Enhanced responses to tumor immunization following total body irradiation are time-dependent

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Diab, Adi ^a   Jenq, Robert R ^a,b   Rizzuto, Gabrielle A ^a,b   Cohen, Adam D ^a,b   Huggins, Deonka W ^a   Merghoub, Taha ^a   Engelhorn, Manuel E ^a   Guevara Patiño, José A ^a   Suh, David ^a   Hubbard Lucey, Vanessa M ^a   Kochman, Adam A ^a   Chen, Suzie ^c   Zhong, Hong ^a   Wolchok, Jedd D ^a,b   Van Den Brink, Marcel R M ^a,b   Houghton, Alan N ^a,b   Perales, Miguel Angel ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA VACCINE; PLASMID DNA;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNIZATION; CANCER RADIOTHERAPY; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; DENDRITIC CELL; DONOR LYMPHOCYTE INFUSION; FEMALE; IMMUNOPHENOTYPING; IMMUNOSTIMULATION; LYMPHOCYTOPENIA; MELANOMA; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; THERAPY EFFECT; TIME; WHOLE BODY RADIATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, NEOPLASM; AUTOANTIGENS; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; IMMUNIZATION; INTRAMOLECULAR OXIDOREDUCTASES; MELANOMA, EXPERIMENTAL; MICE; MICE, TRANSGENIC; NEOPLASMS; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES, REGULATORY; TIME FACTORS; TREATMENT OUTCOME; VACCINES, DNA; WHOLE-BODY IRRADIATION;

EID: 84892561171     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082496     Document Type: Article

References (53)

1. Perales MA, Blachere NE, Engelhorn ME, Ferrone CR, Gold JS et al. (2002) Strategies to overcome immune ignorance and tolerance. Semin Cancer Biol 12: 63-71. doi:10.1006/scbi.2001.0397. PubMed: 11926414.
2. Klebanoff CA, Acquavella N, Yu Z, Restifo NP (2011) Therapeutic cancer vaccines: are we there yet? Immunol Rev 239: 27-44. doi: 10.1111/j.1600-065X. 2010.00979.x. PubMed: 21198663.
3. Schuster SJ, Neelapu SS, Gause BL, Janik JE, Muggia FM et al. (2011) Vaccination with patient-specific tumor-derived antigen in first remission improves disease-free survival in follicular lymphoma. J Clin Oncol 29: 2787-2794. doi:10.1200/JCO.2010.33.3005. PubMed: 21632504.
4. Schwartzentruber DJ, Lawson DH, Richards JM, Conry RM, Miller DM et al. (2011) gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma. N Engl J Med 364: 2119-2127. doi:10.1056/NEJMoa1012863. PubMed: 21631324.
5. Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ et al. (2010) Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med 363: 411-422. doi:10.1056/NEJMoa1001294. PubMed: 20818862.
6. Hellström KE, Hellström I, Kant JA, Tamerius JD (1978) Regression and inhibition of sarcoma growth by interference with a radiosensitive T-cell population. J Exp Med 148: 799-804. doi:10.1084/jem.148.3. 799. PubMed: 308987.
7. Dummer W, Niethammer AG, Baccala R, Lawson BR, Wagner N et al. (2002) T cell homeostatic proliferation elicits effective antitumor autoimmunity. J Clin Invest 110: 185-192. doi:10.1172/JCI0215175. PubMed: 12122110.
8. Ma J, Urba WJ, Si L, Wang Y, Fox BA et al. (2003) Anti-tumor T cell response and protective immunity in mice that received sublethal irradiation and immune reconstitution. Eur J Immunol 33: 2123-2132. doi:10.1002/eji.200324034. PubMed: 12884286.
9. Wang LX, Shu S, Plautz GE (2005) Host lymphodepletion augments T cell adoptive immunotherapy through enhanced intratumoral proliferation of effector cells. Cancer Res 65: 9547-9554. doi: 10.1158/0008-5472.CAN-05-1175. PubMed: 16230420.
10. 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. doi:10.1084/jem.20050732. PubMed: 16203864.
11. 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. doi:10.1172/JCI24480. PubMed: 15931392.
12. Cozzo C, Larkin J 3rd, Caton AJ (2003) Cutting edge: self-peptides drive the peripheral expansion of CD4+CD25+ regulatory T cells. J Immunol 171: 5678-5682. PubMed: 14634074.
13. Baccala R, Theofilopoulos AN (2005) The new paradigm of T-cell homeostatic proliferation-induced autoimmunity. Trends Immunol 26: 5-8. doi:10.1016/j.it.2004.11.006. PubMed: 15629402.
14. Min B, Foucras G, Meier-Schellersheim M, Paul WE (2004) Spontaneous proliferation, a response of naive CD4 T cells determined by the diversity of the memory cell repertoire. Proc Natl Acad Sci U S A 101: 3874-3879. doi:10.1073/pnas.0400606101. PubMed: 15001705.
15. Ginsberg BA, Gallardo HF, Rasalan TS, Adamow M, Mu Z et al. (2010) Immunologic response to xenogeneic gp100 DNA in melanoma patients: comparison of particle-mediated epidermal delivery with intramuscular injection. Clin Cancer Res 16: 4057-4065. doi: 10.1158/1078-0432.CCR-10-1093. PubMed: 20647477.
16. Bowne WB, Srinivasan R, Wolchok JD, Hawkins WG, Blachere NE et al. (1999) Coupling and uncoupling of tumor immunity and autoimmunity. J Exp Med 190: 1717-1722. doi:10.1084/jem.190.11.1717. PubMed: 10587362.
17. Engelhorn ME, Guevara-Patiño JA, Merghoub T, Liu C, Ferrone CR et al. (2008) Mechanisms of immunization against cancer using chimeric antigens. Mol Ther 16: 773-781. doi:10.1038/mt.2008.8. PubMed: 18301399.
18. Overwijk WW, Theoret MR, Finkelstein SE, Surman DR, de Jong LA et al. (2003) Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J Exp Med 198: 569-580. doi:10.1084/jem.20030590. PubMed: 12925674. Available online at: doi:10.1084/jem.20030590 Available online at: PubMed: 12925674
19. Guevara-Patiño JA, Engelhorn ME, Turk MJ, Liu C, Duan F et al. (2006) Optimization of a self antigen for presentation of multiple epitopes in cancer immunity. J Clin Invest 116: 1382-1390. doi: 10.1172/JCI25591. PubMed: 16614758.
20. Zaft T, Sapoznikov A, Krauthgamer R, Littman DR, Jung S (2005) CD11chigh dendritic cell ablation impairs lymphopenia-driven proliferation of naive and memory CD8+ T cells. J Immunol 175: 6428-6435. PubMed: 16272295.
21. He Y, Zhang J, Donahue C, Falo LD Jr (2006) Skin-derived dendritic cells induce potent CD8(+) T cell immunity in recombinant lentivector-mediated genetic immunization. Immunity 24: 643-656. doi:10.1016/j.immuni.2006.03.014. PubMed: 16713981.
22. Mayerova D, Parke EA, Bursch LS, Odumade OA, Hogquist KA (2004) Langerhans cells activate naive self-antigen-specific CD8 T cells in the steady state. Immunity 21: 391-400. doi:10.1016/j.immuni.2004.07.019. PubMed: 15357950.
23. Shibaki A, Sato A, Vogel JC, Miyagawa F, Katz SI (2004) Induction of GVHD-like skin disease by passively transferred CD8(+) T-cell receptor transgenic T cells into keratin 14-ovalbumin transgenic mice. J Invest Dermatol 123: 109-115. doi:10.1111/j.0022-202X.2004.22701.x. PubMed: 15191550.
24. Stoitzner P, Tripp CH, Douillard P, Saeland S, Romani N (2005) Migratory Langerhans cells in mouse lymph nodes in steady state and inflammation. J Invest Dermatol 125: 116-125. doi:10.1111/j.0022-202X.2005.23757.x. PubMed: 15982311.
25. Whitmire JK, Murali-Krishna K, Altman J, Ahmed R (2000) Antiviral CD4 and CD8 T-cell memory: differences in the size of the response and activation requirements. Philos Trans R Soc Lond B Biol Sci 355: 373-379. doi:10.1098/rstb.2000.0577. PubMed: 10794058.
26. Kaech SM, Ahmed R (2001) Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat Immunol 2: 415-422. PubMed: 11323695.
27. Perales MA, Diab A, Cohen AD, Huggins DW, Guevara-Patiño JA et al. (2006) DNA immunization against tissue-restricted antigens enhances tumor immunity after allogeneic hemopoietic stem cell transplantation. J Immunol 177: 4159-4167. PubMed: 16951381.
28. Rapoport AP, Stadtmauer EA, Aqui N, Badros A, Cotte J et al. (2005) Restoration of immunity in lymphopenic individuals with cancer by vaccination and adoptive T-cell transfer. Nat Med 11: 1230-1237. doi: 10.1038/nm1310. PubMed: 16227990.
29. Perales MA, Fantuzzi G, Goldberg SM, Turk MJ, Mortazavi F et al. (2002) GM-CSF DNA induces specific patterns of cytokines and chemokines in the skin: implications for DNA vaccines. Cytokines Cell Mol Ther 7: 125-133. doi:10.1080/13684730310000923. PubMed: 12850812.
30. Xiao Z, Su Y, Yang S, Yin L, Wang W et al. (2006) Protective effect of esculentoside A on radiation-induced dermatitis and fibrosis. Int J Radiat Oncol Biol Phys 65: 882-889. doi:10.1016/j.ijrobp.2006.01.031. PubMed: 16751070.
31. Scott JE, ElKhal A, Freyschmidt EJ, MacArthur DH, McDonald D et al. (2007) Impaired immune response to vaccinia virus inoculated at the site of cutaneous allergic inflammation. J Allergy Clin Immunol 120: 1382-1388. doi:10.1016/j.jaci.2007.08.004. PubMed: 17889291.
32. Okunieff P, Xu J, Hu D, Liu W, Zhang L et al. (2006) Curcumin protects against radiation-induced acute and chronic cutaneous toxicity in mice and decreases mRNA expression of inflammatory and fibrogenic cytokines. Int J Radiat Oncol Biol Phys 65: 890-898. doi:10.1016/j.ijrobp.2006.03.025. PubMed: 16751071.
33. Cummings RJ, Mitra S, Foster TH, Lord EM (2009) Migration of skin dendritic cells in response to ionizing radiation exposure. Radiat Res 171: 687-697. doi:10.1667/RR1600.1. PubMed: 19580475.
34. Antony PA, Piccirillo CA, Akpinarli A, Finkelstein SE, Speiss PJ et al. (2005) CD8+ T cell immunity against a tumor/self-antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells. J Immunol 174: 2591-2601. PubMed: 15728465.
35. Lucas PJ, Kim SJ, Mackall CL, Telford WG, Chu YW et al. (2006) Dysregulation of IL-15-mediated T-cell homeostasis in TGF-beta dominant-negative receptor transgenic mice. Blood 108: 2789-2795. doi:10.1182/blood-2006-05- 025676. PubMed: 16788095.
36. Quezada SA, Peggs KS, Curran MA, Allison JP (2006) CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells. J Clin Invest 116: 1935-1945. doi:10.1172/JCI27745. PubMed: 16778987.
37. Sato E, Olson SH, Ahn J, Bundy B, Nishikawa H et al. (2005) Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci U S A 102: 18538-18543. doi: 10.1073/pnas.0509182102. PubMed: 16344461.
38. Klinman DM, Yi AK, Beaucage SL, Conover J, Krieg AM (1996) CpG motifs present in bacteria DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon gamma. Proc Natl Acad Sci U S A 93: 2879-2883. doi:10.1073/pnas.93.7.2879. PubMed: 8610135.
39. Shiao SL, Coussens LM (2010) The tumor-immune microenvironment and response to radiation therapy. J Mammary Gland Biol Neoplasia 15: 411-421. doi:10.1007/s10911-010-9194-9. PubMed: 21161342.
40. Demaria S, Kawashima N, Yang AM, Devitt ML, Babb JS et al. (2005) Immune-mediated inhibition of metastases after treatment with local radiation and CTLA-4 blockade in a mouse model of breast cancer. Clin Cancer Res 11: 728-734. PubMed: 15701862.
41. Chakraborty M, Abrams SI, Coleman CN, Camphausen K, Schlom J et al. (2004) External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing. Cancer Res 64: 4328-4337. doi:10.1158/0008-5472.CAN-04-0073. PubMed: 15205348.
42. Verbrugge I, Hagekyriakou J, Sharp LL, Galli M, West A et al. (2012) Radiotherapy increases the permissiveness of established mammary tumors to rejection by immunomodulatory antibodies. Cancer Res 72: 3163-3174. doi:10.1158/0008-5472.CAN-12-0210. PubMed: 22570253.
43. Dewan MZ, Galloway AE, Kawashima N, Dewyngaert JK, Babb JS et al. (2009) Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody. Clin Cancer Res 15: 5379-5388. doi: 10.1158/1078-0432.CCR-09-0265. PubMed: 19706802.
44. Lee Y, Auh SL, Wang Y, Burnette B, Wang Y et al. (2009) Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: changing strategies for cancer treatment. Blood 114: 589-595. doi: 10.1182/blood-2009-02- 206870. PubMed: 19349616.
45. Postow MA, Callahan MK, Barker CA, Yamada Y, Yuan J et al. (2012) Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med 366: 925-931. doi:10.1056/NEJMoa1112824. PubMed: 22397654.
46. Hawkins WG, Gold JS, Dyall R, Wolchok JD, Hoos A et al. (2000) Immunization with DNA coding for gp100 results in CD4 T-cell independent antitumor immunity. Surgery 128: 273-280. doi:10.1067/msy.2000.107421. PubMed: 10923004.
47. Gold JS, Ferrone CR, Guevara-Patiño JA, Hawkins WG, Dyall R et al. (2003) A single heteroclitic epitope determines cancer immunity after xenogeneic DNA immunization against a tumor differentiation antigen. J Immunol 170: 5188-5194. PubMed: 12734366.
48. Hung CF, Cheng WF, Chai CY, Hsu KF, He L et al. (2001) Improving vaccine potency through intercellular spreading and enhanced MHC class I presentation of antigen. J Immunol 166: 5733-5740. PubMed: 11313416.
49. Weber LW, Bowne WB, Wolchok JD, Srinivasan R, Qin J et al. (1998) Tumor immunity and autoimmunity induced by immunization with homologous. DNA - J Clin Invest 102: 1258-1264.
50. Ross HM, Weber LW, Wang S, Piskun G, Dyall R et al. (1997) Priming for T-cell-mediated rejection of established tumors by cutaneous DNA immunization. Clin Cancer Res 3: 2191-2196. PubMed: 9815614.
51. Dyall R, Bowne WB, Weber LW, LeMaoult J, Szabo P et al. (1998) Heteroclitic immunization induces tumor immunity. J Exp Med 188: 1553-1561. doi:10.1084/jem.188.9.1553. PubMed: 9802967.
52. Schmaltz C, Alpdogan O, Horndasch KJ, Muriglan SJ, Kappel BJ et al. (2001) Differential use of Fas ligand and perforin cytotoxic pathways by donor T cells in graft-versus-host disease and graft-versus-leukemia effect. Blood 97: 2886-2895. doi:10.1182/blood.V97.9.2886. PubMed: 11313285.
53. Schiffner S, Chen S, Becker JC, Bosserhoff AK (2012) Highly pigmented Tg(Grm1) mouse melanoma develops non-pigmented melanoma cells in distant metastases. Exp Dermatol 21: 786-788. PubMed: 22882420.