Mesothelin Virus-Like Particle Immunization Controls Pancreatic Cancer Growth through CD8+ T Cell Induction and Reduction in the Frequency of CD4+foxp3+ICOS- Regulatory T Cells

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Zhang, Sheng ^a   Yong, Lin Kin ^a   Li, Dali ^a   Cubas, Rafael ^a   Chen, Changyi ^a   Yao, Qizhi ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; MESOTHELIN; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DOWN REGULATION; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; IMMUNOSUPPRESSIVE TREATMENT; MICROENVIRONMENT; MOUSE; NONHUMAN; PANCREAS CANCER; REGULATORY T LYMPHOCYTE; SPLEEN; TUMOR VOLUME; VIRUS LIKE AGENT;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FORKHEAD TRANSCRIPTION FACTORS; GPI-LINKED PROTEINS; HUMANS; INDUCIBLE T-CELL CO-STIMULATOR PROTEIN; INTERLEUKIN-6; LYMPHOCYTES, TUMOR-INFILTRATING; MICE; PANCREATIC NEOPLASMS; T-LYMPHOCYTES, REGULATORY; VACCINATION; VACCINES, VIRUS-LIKE PARTICLE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MURINAE;

EID: 84879953494     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068303     Document Type: Article

References (46)

1. Laheru D, Jaffee EM, (2005) Immunotherapy for pancreatic cancer- science driving clinical progress. Nat Rev Cancer. 5: 459-467.
2. Gilboa E, (2004) The promise of cancer vaccines. Nat Rev Cancer. 4: 401-411.
3. Lollini PL, Cavallo F, Nanni P, Forni G, (2006) Vaccines for tumour prevention. Nat Rev Cancer. 6: 204-216.
4. Finn OJ, (2003) Cancer vaccines: between the idea and the reality. Nat Rev Immunol. 3: 630-641.
5. Ljunggren HG, Malmberg KJ, (2007) Prospects for the use of NK cells in immunotherapy of human cancer. Nat Rev Immunol. 7: 329-339.
6. Wang RF, (2006) Regulatory T cells and innate immune regulation in tumor immunity. Springer Semin Immunopathol. 28: 17-23.
7. Zou W, (2006) Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol. 6: 295-307.
8. Bach JF, (2003) Regulatory T cells under scrutiny. Nat Rev Immunol. 3: 189-198.
9. Campbell DJ, Ziegler SF, (2007) FOXP3 modifies the phenotypic and functional properties of regulatory T cells. Nat Rev Immunol. 7: 305-310.
10. Onizuka S, Tawara I, Shimizu J, Sakaguchi S, Fujita T, et al. (1999) Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody. Cancer Res. 59: 3128-3133.
11. Gotsman I, Grabie N, Gupta R, Dacosta R, MacConmara M, et al. (2006) Impaired regulatory T-cell response and enhanced atherosclerosis in the absence of inducible costimulatory molecule. Circulation. 114: 2047-2055.
12. Akbari O, Freeman GJ, Meyer EH, Greenfield EA, Chang TT, et al. (2002) Antigen-specific regulatory T cells develop via the ICOS-ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat Med. 8: 1024-1032.
13. Ito T, Hanabuchi S, Wang YH, Park WR, Arima K, et al. (2008) Two functional subsets of FOXP3+ regulatory T cells in human thymus and periphery. Immunity. 28: 870-880.
14. Chen Y, Shen S, Gorentla BK, Gao J, Zhong XP, (2012) Murine regulatory T cells contain hyperproliferative and death-prone subsets with differential ICOS expression. J Immunol. 188: 1698-1707.
15. Mellor AL, Munn DH, (2004) IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol. 4: 762-774.
16. Gilliet M, Cao W, Liu YJ, (2008) Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol. 8: 594-606.
17. Liu YJ, (2005) IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol. 23: 275-306.
18. Hoeffel G, Ripoche AC, Matheoud D, Nascimbeni M, Escriou N, et al. (2007) Antigen crosspresentation by human plasmacytoid dendritic cells. Immunity. 27: 481-492.
19. Argani P, Iacobuzio-Donahue C, Ryu B, Rosty C, Goggins M, et al. (2001) Mesothelin is overexpressed in the vast majority of ductal adenocarcinomas of the pancreas: identification of a new pancreatic cancer marker by serial analysis of gene expression (SAGE). Clin Cancer Res. 7: 3862-3868.
20. Hassan R, Laszik ZG, Lerner M, Raffeld M, Postier R, et al. (2005) Mesothelin is overexpressed in pancreaticobiliary adenocarcinomas but not in normal pancreas and chronic pancreatitis. Am J Clin Pathol. 124: 838-845.
21. Li M, Bharadwaj U, Zhang R, Zhang S, Mu H, et al. (2008) Mesothelin is a malignant factor and therapeutic vaccine target for pancreatic cancer. Mol Cancer Ther. 7: 286-296.
22. Hassan R, Ho M, (2008) Mesothelin targeted cancer immunotherapy. Eur J Cancer. 44: 46-53.
23. Da Silva DM, Fausch SC, Verbeek JS, Kast WM, (2007) Uptake of human papillomavirus virus-like particles by dendritic cells is mediated by Fcgamma receptors and contributes to acquisition of T cell immunity. J Immunol. 178: 7587-7597.
24. Schiller JT, Lowy DR, (2001) Papillomavirus-like particle based vaccines: cervical cancer and beyond. Expert Opin Biol Ther. 1: 571-581.
25. Tegerstedt K, Lindencrona JA, Curcio C, Andreasson K, Tullus C, et al. (2005) A single vaccination with polyomavirus VP1/VP2Her2 virus-like particles prevents outgrowth of HER-2/neu-expressing tumors. Cancer Res. 65: 5953-5957.
26. Guo L, Lu X, Kang SM, Chen C, Compans RW, et al. (2003) Enhancement of mucosal immune responses by chimeric influenza HA/SHIV virus-like particles. Virology. 313: 502-513.
27. Yao Q, Zhang R, Guo L, Li M, Chen C, (2004) Th cell-independent immune responses to chimeric hemagglutinin/simian human immunodeficiency virus-like particles vaccine. J Immunol. 173: 1951-1958.
28. Barry M, Bleackley RC, (2002) Cytotoxic T lymphocytes: all roads lead to death. Nat Rev Immunol. 2: 401-409.
29. Kornete M, Sgouroudis E, Piccirillo CA, (2012) ICOS-dependent homeostasis and function of Foxp3+ regulatory T cells in islets of nonobese diabetic mice. J Immunol. 188: 1064-1074.
30. Hung CF, Tsai YC, He L, Wu TC, (2007) Control of mesothelin-expressing ovarian cancer using adoptive transfer of mesothelin peptide-specific CD8+ T cells. Gene Ther. 14: 921-929.
31. Rice J, Ottensmeier CH, Stevenson FK, (2008) DNA vaccines: precision tools for activating effective immunity against cancer. Nat Rev Cancer. 8: 108-120.
32. Banchereau J, Palucka AK, (2005) Dendritic cells as therapeutic vaccines against cancer. Nat Rev Immunol. 5: 296-306.
33. Ashley DM, Faiola B, Nair S, Hale LP, Bigner DD, et al. (1997) Bone marrow-generated dendritic cells pulsed with tumor extracts or tumor RNA induce antitumor immunity against central nervous system tumors. J Exp Med. 186: 1177-1182.
34. Goldberg SM, Bartido SM, Gardner JP, Guevara-Patino JA, Montgomery SC, et al. (2005) Comparison of two cancer vaccines targeting tyrosinase: plasmid DNA and recombinant alphavirus replicon particles. Clin Cancer Res. 11: 8114-8121.
35. Smyth MJ, Teng MW, Swann J, Kyparissoudis K, Godfrey DI, et al. (2006) CD4+CD25+ T regulatory cells suppress NK cell-mediated immunotherapy of cancer. J Immunol. 176: 1582-1587.
36. Nair S, Boczkowski D, Fassnacht M, Pisetsky D, Gilboa E, (2007) Vaccination against the forkhead family transcription factor Foxp3 enhances tumor immunity. Cancer Res. 67: 371-380.
37. Kurooka M, Kaneda Y, (2007) Inactivated Sendai virus particles eradicate tumors by inducing immune responses through blocking regulatory T cells. Cancer Res. 67: 227-236.
38. Gondek DC, Lu LF, Quezada SA, Sakaguchi S, Noelle RJ, (2005) Cutting edge: contact-mediated suppression by CD4+CD25+ regulatory cells involves a granzyme B-dependent, perforin-independent mechanism. J Immunol. 174: 1783-1786.
39. von Boehmer H, (2005) Mechanisms of suppression by suppressor T cells. Nat Immunol. 6: 338-344.
40. Fogle JE, Mexas AM, Tompkins WA, Tompkins MB, (2010) CD4(+)CD25(+) T regulatory cells inhibit CD8(+) IFN-gamma production during acute and chronic FIV infection utilizing a membrane TGF-beta-dependent mechanism. AIDS Res Hum Retroviruses. 26: 201-216.
41. Robertson SJ, Messer RJ, Carmody AB, Hasenkrug KJ, (2006) In vitro suppression of CD8+ T cell function by Friend virus-induced regulatory T cells. J Immunol. 176: 3342-3349.
42. Zhang R, Li M, Chen C, Yao Q, (2004) SHIV virus-like particles bind and activate human dendritic cells. Vaccine. 23: 139-147.
43. Colombo MP, Piconese S, (2007) Regulatory-T-cell inhibition versus depletion: the right choice in cancer immunotherapy. Nat Rev Cancer. 7: 880-887.
44. Miyamoto K, Kingsley CI, Zhang X, Jabs C, Izikson L, et al. (2005) The ICOS molecule plays a crucial role in the development of mucosal tolerance. J Immunol. 175: 7341-7347.
45. Yao Q, Kuhlmann FM, Eller R, Compans RW, Chen C, (2000) Production and characterization of simian-human immunodeficiency virus-like particles. AIDS Res Hum Retroviruses. 16: 227-236.
46. Collison LW, Vignali DA, (2011) In vitro Treg suppression assays. Methods Mol Biol. 707: 21-37.