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PMID: 25071979 Published · epublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Radiation fosters dose-dependent and chemotherapy-induced immunogenic cell death.

Oncoimmunology ·Vol. 3 ·2014-00-00 ·Pages e28518

Golden EB, Frances D, Pellicciotta I, Demaria S, Helen Barcellos-Hoff M, Formenti SC

Abstract

Established tumors are typified by an immunosuppresive microenvironment. Countering this naturally occurring phenomenon, emerging evidence suggests that radiation promotes a proimmunogenic milieu within the tumor capable of stimulating host cancer-specific immune responses. Three cryptic immunogenic components of cytotoxic-agent induced cell death-namely, calreticulin cell surface exposure, the release of high mobility group box 1 (HMGB1) protein, and the liberation of ATP-have been previously shown to be critical for dendritic cell (DC) activation and effector T-cell priming. Thus, these immune-mobilizing components commonly presage tumor rejection in response to treatment. We initially set out to address the hypothesis that radiation-induced immunogenic cell death (ICD) is dose-dependent. Next, we hypothesized that radiation would enhance chemotherapy-induced ICD when given concomitantly, as suggested by the favorable clinical outcomes observed in response to analogous concurrent chemoradiation regimens. Thus, we designed an in vitro assay to examine the 3 hallmark features of ICD at clinically relevant doses of radiation. We then tested the immunogenic-death inducing effects of radiation combined with carboplatin or paclitaxel, focusing on these combinations to mimic chemoradiation regimens actually used in clinical trials of early stage triple negative [NCT0128953/NYU-10-01969] and locally advanced [NYU-06209] breast cancer patients, respectively. Despite the obvious limitations of an in vitro model, radiotherapy produced both a dose-dependent induction and chemotherapeutic enhancement of ICD. These findings provide preliminary evidence that ICD stimulated by either high-dose radiotherapy alone, or concurrent chemoradiation regimens, may contribute to the establishment of a peritumoral proimmunogenic milieu.

Keywords
Immunogenic cell death carboplatin ionizing radiation oxaliplatin paclitaxel
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Golden Encouse B
Department of Radiation Oncology; New York University School of Medicine; New York, NY USA.
Frances Derek
Department of Radiation Oncology; New York University School of Medicine; New York, NY USA.
Pellicciotta Ilenia
Department of Radiation Oncology; New York University School of Medicine; New York, NY USA.
Demaria Sandra
Department of Radiation Oncology; New York University School of Medicine; New York, NY USA ; Department of Pathology; New York University School of Medicine; New York, NY USA.
Helen Barcellos-Hoff Mary
Department of Radiation Oncology; New York University School of Medicine; New York, NY USA.
Formenti Silvia C
Department of Radiation Oncology; New York University School of Medicine; New York, NY USA.
References (37)
37 references, click to expand
  1. The convergence of radiation and immunogenic cell death signaling pathways.
    Front Oncol. 2012 Aug 07;2:88 PMID: 22891162
  2. Calreticulin, a multifunctional Ca2+ binding chaperone of the endoplasmic reticulum.
    Biochem Cell Biol. 1998;76(5):779-85 PMID: 10353711
  3. How to improve the immunogenicity of chemotherapy and radiotherapy.
    Cancer Metastasis Rev. 2011 Mar;30(1):71-82 PMID: 21298323
  4. Immunogenic cell death in cancer therapy.
    Annu Rev Immunol. 2013;31:51-72 PMID: 23157435
  5. Molecular determinants of immunogenic cell death: surface exposure of calreticulin makes the difference.
    J Mol Med (Berl). 2007 Oct;85(10):1069-76 PMID: 17891368
  6. [Contributions of immunogenic cell death to the efficacy of anticancer chemotherapy].
    Bull Mem Acad R Med Belg. 2011;166(3-4):130-8; discussion 139-40 PMID: 22375493
  7. Differences in estimates of cisplatin-induced cell kill in vitro between colorimetric and cell count/colony assays.
    In Vitro Cell Dev Biol Anim. 2006 Nov-Dec;42(10):320-3 PMID: 17316066
  8. An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer.
    Cancer Immunol Res. 2013 Dec;1(6):365-72 PMID: 24563870
  9. Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis.
    Cell Death Differ. 2007 Oct;14(10):1848-50 PMID: 17657249
  10. Effects of chemoradiation on tumor-host interactions: the immunologic side.
    J Clin Oncol. 2008 Mar 20;26(9):1562-3; author reply 1563 PMID: 18349411
  11. Systemic effects of local radiotherapy.
    Lancet Oncol. 2009 Jul;10(7):718-26 PMID: 19573801
  12. Calreticulin exposure dictates the immunogenicity of cancer cell death.
    Nat Med. 2007 Jan;13(1):54-61 PMID: 17187072
  13. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice.
    Science. 2011 Dec 16;334(6062):1573-7 PMID: 22174255
  14. Preoperative twice-weekly paclitaxel with concurrent radiation therapy followed by surgery and postoperative doxorubicin-based chemotherapy in locally advanced breast cancer: a phase I/II trial.
    J Clin Oncol. 2003 Mar 1;21(5):864-70 PMID: 12610186
  15. Restoration of the immunogenicity of cisplatin-induced cancer cell death by endoplasmic reticulum stress.
    Oncogene. 2011 Mar 10;30(10):1147-58 PMID: 21151176
  16. Desirable cell death during anticancer chemotherapy.
    Ann N Y Acad Sci. 2010 Oct;1209:99-108 PMID: 20958322
  17. Increased level of extracellular ATP at tumor sites: in vivo imaging with plasma membrane luciferase.
    PLoS One. 2008 Jul 09;3(7):e2599 PMID: 18612415
  18. The irradiated tumor microenvironment: role of tumor-associated macrophages in vascular recovery.
    Front Physiol. 2013 Jul 17;4:157 PMID: 23882218
  19. Immunogenic tumor cell death for optimal anticancer therapy: the calreticulin exposure pathway.
    Clin Cancer Res. 2010 Jun 15;16(12):3100-4 PMID: 20421432
  20. Molecular characteristics of immunogenic cancer cell death.
    Cell Death Differ. 2008 Jan;15(1):3-12 PMID: 18007663
  21. The HaloTag: a novel technology for cell imaging and protein analysis.
    Methods Mol Biol. 2007;356:195-208 PMID: 16988404
  22. Chemotherapy and radiotherapy: cryptic anticancer vaccines.
    Semin Immunol. 2010 Jun;22(3):113-24 PMID: 20403709
  23. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays.
    J Immunol Methods. 1983 Dec 16;65(1-2):55-63 PMID: 6606682
  24. The interaction between HMGB1 and TLR4 dictates the outcome of anticancer chemotherapy and radiotherapy.
    Immunol Rev. 2007 Dec;220:47-59 PMID: 17979839
  25. Action of x-rays on mammalian cells.
    J Exp Med. 1956 May 1;103(5):653-66 PMID: 13319584
  26. Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay.
    Cancer Res. 1988 Feb 1;48(3):589-601 PMID: 3335022
  27. Combining radiotherapy and cancer immunotherapy: a paradigm shift.
    J Natl Cancer Inst. 2013 Feb 20;105(4):256-65 PMID: 23291374
  28. Chemotherapy induces ATP release from tumor cells.
    Cell Cycle. 2009 Nov 15;8(22):3723-8 PMID: 19855167
  29. Immunogenic death of colon cancer cells treated with oxaliplatin.
    Oncogene. 2010 Jan 28;29(4):482-91 PMID: 19881547
  30. A novel recombinant plasma membrane-targeted luciferase reveals a new pathway for ATP secretion.
    Mol Biol Cell. 2005 Aug;16(8):3659-65 PMID: 15944221
  31. Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody.
    Clin Cancer Res. 2009 Sep 1;15(17):5379-88 PMID: 19706802
  32. Abscopal but desirable: The contribution of immune responses to the efficacy of radiotherapy.
    Oncoimmunology. 2012 Jul 1;1(4):407-408 PMID: 22754758
  33. Immunomodulatory effects of cyclophosphamide and implementations for vaccine design.
    Semin Immunopathol. 2011 Jul;33(4):369-83 PMID: 21611872
  34. Immunologic correlates of the abscopal effect in a patient with melanoma.
    N Engl J Med. 2012 Mar 8;366(10):925-31 PMID: 22397654
  35. Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated.
    Int J Radiat Oncol Biol Phys. 2004 Mar 1;58(3):862-70 PMID: 14967443
  36. Resistance to radio- and chemotherapy and the tumour microenvironment.
    Int J Radiat Biol. 2009 Nov;85(11):920-2 PMID: 19895267
  37. Cardiac glycosides exert anticancer effects by inducing immunogenic cell death.
    Sci Transl Med. 2012 Jul 18;4(143):143ra99 PMID: 22814852
Article Info
Journal
Oncoimmunology
Abbr.
Oncoimmunology
ISSN
2162-4011
Published
2014-00-00
Epub
2014-00-25
Pages
e28518
Language
English
Region
United States
NLM ID
101570526
PMCID
PMC4106151
Grants
NCI NIH HHS · R01 CA161891 · United States
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