A vaccine that co-targets tumor cells and cancer associated fibroblasts results in enhanced antitumor activity by inducing antigen spreading

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Gottschalk, Stephen ^a,b   Yu, Feng ^a   Ji, Minjun ^a   Kakarla, Sunitha ^a,b   Song, Xiao Tong ^a,b  

^a CENTER FOR CELL AND GENE THERAPY   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER VACCINE; DENDRITIC CELL VACCINE; RECOMBINANT GAMMA INTERFERON; SEPRASE; SHORT HAIRPIN RNA; TUMOR ANTIGEN; VIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG POTENCY; DRUG TARGETING; FIBROBLAST; IMMUNOSUPPRESSIVE TREATMENT; LENTIVIRINAE; MELANOMA B16; MOUSE; NEOPLASM; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; T LYMPHOCYTE; TUMOR CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT;

ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FIBROBLASTS; GELATINASES; GENE EXPRESSION; GENETIC VECTORS; HUMANS; LENTIVIRUS; MELANOMA, EXPERIMENTAL; MEMBRANE PROTEINS; NEOPLASMS; PEPTIDE FRAGMENTS; RNA, SMALL INTERFERING; SERINE ENDOPEPTIDASES; T-CELL ANTIGEN RECEPTOR SPECIFICITY;

EID: 84892621138     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082658     Document Type: Article

References (32)

1. Nencioni A, Grunebach F, Schmidt SM, Muller MR, Boy D, et al. (2008) The use of dendritic cells in cancer immunotherapy. Crit Rev Oncol Hematol 65: 191-199.
2. Cirri P, Chiarugi P (2011) Cancer associated fibroblasts: the dark side of the coin. Am J Cancer Res 1: 482-497.
3. Marx J (2008) Cancer biology. All in the stroma: cancer's Cosa Nostra. Science 320: 38-41. 320/5872/38 [pii];10.1126/science.320.5872.38 [doi].
4. Dolznig H, Schweifer N, Puri C, Kraut N, Rettig WJ, et al. (2005) Characterization of cancer stroma markers: in silico analysis of an mRNA expression database for fibroblast activation protein and endosialin. Cancer Immun 5: 10.
5. Navab R, Strumpf D, Bandarchi B, Zhu CQ, Pintilie M, et al. (2011) Prognostic gene-expression signature of carcinoma-associated fibroblasts in non-small cell lung cancer. Proc Natl Acad Sci U S A 108: 7160-7165. 1014506108 [pii];10.1073/pnas.1014506108 [doi].
6. Giannoni E, Bianchini F, Masieri L, Serni S, Torre E, et al. (2010) Reciprocal activation of prostate cancer cells and cancer-associated fibroblasts stimulates epithelial-mesenchymal transition and cancer stemness. Cancer Res 70: 6945-6956. 0008-5472.CAN-10-0785 [pii];10.1158/0008-5472.CAN-10-0785 [doi].
7. Tchou J, Conejo-Garcia J (2012) Targeting the tumor stroma as a novel treatment strategy for breast cancer: shifting from the neoplastic cell-centric to a stroma-centric paradigm. Adv Pharmacol 65: 45-61. B978-0-12-397927-8.00003- 8 [pii];10.1016/B978-0-12-397927-8.00003-8 [doi].
8. Ostman A, Augsten M (2009) Cancer-associated fibroblasts and tumor growth - bystanders turning into key players. Curr Opin Genet Dev 19: 67-73.
9. Polyak K, Haviv I, Campbell IG (2009) Co-evolution of tumor cells and their microenvironment. Trends Genet 25: 30-38. S0168-9525(08)00309-0 [pii];10.1016/j.tig.2008.10.012 [doi].
10. Chometon G, Jendrossek V (2009) Targeting the tumour stroma to increase efficacy of chemo- and radiotherapy. Clin Transl Oncol 11: 75-81. 1198 [pii].
11. Rettig WJ, Su SL, Fortunato SR, Scanlan MJ, Raj BK, et al. (1994) Fibroblast activation protein: purification, epitope mapping and induction by growth factors. Int J Cancer 58: 385-392.
12. Kraman M, Bambrough PJ, Arnold JN, Roberts EW, Magiera L, et al. (2010) Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-alpha. Science 330: 827-830.
13. Loeffler M, Kruger JA, Niethammer AG, Reisfeld RA (2006) Targeting tumor-associated fibroblasts improves cancer chemotherapy by increasing intratumoral drug uptake. J Clin Invest 116: 1955-1962.
14. Liao D, Luo Y, Markowitz D, Xiang R, Reisfeld RA (2009) Cancer associated fibroblasts promote tumor growth and metastasis by modulating the tumor immune microenvironment in a 4T1 murine breast cancer model. PLoS One 4: e7965. 10.1371/journal.pone.0007965 [doi].
15. Song XT, Evel-Kabler K, Shen L, Rollins L, Huang XF, et al. (2008) A20 is an antigen presentation attenuator, and its inhibition overcomes regulatory T cell-mediated suppression. Nat Med 14: 258-265.
16. Shen L, Evel-Kabler K, Strube R, Chen SY (2004) Silencing of SOCS1 enhances antigen presentation by dendritic cells and antigen-specific anti-tumor immunity. Nat Biotechnol 22: 1546-1553.
17. Song XT, Evel-Kabler K, Rollins L, Aldrich M, Gao F, et al. (2006) An alternative and effective HIV vaccination approach based on inhibition of antigen presentation attenuators in dendritic cells. PLoS Med 3: e11.
18. Lee J, Fassnacht M, Nair S, Boczkowski D, Gilboa E (2005) Tumor immunotherapy targeting fibroblast activation protein, a product expressed in tumor-associated fibroblasts. Cancer Res 65: 11156-11163.
19. Zhang B, Bowerman NA, Salama JK, Schmidt H, Spiotto MT, et al. (2007) Induced sensitization of tumor stroma leads to eradication of established cancer by T cells. J Exp Med 204: 49-55.
20. Kakarla S, Song XT, Gottschalk S (2012) Cancer-associated fibroblasts as targets for immunotherapy. Immunotherapy 4: 1129-1138. 10.2217/imt.12.112 [doi].
21. Santos AM, Jung J, Aziz N, Kissil JL, Pure E (2009) Targeting fibroblast activation protein inhibits tumor stromagenesis and growth in mice. J Clin Invest 119: 3613-3625. 38988 [pii];10.1172/JCI38988 [doi].
22. Kelly T (2005) Fibroblast activation protein-alpha and dipeptidyl peptidase IV (CD26): cell-surface proteases that activate cell signaling and are potential targets for cancer therapy. Drug Resist Updat 8: 51-58. S1368-7646(05)00025-7 [pii];10.1016/j.drup.2005.03.002 [doi].
23. Cunningham CC (2007) Talabostat. Expert Opin Investig Drugs 16: 1459-1465. 10.1517/13543784.16.9.1459 [doi].
24. Scott AM, Wiseman G, Welt S, Adjei A, Lee FT, et al. (2003) A Phase I dose-escalation study of sibrotuzumab in patients with advanced or metastatic fibroblast activation protein-positive cancer. Clin Cancer Res 9: 1639-1647.
25. Wen Y, Wang CT, Ma TT, Li ZY, Zhou LN, et al. (2010) Immunotherapy targeting fibroblast activation protein inhibits tumor growth and increases survival in a murine colon cancer model. Cancer Sci 101: 2325-2332. CAS1695 [pii];10.1111/j.1349-7006.2010.01695.x [doi].
26. Disis ML, Gooley TA, Rinn K, Davis D, Piepkorn M, et al. (2002) Generation of T-cell immunity to the HER-2/neu protein after active immunization with HER-2/neu peptide-based vaccines. J Clin Oncol 20: 2624-2632.
27. Butterfield LH, Ribas A, Dissette VB, Amarnani SN, Vu HT, et al. (2003) Determinant spreading associated with clinical response in dendritic cell-based immunotherapy for malignant melanoma. Clin Cancer Res 9: 998-1008.
28. Wierecky J, Muller MR, Wirths S, Halder-Oehler E, Dorfel D, et al. (2006) Immunologic and clinical responses after vaccinations with peptide-pulsed dendritic cells in metastatic renal cancer patients. Cancer Res 66: 5910-5918. 66/11/5910 [pii];10.1158/0008-5472.CAN-05-3905 [doi].
29. Hunder NN, Wallen H, Cao J, Hendricks DW, Reilly JZ, et al. (2008) Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. N Engl J Med 358: 2698-2703.
30. Sampson JH, Heimberger AB, Archer GE, Aldape KD, Friedman AH, et al. (2010) Immunologic escape after prolonged progression-free survival with epidermal growth factor receptor variant III peptide vaccination in patients with newly diagnosed glioblastoma. J Clin Oncol 28: 4722-4729.
31. Gottschalk S, Ng CYC, Smith CA, Perez M, Sample C, et al. (2001) An Epstein-Barr virus deletion mutant that causes fatal lymphoproliferative disease unresponsive to virus-specific T cell therapy. Blood 97: 835-843.
32. Spiotto MT, Rowley DA, Schreiber H (2004) Bystander elimination of antigen loss variants in established tumors. Nat Med 10: 294-298.