc. Natl. Acad. Sci. USA. 2002. 99: 9421-9426.
25. Held, G., Matsuo, M., Epel, M., Gnjatic, S., Ritter, G., Lee, S. Y., Tai, T. Y. et al., Dissecting cytotoxic T cell responses towards the NY-ESO-1 protein by peptide/MHC-specific antibody fragments. Eur. J. Immunol. 2004. 34: 2919-2929.
26. Lev, A., Denkberg, G., Cohen, C. J., Tzukerman, M., Skorecki, K. L., Chames, P., Hoogenboom, H. R. and Reiter, Y., Isolation and characterization of human recombinant antibodies endowed with the antigen-specific, major histocompatibility complex-restricted specificity of T cells directed toward the widely expressed tumor T-cell epitopes of the telomerase catalytic subunit. Cancer Res. 2002. 62: 3184-3194.
27. Niv, R., Cohen, C. J., Denkberg, G., Segal, D. and Reiter, Y., Antibody engineering for targeted therapy of cancer: Recombinant Fv-immunotoxins. Curr. Pharm. Biotechnol. 2001. 2: 19-46.
28. Reiter, Y., Brinkmann, U.,Webber, K. O., Jung, S. H., Lee, B. and Pastan, I., Engineering interchain disulfide bonds into conserved framework regions of Fv fragments: Improved biochemical characteristics of recombinant immunotoxins containing disulfide-stabilized Fv. Protein Eng. 1994. 7: 697-704.
29. Benhar, I. and Pastan, I., Cloning, expression and characterization of the Fv fragments of the anti-carbohydrate mAbs B1 and B5 as single-chain immunotoxins. Protein Eng. 1994. 7: 1509-1515.
30. Brinkmann, U. and Pastan, I., Immunotoxins against cancer. Biochim. Biophys. Acta 1994. 1198: 27-45.
31. Goldenberg, M. M., Trastuzumab, a recombinant DNA-derived humanized monoclonal antibody, a novel agent for the treatment of metastatic breast cancer. Clin. Ther. 1999. 21: 309-318.
32. Lode, H. N. and Reisfeld, R. A., Targeted cytokines for cancer immunotherapy. Immunol. Res. 2000. 21: 279-288.
33. Kataoka, A., Ishida, M., Murakami, S. and Ohno, S., Sensitization of chemotherapy by anti-HER. Breast Cancer 2004. 11: 105-115.
34. Pastan, I. and Kreitman, R. J., Immunotoxins in cancer therapy. Curr. Opin. Investig. Drugs 2002. 3: 1089-1091.
35. Denkberg, G., Cohen, C. J., Segal, D., Kirkin, A. F. and Reiter, Y., Recombinant human single-chain MHC-peptide complexes made from E. coli by in vitro refolding: Functional single-chain MHC-peptide complexes and tetramers with tumor associated antigens. Eur. J. Immunol. 2000. 30: 3522-3532.
36. Denkberg, G., Cohen, C. J. and Reiter, Y., Critical role for CD8 in binding of MHC tetramers to TCR: CD8 antibodies block specific binding of human tumor-specific MHC-peptide tetramers to TCR. J. Immunol. 2001. 167: 270-276.
37. de Haard, H. J., van Neer, N., Reurs, A., Hufton, S. E., Roovers, R. C., Henderikx, P., de Bruine, A. P. et al., Large non-immunized human Fab fragment phage library that permits rapid isolation and kinetic analysis of high affinity antibodies. J. Biol. Chem. 1999. 274: 18218-18230.
38. Pastan, I., Targeted therapy of cancer with recombinant immunotoxins. Biochim. Biophys. Acta 1997. 1333: C1-C6.
39. Kreitman, R. J. and Pastan, I., Importance of the glutamate residue of KDEL in increasing the cytotoxicity of Pseudomonas exotoxin derivatives and for increased binding to the KDEL receptor. Biochem. J. 1995. 307: 29-37.
40. Lee, P. P., Yee, C., Savage, P. A. Fong, L., Brockstedt, D., Weber, J. S., Johnson, D. et al., Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients. Nat. Med. 1999. 5: 677-685.
41. Ogg, G. S., Jin, X., Bonhoeffer, S., Dunbar, P. R., Nowak, M. A., Monard, S., Segal, J. P. et al., Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 1998. 279: 2103-2106.
42. Restifo, N. P., Esquivel, F., Kawakami, Y., Yewdell, J. W., Mule, J. J., Rosenberg, S. A. and Bennink, J. R., Identification of human cancers deficient in antigen processing. J. Exp. Med. 1993. 177: 265-272.
43. Seliger, B., Maeurer, M. J. and Ferrone, S., Antigen-processing machinery breakdown and tumor growth. Immunol. Today 2000. 21: 455-464.
44. Esche, C., Shurin, M. R. and Lotze, M. T., The use of dendritic cells for cancer vaccination. Curr. Opin. Mol. Ther. 1999. 1: 72-81.
45. Kugler, A., Stuhler, G.,Walden, P., Zoller, G., Zobywalski, A., Brossart, P., Trefzer, U. et al., Regression of human metastatic renal cell carcinoma after vaccination with tumor cell-dendritic cell hybrids. Nat. Med. 2000. 6: 332-336.
46. Aharoni, R., Teitelbaum, D., Arnon, R. and Puri, J., Immunomodulation of experimental allergic encephalomyelitis by antibodies to the antigen-Ia complex. Nature 1991. 351: 147-150.
47. Stryhn, A., Andersen, P. S., Pedersen, L. O., Svejgaard, A., Holm, A., Thorpe, C. J., Fugger, L. et al., Shared fine specificity between T-cell receptors and an antibody recognizing a peptide/major histocompatibility class I complex. Proc. Natl. Acad. Sci. USA 1996. 93: 10338-10342.
48. Krogsgaard, M., Wucherpfennig, K. W., Cannella, B., Hansen, B. E., Svejgaard, A., Pyrdol, J., Ditzel, H. et al., Visualization of myelin basic protein (MBP) T cell epitopes in multiple sclerosis lesions using a monoclonal antibody specific for the human histocompatibility leukocyte antigen (HLA)-DR2-MBP 85-99 complex. J. Exp. Med. 2000. 191: 1395-1412.
49. Andersen, P. S., Stryhn, A., Hansen, B. E., Fugger, L., Engberg, J. and Buus, S., A recombinant antibody with the antigen-specific, major histocompatibility complex-restricted specificity of T cells. Proc. Natl. Acad. Sci. USA 1996. 93: 1820-1824.
50. Porgador, A., Yewdell, J.W., Deng, Y., Bennink, J. R. and Germain, R. N., Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 1997. 6: 715-726.
51. McCafferty, J., Griffiths, A. D., Winter, G. and Chiswell, D. J., Phage antibodies: Filamentous phage displaying antibody variable domains. Nature 1990. 348: 552-554.
52. Winter, G., Griffiths, A. D., Hawkins, R. E. and Hoogenboom, H. R., Making antibodies by phage display technology. Annu. Rev. Immunol. 1994. 12: 433-455.
53. Clackson, T., Hoogenboom, H. R., Griffiths, A. D. and Winter, G., Making antibody fragments using phage display libraries. Nature 1991. 352: 624-628.
54. Barbas, C. F., III, Kang, A. S., Lerner, R. A. and Benkovic, S. J., Assembly of combinatorial antibody libraries on phage surfaces: The gene III site. Proc. Natl. Acad. Sci. USA 1991. 88: 7978-7982.
55. Wolfgang, C. D., Essand, M., Lee, B. and Pastan, I., T-cell receptor gamma chain alternate reading frame protein (TARP) expression in prostate cancer cells leads to an increased growth rate and induction of caveolins and amphiregulin. Cancer Res. 2001. 61: 8122-8126.
56. Williams, A., Peh, C. A. and Elliott, T., The cell biology of MHC class 1 antigen presentation. Tissue Antigens 2002. 59: 3-17.
57. Rudolph, M. G. and Wilson, I. A., The specificity of TCR/pMHC interaction. Curr. Opin. Immunol. 2002. 14: 52-65.
58. Rammensee, H. G., Falk, K. and Rotzschke, O., Peptides naturally presented by MHC class I molecules. Annu. Rev. Immunol. 1993. 11: 213-244.
59. Germain, R. N. and Margulies, D. H., The biochemistry and cell biology of antigen processing and presentation. Annu. Rev. Immunol. 1993. 11: 403-450.
60. Matsumura, M., Fremont, D. H., Peterson, P. A. and Wilson, I. A., Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science 1992. 257: 927-934.
61. Davis, M. M., Boniface, J. J., Reich, Z., Lyons, D., Hampl, J., Arden, B. and Chien, Y., Ligand recognition by alpha beta T cell receptors. Annu. Rev. Immunol. 1998. 16: 523-544.
62. Parker, K. C., Bednarek, M. A., Hull, L. K., Utz, U., Cunningham, B., Zweerink, H. J., Biddison, W. E. and Coligan, J. E., Sequence motifs important for peptide binding to the human MHC class I molecule, HLA-A2. J. Immunol. 1992. 149: 3580-3587.
63. Denkberg, G., Klechevsky, E. and Reiter, Y., Modification of a tumor-derived peptide at an HLA-A2 anchor residue can alter the conformation of the MHC-peptide complex: Probing with TCR-like recombinant antibodies. J. Immunol. 2002. 169: 4399-4407.
64. Clay, T. M., Custer, M. C., McKee, M. D., Parkhurst, M., Robbins, P. F., Kerstann, K., Wunderlich, J. et al., Changes in the fine specificity of gp100(209-217)-reactive T cells in patients following vaccination with a peptide modified at an HLA-A2.1 anchor residue. J. Immunol. 1999. 162: 1749-1755.
65. Rosenberg, S. A., Progress in human tumour immunology and immuno-therapy. Nature 2001. 411: 380-384.
66. Rosenberg, S. A., Yang, J. C., Schwartzentruber, D. J., Hwu, P., Marincola, F. M., Topalian, S. L., Restifo, N. P. et al., I mmunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma. Nat. Med. 1998. 4: 321-327.
67. Altman, J. D., Moss, P. A., Goulder, P. J., Barouch, D. H., McHeyzer-Williams, M. G., Bell, J. I., McMichael, A. J. et al., Phenotypic analysis of antigen-specific T lymphocytes. Science 1996. 274: 94-96.
68. Pascolo, S., Bervas, N., Ure, J. M., Smith, A. G., Lemonnier, F. A. and Perarnau, B., HLA-A2.1-restricted education and cytolytic activity of CD8(+) T lymphocytes from beta2 microglobulin (beta2m) HLA-A2.1 monochain transgenic H-2Db beta2m double knockout mice. J. Exp. Med. 1997. 185: 2043-2051.
69. Barnstable, C. J., Bodmer, W. F., Brown, G., Galfre, G., Milstein, C., Williams, A. F. and Ziegler, A., Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens - new tools for genetic analysis. Cell 1978. 14: 9-20.
70. Brinkmann, U., Pai, L. H., FitzGerald, D. J., Willingham, M. and Pastan, I., B3(Fv)-PE38KDEL, a single-chain immunotoxin that causes complete regression of a human carcinoma in mice. Proc. Natl. Acad. Sci. USA 1991. 88: 8616-8620.