Exosomal pMHC-I complex targets T cell-based vaccine to directly stimulate CTL responses leading to antitumor immunity in transgenic FVBneuN and HLA-A2/HER2 mice and eradicating trastuzumab-resistant tumor in athymic nude mice

Breast Cancer Research and Treatment

Volumn 140, Issue 2, 2013, Pages 273-284

  Wang, Lu ^a   Xie, Yufeng ^a   Ahmed, Khawaja Ashfaque ^a   Ahmed, Shahid ^b   Sami, Amer ^b   Chibbar, Rajni ^b   Xu, Qingyong ^b   Kane, Susan E ^d   Hao, Siguo ^e   Mulligan, Sean J ^c   Xiang, Jim ^a,f  

^a SASKATCHEWAN CANCER AGENCY   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

^d CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^e SHANGHAI JIAO TONG UNIVERSITY   (China)

^f Saskatoon Cancer Center   (Canada)

Author keywords

HER2; T cell based vaccine; Transgenic HLA A2 HER2 mice; Trastuzumab resistance

Indexed keywords

ADENOVIRUS VECTOR; CANCER VACCINE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TRASTUZUMAB; ERBB2 PROTEIN, HUMAN; HLA A2 ANTIGEN; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER RESISTANCE; CANCER SIZE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; EXOSOME; FEMALE; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; TRANSGENIC MOUSE; TUMOR IMMUNITY; ANIMAL; BREAST TUMOR; DRUG RESISTANCE; GENETICS; HUMAN; IMMUNOLOGY; MAJOR HISTOCOMPATIBILITY COMPLEX; METABOLISM; NUDE MOUSE;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; BREAST NEOPLASMS; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; DRUG RESISTANCE, NEOPLASM; EXOSOMES; FEMALE; HLA-A2 ANTIGEN; HUMANS; MAJOR HISTOCOMPATIBILITY COMPLEX; MICE; MICE, NUDE; MICE, TRANSGENIC; RECEPTOR, ERBB-2; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84881452141     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-013-2626-7     Document Type: Article

References (43)

1. Schechter AL, Hung MC, Vaidyanathan L, Weinberg RA, Yang-Feng TL, Francke U, Ullrich A, Coussens L (1985) The neu gene: an erbB-homologous gene distinct from and unlinked to the gene encoding the EGF receptor. Science 229(4717):976-978
2. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE, Levin WJ, Stuart SG, Udove J, Ullrich A, et al. (1989) Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 244(4905):707-712
3. Gonzalez-Angulo AM, Hortobagyi GN, Esteva FJ (2006) Adjuvant therapy with trastuzumab for HER-2/neu-positive breast cancer. Oncologist 11(8):857-867
4. Vogel CL, Cobleigh MA, Tripathy D, Gutheil JC, Harris LN, Fehrenbacher L, Slamon DJ, Murphy M, Novotny WF, Burchmore M, Shak S, Stewart SJ, Press M (2002) Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer. J Clin Oncol 20(3):719-726
5. Berns K, Horlings HM, Hennessy BT, Madiredjo M, Hijmans EM, Beelen K, Linn SC, Gonzalez-Angulo AM, Stemke-Hale K, Hauptmann M, Beijersbergen RL, Mills GB, van de Vijver MJ, Bernards R (2007) A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell 12(4):395-402
6. Nahta R, Esteva FJ (2006) Herceptin: mechanisms of action and resistance. Cancer Lett 232(2):123-138
7. Nahta R, Esteva FJ (2006) HER2 therapy: molecular mechanisms of trastuzumab resistance. Breast Cancer Res 8(6):215
8. Hao S, Yuan J, Xiang J (2007) Nonspecific CD4(+) T cells with uptake of antigen-specific dendritic cell-released exosomes stimulate antigen-specific CD8(+) CTL responses and long-term T cell memory. J Leukoc Biol 82(4):829-838
9. Hao S, Liu Y, Yuan J, Zhang X, He T, Wu X, Wei Y, Sun D, Xiang J (2007) Novel exosome-targeted CD4+ T cell vaccine counteracting CD4+25+ regulatory T cell-mediated immune suppression and stimulating efficient central memory CD8+ CTL responses. J Immunol 179(5):2731-2740
10. Xie Y, Wang L, Freywald A, Qureshi M, Chen Y, Xiang J (2013) A novel T cell-based vaccine capable of stimulating long-term functional CTL memory against B16 melanoma via CD40L signaling. Cell Mol Immunol 10(1):72-77
11. Ahmed KA, Wang L, Munegowda MA, Mulligan SJ, Gordon JR, Griebel P, Xiang J (2012) Direct in vivo evidence of CD4+ T cell requirement for CTL response and memory via pMHC-I targeting and CD40L signaling. J Leukoc Biol 92(2):289-300
12. Sas S, Chan T, Sami A, El-Gayed A, Xiang J (2008) Vaccination of fiber-modified adenovirus-transfected dendritic cells to express HER-2/neu stimulates efficient HER-2/neu-specific humoral and CTL responses and reduces breast carcinogenesis in transgenic mice. Cancer Gene Ther 15(10):655-666
13. Chan T, Sami A, El-Gayed A, Guo X, Xiang J (2006) HER-2/neu-gene engineered dendritic cell vaccine stimulates stronger HER-2/neu-specific immune responses compared to DNA vaccination. Gene Ther 13(19):1391-1402
14. Chen Z, Huang H, Chang T, Carlsen S, Saxena A, Marr R, Xing Z, Xiang J (2002) Enhanced HER-2/neu-specific antitumor immunity by cotransduction of mouse dendritic cells with two genes encoding HER-2/neu and alpha tumor necrosis factor. Cancer Gene Ther 9(9):778-786
15. Eddy SF, Kane SE, Sonenshein GE (2007) Trastuzumab-resistant HER2-driven breast cancer cells are sensitive to epigallocatechin-3 gallate. Cancer Res 67(19):9018-9023
16. Piechocki MP, Ho YS, Pilon S, Wei WZ (2003) Human ErbB-2 (Her-2) transgenic mice: a model system for testing Her-2 based vaccines. J Immunol 171(11):5787-5794
17. Hao S, Bai O, Li F, Yuan J, Laferte S, Xiang J (2007) Mature dendritic cells pulsed with exosomes stimulate efficient cytotoxic T-lymphocyte responses and antitumour immunity. Immunology 120(1):90-102
18. Xiang J, Huang H, Liu Y (2005) A new dynamic model of CD8+ T effector cell responses via CD4+ T helper-antigen-presenting cells. J Immunol 174(12):7497-7505
19. Wang JC, Livingstone AM (2003) Cutting edge: CD4+ T cell help can be essential for primary CD8+ T cell responses in vivo. J Immunol 171(12):6339-6343
20. Nanjundappa RH, Wang R, Xie Y, Umeshappa CS, Chibbar R, Wei Y, Liu Q, Xiang J (2011) GP120-specific exosome-targeted T cell-based vaccine capable of stimulating DC- and CD4(+) T-independent CTL responses. Vaccine 29(19):3538-3547
21. Chen Y, Xie Y, Chan T, Sami A, Ahmed S, Liu Q, Xiang J (2011) Adjuvant effect of HER-2/neu-specific adenoviral vector stimulating CD8(+) T and natural killer cell responses on anti-HER-2/neu antibody therapy for well-established breast tumors in HER-2/neu transgenic mice. Cancer Gene Ther 18(7):489-499
22. Press MF, Pike MC, Chazin VR, Hung G, Udove JA, Markowicz M, Danyluk J, Godolphin W, Sliwkowski M, Akita R, et al. (1993) Her-2/neu expression in node-negative breast cancer: direct tissue quantitation by computerized image analysis and association of overexpression with increased risk of recurrent disease. Cancer Res 53(20):4960-4970
23. Ross JS, Fletcher JA, Linette GP, Stec J, Clark E, Ayers M, Symmans WF, Pusztai L, Bloom KJ (2003) The Her-2/neu gene and protein in breast cancer 2003: biomarker and target of therapy. Oncologist 8(4):307-325
24. Koeppen HK, Wright BD, Burt AD, Quirke P, McNicol AM, Dybdal NO, Sliwkowski MX, Hillan KJ (2001) Overexpression of HER2/neu in solid tumours: an immunohistochemical survey. Histopathology 38(2):96-104
25. Press MF, Cordon-Cardo C, Slamon DJ (1990) Expression of the HER-2/neu proto-oncogene in normal human adult and fetal tissues. Oncogene 5(7):953-962
26. Ward RL, Hawkins NJ, Coomber D, Disis ML (1999) Antibody immunity to the HER-2/neu oncogenic protein in patients with colorectal cancer. Hum Immunol 60(6):510-515
27. Kiessling R, Wei WZ, Herrmann F, Lindencrona JA, Choudhury A, Kono K, Seliger B (2002) Cellular immunity to the Her-2/neu protooncogene. Adv Cancer Res 85:101-144
28. Baxevanis CN, Sotiropoulou PA, Sotiriadou NN, Papamichail M (2004) Immunobiology of HER-2/neu oncoprotein and its potential application in cancer immunotherapy. Cancer Immunol Immunother 53(3):166-175
29. Baxevanis CN, Voutsas IF, Gritzapis AD, Perez SA, Papamichail M (2010) HER-2/neu as a target for cancer vaccines. Immunotherapy 2(2):213-226
30. Baxevanis CN, Sotiriadou NN, Gritzapis AD, Sotiropoulou PA, Perez SA, Cacoullos NT, Papamichail M (2006) Immunogenic HER-2/neu peptides as tumor vaccines. Cancer Immunol Immunother 55(1):85-95
31. Eck SC, Turka LA (2001) Adoptive transfer enables tumor rejection targeted against a self-antigen without the induction of autoimmunity. Cancer Res 61(7):3077-3083
32. Garcia-Hernandez Mde L, Gray A, Hubby B, Klinger OJ, Kast WM (2008) Prostate stem cell antigen vaccination induces a long-term protective immune response against prostate cancer in the absence of autoimmunity. Cancer Res 68(3):861-869
33. Lane C, Leitch J, Tan X, Hadjati J, Bramson JL, Wan Y (2004) Vaccination-induced autoimmune vitiligo is a consequence of secondary trauma to the skin. Cancer Res 64(4):1509-1514
34. Palmer DC, Chan CC, Gattinoni L, Wrzesinski C, Paulos CM, Hinrichs CS, Powell DJ Jr, Klebanoff CA, Finkelstein SE, Fariss RN, Yu Z, Nussenblatt RB, Rosenberg SA, Restifo NP (2008) Effective tumor treatment targeting a melanoma/melanocyte-associated antigen triggers severe ocular autoimmunity. Proc Natl Acad Sci USA 105(23):8061-8066
35. Bos R, van Duikeren S, Morreau H, Franken K, Schumacher TN, Haanen JB, van der Burg SH, Melief CJ, Offringa R (2008) Balancing between antitumor efficacy and autoimmune pathology in T-cell-mediated targeting of carcinoembryonic antigen. Cancer Res 68(20):8446-8455
36. Baxevanis CN, Perez SA, Papamichail M (2009) Cancer immunotherapy. Crit Rev Clin Lab Sci 46(4):167-189
37. Sumoza-Toledo A, Eaton AD, Sarukhan A (2006) Regulatory T cells inhibit protein kinase C theta recruitment to the immune synapse of naive T cells with the same antigen specificity. J Immunol 176(10):5779-5787
38. Whittington PJ, Piechocki MP, Heng HH, Jacob JB, Jones RF, Back JB, Wei WZ (2008) DNA vaccination controls Her-2+ tumors that are refractory to targeted therapies. Cancer Res 68(18):7502-7511
39. Radkevich-Brown O, Jacob J, Kershaw M, Wei WZ (2009) Genetic regulation of the response to Her-2 DNA vaccination in human Her-2 transgenic mice. Cancer Res 69(1):212-218
40. Dai S, Wan T, Wang B, Zhou X, Xiu F, Chen T, Wu Y, Cao X (2005) More efficient induction of HLA-A*0201-restricted and carcinoembryonic antigen (CEA)-specific CTL response by immunization with exosomes prepared from heat-stressed CEA-positive tumor cells. Clin Cancer Res 11(20):7554-7563
41. Saha A, Chatterjee SK, Foon KA, Celis E, Bhattacharya-Chatterjee M (2007) Therapy of established tumors in a novel murine model transgenic for human carcinoembryonic antigen and HLA-A2 with a combination of anti-idiotype vaccine and CTL peptides of carcinoembryonic antigen. Cancer Res 67(6):2881-2892
42. Saha A, Bhattacharya-Chatterjee M, Foon KA, Celis E, Chatterjee SK (2009) Stimulatory effects of CpG oligodeoxynucleotide on dendritic cell-based immunotherapy of colon cancer in CEA/HLA-A2 transgenic mice. Int J Cancer 124(4):877-888
43. Hao S, Ye Z, Li F, Meng Q, Qureshi M, Yang J, Xiang J (2006) Epigenetic transfer of metastatic activity by uptake of highly metastatic B16 melanoma cell-released exosomes. Exp Oncol 28(2):126-131