Adoptive transfer of mammaglobin-A epitope specific CD8 T cells combined with a single low dose of total body irradiation eradicates breast tumors

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Lerret, Nadine M ^a   Rogozinska, Magdalena ^a   Jaramillo, Andrés ^a,b   Marzo, Amanda L ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b Histocompatibility Laboratory   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; EPITOPE; GAMMA INTERFERON; GRANZYME B; INTERLEUKIN 7 RECEPTOR; L SELECTIN; MAMMAGLOBIN A; SCAVENGER RECEPTOR; SCAVENGER RECEPTOR 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST TUMOR; CANCER CONTROL; CANCER INHIBITION; CANCER PREVENTION; CANCER RECURRENCE; CANCER RELAPSE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; DNA IMMUNIZATION; DOWN REGULATION; HUMAN; HUMAN CELL; IN VIVO STUDY; LIPID TRANSPORT; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RADIATION DOSE; SPLEEN CELL; T LYMPHOCYTE SUBPOPULATION; TUMOR REGRESSION; TUMOR REJECTION; WHOLE BODY RADIATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD27; BREAST NEOPLASMS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; EPITOPES, T-LYMPHOCYTE; FEMALE; HUMANS; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; INTERLEUKIN-7 RECEPTOR ALPHA SUBUNIT; L-SELECTIN; LIPID METABOLISM; MAMMAGLOBIN A; MICE; MICE, SCID; MICE, TRANSGENIC; SCAVENGER RECEPTORS, CLASS A; TUMOR NECROSIS FACTOR-ALPHA; VACCINES, DNA; WHOLE-BODY IRRADIATION;

MUS;

EID: 84864102039     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041240     Document Type: Article

References (38)

1. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A, (1999) Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
2. Watson MA, Dintzis S, Darrow CM, Voss LE, DiPersio J, et al. (1999) Mammaglobin expression in primary, metastatic, and occult breast cancer. Cancer Res 59: 3028-3031.
3. Jaramillo A, Narayanan K, Campbell LG, Benshoff ND, Lybarger L, et al. (2004) Recognition of HLA-A2-restricted mammaglobin-A-derived epitopes by CD8+ cytotoxic T lymphocytes from breast cancer patients. Breast Cancer Res Treat 88: 29-41.
4. Narayanan K, Jaramillo A, Benshoff ND, Campbell LG, Fleming TP, et al. (2004) Response of established human breast tumors to vaccination with mammaglobin-A cDNA. J Natl Cancer Inst 96: 1388-1396.
5. Lacey SF, La Rosa C, Kaltcheva T, Srivastava T, Seidel A, et al. (2011) Characterization of immunologic properties of a second HLA-A2 epitope from a granule protease in CML patients and HLA-A2 transgenic mice. Blood 118: 2159-2169.
6. Gallez-Hawkins G VM, Li X, Sanborn MC, Lomeli NA, Zaia JA, (2003) Use of Transgenic HLA A* 0201/Kb and HHD II Mice to Evaluate Frequency of Cytomegalovirus IE1-Derived Peptide Usage in Eliciting Human CD8 Cytokine Response. Journal of Virology 77: 4457-4462.
7. Shirai M, Arichi T, Nishioka M, Nomura T, Ikeda K, et al. (1995) CTL responses of HLA-A2.1-transgenic mice specific for hepatitis C viral peptides predict epitopes for CTL of humans carrying HLA-A2.1. J Immunol 154: 2733-2742.
8. Vitiello A, Marchesini D, Furze J, Sherman LA, Chesnut RW, (1991) Analysis of the HLA-restricted influenza-specific cytotoxic T lymphocyte response in transgenic mice carrying a chimeric human-mouse class I major histocompatibility complex. J Exp Med 173: 1007-1015.
9. Dudley ME, Rosenberg SA, (2003) Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat Rev Cancer 3: 666-675.
10. Sussman JJ, Shu S, Sondak VK, Chang AE, (1994) Activation of T lymphocytes for the adoptive immunotherapy of cancer. Ann Surg Oncol 1: 296-306.
11. Paulos CM, Wrzesinski C, Kaiser A, Hinrichs CS, Chieppa M, et al. (2007) Microbial translocation augments the function of adoptively transferred self/tumor-specific CD8+ T cells via TLR4 signaling. J Clin Invest 117: 2197-2204.
12. Gattinoni L, Finkelstein SE, Klebanoff CA, Antony PA, Palmer DC, et al. (2005) Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med 202: 907-912.
13. Paulos CM, Kaiser A, Wrzesinski C, Hinrichs CS, Cassard L, et al. (2007) Toll-like receptors in tumor immunotherapy. Clin Cancer Res 13: 5280-5289.
14. Masopust D, Vezys V, Marzo AL, Lefrancois L, (2001) Preferential localization of effector memory cells in nonlymphoid tissue. Science 291: 2413-2417.
15. Weninger W, Crowley MA, Manjunath N, von Andrian UH, (2001) Migratory properties of naive, effector, and memory CD8(+) T cells. J Exp Med 194: 953-966.
16. Beverley PC, (2008) Primer: making sense of T-cell memory. Nat Clin Pract Rheumatol 4: 43-49.
17. Hendriks J, Xiao Y, Borst J, (2003) CD27 promotes survival of activated T cells and complements CD28 in generation and establishment of the effector T cell pool. J Exp Med 198: 1369-1380.
18. Croft M, (2003) Co-stimulatory members of the TNFR family: keys to effective T-cell immunity? Nat Rev Immunol 3: 609-620.
19. Marzo AL, Yagita H, Lefrancois L, (2007) Cutting edge: migration to nonlymphoid tissues results in functional conversion of central to effector memory CD8 T cells. J Immunol 179: 36-40.
20. Intlekofer AM, Takemoto N, Wherry EJ, Longworth SA, Northrup JT, et al. (2005) Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat Immunol 6: 1236-1244.
21. Hand TW, Morre M, Kaech SM, (2007) Expression of IL-7 receptor alpha is necessary but not sufficient for the formation of memory CD8 T cells during viral infection. Proc Natl Acad Sci U S A 104: 11730-11735.
22. Kaech SM, Tan JT, Wherry EJ, Konieczny BT, Surh CD, et al. (2003) Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol 4: 1191-1198.
23. Schluns KS, Kieper WC, Jameson SC, Lefrancois L, (2000) Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat Immunol 1: 426-432.
24. Bachmann MF, Wolint P, Schwarz K, Jager P, Oxenius A, (2005) Functional properties and lineage relationship of CD8+ T cell subsets identified by expression of IL-7 receptor alpha and CD62L. J Immunol 175: 4686-4696.
25. Thomas WD, Hersey P, (1998) TNF-related apoptosis-inducing ligand (TRAIL) induces apoptosis in Fas ligand-resistant melanoma cells and mediates CD4 T cell killing of target cells. J Immunol 161: 2195-2200.
26. Marzo AL, Kinnear BF, Lake RA, Frelinger JJ, Collins EJ, et al. (2000) Tumor-specific CD4+ T cells have a major "post-licensing" role in CTL mediated anti-tumor immunity. J Immunol 165: 6047-6055.
27. Fallarino F, Grohmann U, Bianchi R, Vacca C, Fioretti MC, et al. (2000) Th1 and Th2 cell clones to a poorly immunogenic tumor antigen initiate CD8+ T cell-dependent tumor eradication in vivo. J Immunol 165: 5495-5501.
28. Wong SB, Bos R, Sherman LA, (2008) Tumor-specific CD4+ T cells render the tumor environment permissive for infiltration by low-avidity CD8+ T cells. J Immunol 180: 3122-3131.
29. Herber DL, Cao W, Nefedova Y, Novitskiy SV, Nagaraj S, et al. (2010) Lipid accumulation and dendritic cell dysfunction in cancer. Nat Med 16: 880-886.
30. Yee C, Thompson JA, Byrd D, Riddell SR, Roche P, et al. (2002) Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: in vivo persistence, migration, and antitumor effect of transferred T cells. Proc Natl Acad Sci U S A 99: 16168-16173.
31. Powell DJ Jr, Dudley ME, Robbins PF, Rosenberg SA, (2005) Transition of late-stage effector T cells to CD27+ CD28+ tumor-reactive effector memory T cells in humans after adoptive cell transfer therapy. Blood 105: 241-250.
32. Sussman JJ, Parihar R, Winstead K, Finkelman FD, (2004) Prolonged culture of vaccine-primed lymphocytes results in decreased antitumor killing and change in cytokine secretion. Cancer Res 64: 9124-9130.
33. Gattinoni L, Klebanoff CA, Palmer DC, Wrzesinski C, Kerstann K, et al. (2005) Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. J Clin Invest 115: 1616-1626.
34. Klebanoff CA, Gattinoni L, Torabi-Parizi P, Kerstann K, Cardones AR, et al. (2005) Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci U S A 102: 9571-9576.
35. Zhang P, Cote AL, de Vries VC, Usherwood EJ, Turk MJ, (2007) Induction of postsurgical tumor immunity and T-cell memory by a poorly immunogenic tumor. Cancer Res 67: 6468-6476.
36. Perret R, Ronchese F, (2008) Effector CD8+ T cells activated in vitro confer immediate and long-term tumor protection in vivo. Eur J Immunol 38: 2886-2895.
37. Sallusto F, Geginat J, Lanzavecchia A, (2004) Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 22: 745-763.
38. Knutson KL, Disis ML, (2005) Tumor antigen-specific T helper cells in cancer immunity and immunotherapy. Cancer Immunol Immunother 54: 721-728.