Vaccine injection site matters: Qualitative and quantitative defects in CD8 T cells primed as a function of proximity to the tumor in a murine glioma model

Journal of Immunology

Volumn 190, Issue 2, 2013, Pages 613-620

  Ohlfest, John R ^a   Andersen, Brian M ^a   Litterman, Adam J ^a   Xia, Junzhe ^a   Pennell, Christopher A ^a   Swier, Lauryn E ^a   Salazar, Andres M ^b   Olin, Michael R ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b Oncovir Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYMETHYLCELLULOSE POLYCYTIDYLIC POLYINOSINIC ACID POLYLYSINE; GAMMA INTERFERON; OVALBUMIN; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; GLIOMA; IMMUNE RESPONSE; INJECTION SITE; LYMPHOCYTE COUNT; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIMED LYMPHOCYTE TYPING; PRIORITY JOURNAL; RECEPTOR AFFINITY; T LYMPHOCYTE PRIMING; TUMOR LOCALIZATION;

ANIMALS; BRAIN NEOPLASMS; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; FEMALE; GLIOMA; MICE; RECEPTORS, ANTIGEN, T-CELL;

EID: 84872184215     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201557     Document Type: Article

References (53)

1. Chang, C. N., Y. C. Huang, D. M. Yang, K. Kikuta, K. J. Wei, T. Kubota, and W. K. Yang. 2011. A phase I/II clinical trial investigating the adverse and therapeutic effects of a postoperative autologous dendritic cell tumor vaccine in patients with malignant glioma. J. Clin. Neurosci. 18: 1048-1054.
2. Okada, H., F. S. Lieberman, H. D. Edington, T. F. Witham, M. J. Wargo, Q. Cai, E. H. Elder, T. L. Whiteside, S. C. Schold, Jr., and I. F. Pollack. 2003. Autologous glioma cell vaccine admixed with interleukin-4 gene transfected fibroblasts in the treatment of recurrent glioblastoma: preliminary observations in a patient with a favorable response to therapy. J. Neurooncol. 64: 13-20.
3. Ardon, H., S. W. Van Gool, T. Verschuere, W. Maes, S. Fieuws, R. Sciot, G. Wilms, P. Demaerel, J. Goffin, F. Van Calenbergh, et al. 2012. Integration of autologous dendritic cell-based immunotherapy in the standard of care treatment for patients with newly diagnosed glioblastoma: results of the HGG-2006 phase I/II trial. Cancer Immunol. Immunother. 61: 2033-2044.
4. Yamanaka, R., T. Abe, N. Yajima, N. Tsuchiya, J. Homma, T. Kobayashi, M. Narita, M. Takahashi, and R. Tanaka. 2003. Vaccination of recurrent glioma patients with tumour lysate-pulsed dendritic cells elicits immune responses: results of a clinical phase I/II trial. Br. J. Cancer 89: 1172-1179.
5. Kikuchi, T., Y. Akasaki, M. Irie, S. Homma, T. Abe, and T. Ohno. 2001. Results of a phase I clinical trial of vaccination of glioma patients with fusions of dendritic and glioma cells. Cancer Immunol. Immunother. 50: 337-344.
6. Morton, D. L., D. R. Wen, J. H. Wong, J. S. Economou, L. A. Cagle, F. K. Storm, L. J. Foshag, and A. J. Cochran. 1992. Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch. Surg. 127: 392-399.
7. Cochran, A. J., B. R. Balda, H. Starz, D. Bachter, D. N. Krag, C. W. Cruse, R. Pijpers, and D. L. Morton. 2000. The Augsburg Consensus. Techniques of lymphatic mapping, sentinel lymphadenectomy, and completion lymphadenectomy in cutaneous malignancies. Cancer 89: 236-241.
8. Cochran, A. J., D. L. Morton, S. Stern, A. M. Lana, R. Essner, and D. R. Wen. 2001. Sentinel lymph nodes show profound downregulation of antigen-presenting cells of the paracortex: implications for tumor biology and treatment. Mod. Pathol. 14: 604-608.
9. Lana, A. M., D. R. Wen, and A. J. Cochran. 2001. The morphology, immunophenotype and distribution of paracortical dendritic leucocytes in lymph nodes regional to cutaneous melanoma. Melanoma Res. 11: 401-410.
10. Matsuura, K., Y. Yamaguchi, H. Ueno, A. Osaki, K. Arihiro, and T. Toge. 2006. Maturation of dendritic cells and T-cell responses in sentinel lymph nodes from patients with breast carcinoma. Cancer 106: 1227-1236.
11. Hoon, D. S., R. J. Bowker, and A. J. Cochran. 1987. Suppressor cell activity in melanoma-draining lymph nodes. Cancer Res. 47: 1529-1533.
12. Hoon, D. S., E. L. Korn, and A. J. Cochran. 1987. Variations in functional immunocompetence of individual tumor-draining lymph nodes in humans. Cancer Res. 47: 1740-1744.
13. Wen, D. R., D. S. Hoon, C. Chang, and A. J. Cochran. 1989. Variations in lymphokine generation by individual lymph nodes draining human malignant tumors. Cancer Immunol. Immunother. 30: 277-282.
14. Farzad, Z., A. J. Cochran, W. H. McBride, J. D. Gray, V. Wong, and D. L. Morton. 1990. Lymphocyte subset alterations in nodes regional to human melanoma. Cancer Res. 50: 3585-3588.
15. Ostroukhova, M., Z. Qi, T. B. Oriss, B. Dixon-McCarthy, P. Ray, and A. Ray. 2006. Treg-mediated immunosuppression involves activation of the Notch-HES1 axis by membrane-bound TGF-beta. J. Clin. Invest. 116: 996-1004.
16. Chen, M. L., M. J. Pittet, L. Gorelik, R. A. Flavell, R. Weissleder, H. von Boehmer, and K. Khazaie. 2005. Regulatory T cells suppress tumor-specific CD8 T cell cytotoxicity through TGF-beta signals in vivo. Proc. Natl. Acad. Sci. USA 102: 419-424.
17. Baratelli, F., Y. Lin, L. Zhu, S. C. Yang, N. Heuzé-Vourc'h, G. Zeng, K. Reckamp, M. Dohadwala, S. Sharma, and S. M. Dubinett. 2005. Prostaglandin E2 induces FOXP3 gene expression and T regulatory cell function in human CD4+ T cells. J. Immunol. 175: 1483-1490.
18. Sharma, S., S. C. Yang, L. Zhu, K. Reckamp, B. Gardner, F. Baratelli, M. Huang, R. K. Batra, and S. M. Dubinett. 2005. Tumor cyclooxygenase-2/ prostaglandin E2-dependent promotion of FOXP3 expression and CD4+ CD25+ T regulatory cell activities in lung cancer. Cancer Res. 65: 5211-5220.
19. Tran Thang, N. N., M. Derouazi, G. Philippin, S. Arcidiaco, W. Di Berardino-Besson, F. Masson, S. Hoepner, C. Riccadonna, K. Burkhardt, A. Guha, et al. 2010. Immune infiltration of spontaneous mouse astrocytomas is dominated by immunosuppressive cells from early stages of tumor development. Cancer Res. 70: 4829-4839.
20. Boissonnas, A., A. Scholer-Dahirel, V. Simon-Blancal, L. Pace, F. Valet, A. Kissenpfennig, T. Sparwasser, B. Malissen, L. Fetler, and S. Amigorena. 2010. Foxp3+ T cells induce perforin-dependent dendritic cell death in tumor-draining lymph nodes. Immunity 32: 266-278.
21. Gordon, L. B., P. M. Knopf, and H. F. Cserr. 1992. Ovalbumin is more immunogenic when introduced into brain or cerebrospinal fluid than into extracerebral sites. J. Neuroimmunol. 40: 81-87.
22. Harling-Berg, C. J., T. J. Park, and P. M. Knopf. 1999. Role of the cervical lymphatics in the Th2-type hierarchy of CNS immune regulation. J. Neuroimmunol. 101: 111-127.
23. Gordon, L. B., S. C. Nolan, H. F. Cserr, P. M. Knopf, and C. J. Harling-Berg. 1997. Growth of P511 mastocytoma cells in BALB/c mouse brain elicits CTL response without tumor elimination: a new tumor model for regional central nervous system immunity. J. Immunol. 159: 2399-2408.
24. Gordon, L. B., S. C. Nolan, B. R. Ksander, P. M. Knopf, and C. J. Harling-Berg. 1998. Normal cerebrospinal fluid suppresses the in vitro development of cytotoxic T cells: role of the brain microenvironment in CNS immune regulation. J. Neuroimmunol. 88: 77-84.
25. Lohr, J., T. Ratliff, A. Huppertz, Y. Ge, C. Dictus, R. Ahmadi, S. Grau, N. Hiraoka, V. Eckstein, R. C. Ecker, et al. 2011. Effector T-cell infiltration positively impacts survival of glioblastoma patients and is impaired by tumor-derived TGF-β. Clin. Cancer Res. 17: 4296-4308.
26. Barcia, C., Jr., A. Gómez, J. M. Gallego-Sanchez, A. Perez-Vallés, M. G. Castro, P. R. Lowenstein, C. Barcia, Sr., and M. T. Herrero. 2009. Infiltrating CTLs in human glioblastoma establish immunological synapses with tumorigenic cells. Am. J. Pathol. 175: 786-798.
27. Prins, R. M., H. Soto, V. Konkankit, S. K. Odesa, A. Eskin, W. H. Yong, S. F. Nelson, and L. M. Liau. 2011. Gene expression profile correlates with T-cell infiltration and relative survival in glioblastoma patients vaccinated with dendritic cell immunotherapy. Clin. Cancer Res. 17: 1603-1615.
28. Gustafson, M. P., Y. Lin, K. C. New, P. A. Bulur, B. P. O'Neill, D. A. Gastineau, and A. B. Dietz. 2010. Systemic immune suppression in glioblastoma: the interplay between CD14+HLA-DRlo/neg monocytes, tumor factors, and dexamethasone. Neuro-oncol. 12: 631-644.
29. Sampson, J. H., K. D. Aldape, G. E. Archer, A. Coan, A. Desjardins, A. H. Friedman, H. S. Friedman, M. R. Gilbert, J. E. Herndon, R. E. McLendon, et al. 2011. Greater chemotherapy-induced lymphopenia enhances tumor-specific immune responses that eliminate EGFRvIII-expressing tumor cells in patients with glioblastoma. Neuro-oncol. 13: 324-333.
30. Grossman, S. A., X. Ye, G. Lesser, A. Sloan, H. Carraway, S. Desideri, and S. Piantadosi; NABTT CNS Consortium. 2011. Immunosuppression in patients with high-grade gliomas treated with radiation and temozolomide. Clin. Cancer Res. 17: 5473-5480.
31. Fujita, M., G. Kohanbash, W. Fellows-Mayle, R. L. Hamilton, Y. Komohara, S. A. Decker, J. R. Ohlfest, and H. Okada. 2011. COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells. Cancer Res. 71: 2664-2674.
32. Wei, J., A. Wu, L. Y. Kong, Y. Wang, G. Fuller, I. Fokt, G. Melillo, W. Priebe, and A. B. Heimberger. 2011. Hypoxia potentiates glioma-mediated immunosuppression. PLoS ONE 6: e16195.
33. Wischhusen, J., M. A. Friese, M. Mittelbronn, R. Meyermann, and M. Weller. 2005. HLA-E protects glioma cells from NKG2D-mediated immune responses in vitro: implications for immune escape in vivo. J. Neuropathol. Exp. Neurol. 64: 523-528.
34. Parsa, A. T., J. S. Waldron, A. Panner, C. A. Crane, I. F. Parney, J. J. Barry, K. E. Cachola, J. C. Murray, T. Tihan, M. C. Jensen, et al. 2007. Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat. Med. 13: 84-88.
35. Munn, D. H., and A. L. Mellor. 2006. The tumor-draining lymph node as an immune-privileged site. Immunol. Rev. 213: 146-158.
36. Cochran, A. J., R. R. Huang, J. Lee, E. Itakura, S. P. Leong, and R. Essner. 2006. Tumour-induced immune modulation of sentinel lymph nodes. Nat. Rev. Immunol. 6: 659-670.
37. Moran, A. E., K. L. Holzapfel, Y. Xing, N. R. Cunningham, J. S. Maltzman, J. Punt, and K. A. Hogquist. 2011. T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J. Exp. Med. 208: 1279-1289.
38. Wu, A., S. Oh, K. Ericson, Z. L. Demorest, I. Vengco, S. Gharagozlou, W. Chen, W. C. Low, and J. R. Ohlfest. 2007. Transposon-based interferon gamma gene transfer overcomes limitations of episomal plasmid for immunogene therapy of glioblastoma. Cancer Gene Ther. 14: 550-560.
39. Hommel, M., and P. D. Hodgkin. 2007. TCR affinity promotes CD8+ T cell expansion by regulating survival. J. Immunol. 179: 2250-2260.
40. Olin, M. R., B. M. Andersen, D. M. Zellmer, P. T. Grogan, F. E. Popescu, Z. Xiong, C. L. Forster, C. Seiler, K. S. SantaCruz, W. Chen, et al. 2010. Superior efficacy of tumor cell vaccines grown in physiologic oxygen. Clin. Cancer Res. 16: 4800-4808.
41. Shu, S., A. J. Cochran, R. R. Huang, D. L. Morton, and H. T. Maecker. 2006. Immune responses in the draining lymph nodes against cancer: implications for immunotherapy. Cancer Metastasis Rev. 25: 233-242.
42. Gajewski, T. F., Y. Meng, C. Blank, I. Brown, A. Kacha, J. Kline, and H. Harlin. 2006. Immune resistance orchestrated by the tumor microenvironment. Immunol. Rev. 213: 131-145.
43. Jenkins, M. K., and R. H. Schwartz. 1987. Antigen presentation by chemically modified splenocytes induces antigen-specific T cell unresponsiveness in vitro and in vivo. J. Exp. Med. 165: 302-319.
44. Hodi, F. S., S. J. O'Day, D. F. McDermott, R. W. Weber, J. A. Sosman, J. B. Haanen, R. Gonzalez, C. Robert, D. Schadendorf, J. C. Hassel, et al. 2010. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363: 711-723.
45. Curiel, T. J., S. Wei, H. Dong, X. Alvarez, P. Cheng, P. Mottram, R. Krzysiek, K. L. Knutson, B. Daniel, M. C. Zimmermann, et al. 2003. Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity. Nat. Med. 9: 562-567.
46. Gerner, M. Y., K. A. Casey, and M. F. Mescher. 2008. Defective MHC class II presentation by dendritic cells limits CD4 T cell help for antitumor CD8 T cell responses. J. Immunol. 181: 155-164.
47. Viguier, M., F. Lemaître, O. Verola, M. S. Cho, G. Gorochov, L. Dubertret, H. Bachelez, P. Kourilsky, and L. Ferradini. 2004. Foxp3 expressing CD4+CD25 (high) regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibit the function of infiltrating T cells. J. Immunol. 173: 1444-1453.
48. Hiura, T., H. Kagamu, S. Miura, A. Ishida, H. Tanaka, J. Tanaka, F. Gejyo, and H. Yoshizawa. 2005. Both regulatory T cells and antitumor effector T cells are primed in the same draining lymph nodes during tumor progression. J. Immunol. 175: 5058-5066.
49. Manuel, E. R., W. A. Charini, P. Sen, F. W. Peyerl, M. J. Kuroda, J. E. Schmitz, P. Autissier, D. A. Sheeter, B. E. Torbett, and N. L. Letvin. 2006. Contribution of T-cell receptor repertoire breadth to the dominance of epitope-specific CD8+ T-lymphocyte responses. J. Virol. 80: 12032-12040.
50. Busch, D. H., and E. G. Pamer. 1999. T cell affinity maturation by selective expansion during infection. J. Exp. Med. 189: 701-710.
51. Yachi, P. P., J. Ampudia, T. Zal, and N. R. Gascoigne. 2006. Altered peptide ligands induce delayed CD8-T cell receptor interaction - a role for CD8 in distinguishing antigen quality. Immunity 25: 203-211.
52. Daniels, M. A., and S. C. Jameson. 2000. Critical role for CD8 in T cell receptor binding and activation by peptide/major histocompatibility complex multimers. J. Exp. Med. 191: 335-346.
53. Monu, N., and A. B. Frey. 2007. Suppression of proximal T cell receptor signaling and lytic function in CD8+ tumor-infiltrating T cells. Cancer Res. 67: 11447-11454.