CD4+ T Cells Play a Critical Role in the Generation of Primary and Memory Antitumor Immune Responses Elicited by SA-4-1BBL and TAA-Based Vaccines in Mouse Tumor Models

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Sharma, Rajesh K ^a   Yolcu, Esma S ^a   Srivastava, Abhishek K ^a   Shirwan, Haval ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOLOGICAL ADJUVANT; PROTEIN E7; SA 4 1BBL; SURVIVIN; UNCLASSIFIED DRUG;

ADJUVANT THERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DISEASE FREE SURVIVAL; DRUG DOSE COMPARISON; DRUG EFFICACY; IMMUNOLOGICAL MEMORY; LUNG CARCINOMA; MOUSE; NONHUMAN; OPTIMAL DRUG DOSE; OVARY CANCER; T CELL DEPLETION; TUMOR GROWTH; UTERINE CERVIX CANCER;

ANIMALS; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; MICE; MICE, INBRED C57BL; UTERINE CERVICAL NEOPLASMS; VIRAL PROTEINS;

EID: 84884192283     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073145     Document Type: Article

References (44)

1. Keene JA, Forman J, (1982) Helper activity is required for the in vivo generation of cytotoxic T lymphocytes. J Exp Med 155: 768-782.
2. Sun JC, Bevan MJ, (2003) Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300: 339-342.
3. Sun JC, Williams MA, Bevan MJ, (2004) CD4+ T cells are required for the maintenance, not programming, of memory CD8+ T cells after acute infection. Nat Immunol 5: 927-933.
4. Swain SL, McKinstry KK, Strutt TM, (2012) Expanding roles for CD4(+) T cells in immunity to viruses. Nat Rev Immunol 12: 136-148.
5. Hirschhorn-Cymerman D, Budhu S, Kitano S, Liu C, Zhao F, et al. (2012) Induction of tumoricidal function in CD4+ T cells is associated with concomitant memory and terminally differentiated phenotype. J Exp Med 209: 2113-2126.
6. Mitchison NA, (1971) The carrier effect in the secondary response to hapten-protein conjugates. II. Cellular cooperation. Eur J Immunol 1: 18-27.
7. van den Broeke LT, Daschbach E, Thomas EK, Andringa G, Berzofsky JA, (2003) Dendritic cell-induced activation of adaptive and innate antitumor immunity. J Immunol 171: 5842-5852.
8. Williams MA, Tyznik AJ, Bevan MJ, (2006) Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory T cells. Nature 441: 890-893.
9. Weidanz JA, Nguyen T, Woodburn T, Neethling FA, Chiriva-Internati M, et al. (2006) Levels of specific peptide-HLA class I complex predicts tumor cell susceptibility to CTL killing. J Immunol 177: 5088-5097.
10. Bos R, Sherman LA, (2010) CD4+ T-cell help in the tumor milieu is required for recruitment and cytolytic function of CD8+ T lymphocytes. Cancer Res 70: 8368-8377.
11. 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.
12. Janssen EM, Lemmens EE, Wolfe T, Christen U, von Herrath MG, et al. (2003) CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 421: 852-856.
13. Mintern JD, Davey GM, Belz GT, Carbone FR, Heath WR, (2002) Cutting edge: precursor frequency affects the helper dependence of cytotoxic T cells. J Immunol 168: 977-980.
14. 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: 6339-6343.
15. Lin CT, Chang TC, Shaw SW, Cheng PJ, Huang CT, et al. (2006) Maintenance of CD8 effector T cells by CD4 helper T cells eradicates growing tumors and promotes long-term tumor immunity. Vaccine 24: 6199-6207.
16. Schoenberger SP, Toes RE, van der Voort EI, Offringa R, Melief CJ, (1998) T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393: 480-483.
17. Velders MP, Markiewicz MA, Eiben GL, Kast WM, (2003) CD4+ T cell matters in tumor immunity. Int Rev Immunol 22: 113-140.
18. Bullock TN, Yagita H, (2005) Induction of CD70 on dendritic cells through CD40 or TLR stimulation contributes to the development of CD8+ T cell responses in the absence of CD4+ T cells. J Immunol 174: 710-717.
19. Croft M, (2003) Co-stimulatory members of the TNFR family: keys to effective T-cell immunity? Nat Rev Immunol 3: 609-620.
20. Schabowsky RH, Sharma RK, Madireddi S, Srivastava A, Yolcu ES, et al. (2009) ProtEx technology for the generation of novel therapeutic cancer vaccines. Exp Mol Pathol 86: 198-207.
21. Schabowsky RH, Elpek KG, Madireddi S, Sharma RK, Yolcu ES, et al. (2009) A novel form of 4-1BBL has better immunomodulatory activity than an agonistic anti-4-1BB Ab without Ab-associated severe toxicity. Vaccine 28: 512-522.
22. Singh NP, Yolcu ES, Taylor DD, Gercel-Taylor C, Metzinger DS, et al. (2003) A novel approach to cancer immunotherapy: tumor cells decorated with CD80 generate effective antitumor immunity. Cancer Res 63: 4067-4073.
23. Singh NP, Miller RW, Yolcu ES, Kilinc MO, Oechsli M, et al. (2006) Primary tumor cells resected from cancer patients and decorated with a novel form of CD80 protein serve as effective antigen-presenting cells for the induction of autologous T cell immune responses ex vivo. Hum Gene Ther 17: 334-346.
24. Sharma RK, Elpek KG, Yolcu ES, Schabowsky R-H, Zhao H, et al. (2009) Costimulation as a platform for the development of vaccines: a peptide-based vaccine containing a novel from of 4-1BBL eradicates established tumors. Cancer Res 69: 4319-4326.
25. Sharma RK, Srivastava AK, Yolcu ES, MacLeod KJ, Schabowsky RH, et al. (2010) SA-4-1BBL as the immunomodulatory component of a HPV-16 E7 protein based vaccine shows robust therapeutic efficacy in a mouse cervical cancer model. Vaccine 28: 5794-5802.
26. Sharma RK, Schabowsky R-H, Srivastava A, Elpek KG, Madireddi S, et al. (2010) 4-1BB ligand as an effective multifunctional immunomodulator and antigen delivery vehicle for the development of therapeutic cancer vaccines. Cancer Res 70: 3945-3954.
27. Sharma RK, Yolcu ES, Elpek KG, Shirwan H, (2010) Tumor cells engineered to codisplay on their surface 4-1BBL and LIGHT costimulatory proteins as a novel vaccine approach for cancer immunotherapy. Cancer Gene Ther 17: 730-741.
28. Srivastava AK, Sharma RK, Yolcu ES, Ulker V, MacLeod K, et al. (2012) Prime-Boost Vaccination with SA-4-1BBL Costimulatory Molecule and Survivin Eradicates Lung Carcinoma in CD8(+) T and NK Cell Dependent Manner. PLoS One 7: e48463.
29. Rabu C, Quemener A, Jacques Y, Echasserieau K, Vusio P, et al. (2005) Production of recombinant human trimeric CD137L (4-1BBL). Cross-linking is essential to its T cell co-stimulation activity. J Biol Chem 280: 41472-41481.
30. Elpek KG, Yolcu ES, Franke DD, Lacelle C, Schabowsky RH, et al. (2007) Ex vivo expansion of CD4+ CD25+ FoxP3+ T regulatory cells based on synergy between IL-2 and 4-1BB signaling. J Immunol 179: 7295-7304.
31. Vezys V, Penaloza-MacMaster P, Barber DL, Ha SJ, Konieczny B, et al. (2011) 4-1BB signaling synergizes with programmed death ligand 1 blockade to augment CD8 T cell responses during chronic viral infection. J Immunol 187: 1634-1642.
32. Huang CY, Chen JJ, Shen KY, Chang LS, Yeh YC, et al. (2012) Recombinant lipidated HPV E7 induces a Th-1-biased immune response and protective immunity against cervical cancer in a mouse model. PLoS One 7: e40970.
33. Keene JA, Forman J, (1982) Helper activity is required for the in vivo generation of cytotoxic T lymphocytes. J Exp Med 155: 768-782.
34. Guerder S, Matzinger P, (1992) A fail-safe mechanism for maintaining self-tolerance. J Exp Med 176: 553-564.
35. Yang Y, Xiang Z, Ertl HC, Wilson JM, (1995) Upregulation of class I major histocompatibility complex antigens by interferon gamma is necessary for T-cell-mediated elimination of recombinant adenovirus-infected hepatocytes in vivo. Proc Natl Acad Sci U S A 92: 7257-7261.
36. Riberdy JM, Christensen JP, Branum K, Doherty PC, (2000) Diminished primary and secondary influenza virus-specific CD8(+) T-cell responses in CD4-depleted Ig(-/-) mice. J Virol 74: 9762-9765.
37. Novy P, Quigley M, Huang X, Yang Y, (2007) CD4 T cells are required for CD8 T cell survival during both primary and memory recall responses. J Immunol 179: 8243-8251.
38. Janssen EM, Droin NM, Lemmens EE, Pinkoski MJ, Bensinger SJ, et al. (2005) CD4+ T-cell help controls CD8+ T-cell memory via TRAIL-mediated activation-induced cell death. Nature 434: 88-93.
39. Bos R, Sherman LA, (2010) CD4+ T-cell help in the tumor milieu is required for recruitment and cytolytic function of CD8+ T lymphocytes. Cancer Res 70: 8368-8377.
40. Whitmire JK, Tan JT, Whitton JL, (2005) Interferon-gamma acts directly on CD8+ T cells to increase their abundance during virus infection. J Exp Med 201: 1053-1059.
41. Mortarini R, Piris A, Maurichi A, Molla A, Bersani I, et al. (2003) Lack of terminally differentiated tumor-specific CD8+ T cells at tumor site in spite of antitumor immunity to self-antigens in human metastatic melanoma. Cancer Res 63: 2535-2545.
42. Feltkamp MC, Smits HL, Vierboom MP, Minnaar RP, de Jongh BM, et al. (1993) Vaccination with cytotoxic T lymphocyte epitope-containing peptide protects against a tumor induced by human papillomavirus type 16-transformed cells. Eur J Immunol 23: 2242-2249.
43. Borowski AB, Boesteanu AC, Mueller YM, Carafides C, Topham DJ, et al. (2007) Memory CD8+ T cells require CD28 costimulation. J Immunol 179: 6494-6503.
44. Dolfi DV, Duttagupta PA, Boesteanu AC, Mueller YM, Oliai CH, et al. (2011) Dendritic cells and CD28 costimulation are required to sustain virus-specific CD8+ T cell responses during the effector phase in vivo. J Immunol 186: 4599-4608.