Доступ предоставлен для: Guest
Onco Therapeutics

Выходит 4 номеров в год

ISSN Печать: 2694-4642

ISSN Онлайн: 2694-4650

Indexed in

Harnessing Radiation Effects on the Immune System: Balancing Acts

Том 8, Выпуск 2, 2021, pp. 37-50
DOI: 10.1615/ForumImmunDisTher.2021041475
Get accessDownload

Краткое описание

The potential of radiotherapy (RT) to induce immune recognition of cancer cells is a growing topic of research. It has been suggested that partial volume irradiation used in GRID therapy/Lattice RT, a type of RT in which radiation does not cover the entire tumor intentionally but rather is spatially fractionated, sometimes induces an immune response. The therapeutic benefits of RT may not be limited solely to the targeted volume, but also present systemic antitumor effects, called the abscopal effect. The next challenge of RT now is to balance and control this immune response in patients. Here, we review what is known about the impact of RT on the innate and adaptive immune response.

ЛИТЕРАТУРА
  1. Grass GD, Krishna N, Kim S. The immune mechanisms of abscopal effect in radiation therapy. Curr Probl Cancer. 2016;40(1):10-24.

  2. Schaue D, McBride WH. Opportunities and challenges of radiotherapy for treating cancer. Nat Rev Clin Oncol. 2015;12(9):527-40.

  3. Siva S, MacManus MP, Martin RF, Martin OA. Abscopal effects of radiation therapy: A clinical review for the radiobiologist. Cancer Lett. 2015;356(1):82-90.

  4. Abuodeh Y, Venkat P, Kim S. Systematic review of case reports on the abscopal effect. Curr Probl Cancer. 2016;40(1):25-37.

  5. Vatner RE, Cooper BT, Vanpouille-Box C, Demaria S, Formenti SC. Combinations of immunotherapy and radiation in cancer therapy. Front Oncol. 2014;4:325.

  6. Tsoutsou PG, Zaman K, Martin Lluesma S, Cagnon L, Kandalaft L, Vozenin MC. Emerging opportunities of radiotherapy combined with immunotherapy in the era of breast cancer heterogeneity. Front Oncol. 2018;8:609.

  7. Ebner DK, Tinganelli W, Helm A, Bisio A, Yamada S, Kamada T, Shimokawa T, Durante M. The immunoregulatory potential of particle radiation in cancer therapy. Front Immunol. 2017;8:99.

  8. Formenti SC, Demaria S. Combining radiotherapy and cancer immunotherapy: A paradigm shift. J Natl Cancer Inst. 2013;105(4):256-65.

  9. Derer A, Frey B, Fietkau R, Gaipl US. Immune-modulating properties of ionizing radiation: Rationale for the treatment of cancer by combination radiotherapy and immune checkpoint inhibitors. Cancer Immunol Immunother. 2016;65(7):779-86.

  10. Frey B, Rubner Y, Kulzer L, Werthmoller N, Weiss EM, Fietkau R, Gaipl US. Antitumor immune responses induced by ionizing irradiation and further immune stimulation. Cancer Immunol Immunother. 2014;63(1):29-36.

  11. Herrera FG, Bourhis J, Coukos G. Radiotherapy combination opportunities leveraging immunity for the next oncology practice. CA Cancer J Clin. 2017;67(1):65-85.

  12. Chajon E, Castelli J, Marsiglia H, De Crevoisier R. The synergistic effect of radiotherapy and immunotherapy: A promising but not simple partnership. Crit Rev Oncol Hematol. 2017;111:124-32.

  13. Park B, Yee C, Lee K-M. The effect of radiation on the immune response to cancers. Int J Mol Sci. 2014;15(1):927-43.

  14. Gandhi SJ, Minn AJ, Vonderheide RH, Wherry EJ, Hahn SM, Maity A. Awakening the immune system with radiation: Optimal dose and fractionation. Cancer Lett. 2015;368(2):185-90.

  15. Shevtsov M, Sato H, Multhoff G, Shibata A. Novel approaches to improve the efficacy of immuno-radiotherapy. Front Oncol. 2019;9:156.

  16. Ma Y, Pitt JM, Li Q, Yang H. The renaissance of anti-neo-plastic immunity from tumor cell demise. Immunol Rev. 2017;280(1):194-206.

  17. Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature. 2009;461(7265):788-92.

  18. Rodriguez-Ruiz ME, Vanpouille-Box C, Melero I, Formenti SC, Demaria S. Immunological mechanisms responsible for radiation-induced abscopal effect. Trends Immunol. 2018;39(8):644-55.

  19. Bockel S, Durand B, Deutsch E. Combining radiation therapy and cancer immune therapies: From preclinical findings to clinical applications. Cancer Radiother J Soc Francaise Radiother Oncol. 2018;22(6-7):567-80.

  20. Weichselbaum RR, Liang H, Deng L, Fu YX. Radiotherapy and immunotherapy: A beneficial liaison? Nat Rev Clin Oncol. 2017;14(6):365-79.

  21. Bose D. cGAS/STING pathway in cancer: Jekyll and Hyde story of cancer immune response. Int J Mol Sci. 2017;18(11):E2456.

  22. Sokolowska O, Nowis D. STING Signaling in cancer cells: Important or not? Arch Immunol Ther Exp. 2018;66(2):125-32.

  23. Lauber K, Ernst A, Orth M, Herrmann M, Belka C. Dying cell clearance and its impact on the outcome of tumor radiotherapy. Front Oncol. 2012;2:116.

  24. Finkelstein SE, Timmerman R, McBride WH, Schaue D, Hoffe SE, Mantz CA, Wilson GD. The confluence of stereotactic ablative radiotherapy and tumor immunology. Clin Dev Immunol. 2011;2011:439752.

  25. Walle T, Martinez Monge R, Cerwenka A, Ajona D, Melero I, Lecanda F. Radiation effects on antitumor immune responses: Current perspectives and challenges. Ther Adv Med Oncol. 2018;10:1758834017742575.

  26. Carvalho H de A, Villar RC. Radiotherapy and immune response: The systemic effects of a local treatment. Clin Sao Paulo Braz. 2018;73(Suppl 1):e557s.

  27. Markovsky E, Budhu S, Samstein RM, Li H, Russell J, Zhang Z, Drill E, Bodden C, Chen Q, Powell SN, Merghoub T, Wolchok JD, Humm J, Deasy JO, Haimovitz-Friedman A. An antitumor immune response is evoked by partial-volume single-dose radiation in 2 murine models. Int J Radiat Oncol Biol Phys. 2019;103(3):697-708.

  28. Kanagavelu S, Gupta S, Wu X, Philip S, Wattenberg MM, Hodge JW, Couto MD, Chung KD, Ahmed MM. In vivo effects of lattice radiation therapy on local and distant lung cancer: Potential role of immunomodulation. Radiat Res. 2014;182(2):149-62.

  29. Hallahan D, Kuchibhotla J, Wyble C. Cell adhesion molecules mediate radiation-induced leukocyte adhesion to the vascular endothelium. Cancer Res. 1996;56(22):5150-5.

  30. Bernier J. Immuno-oncology: Allying forces of radio- and immuno-therapy to enhance cancer cell killing. Crit Rev Oncol Hematol. 2016;108:97-108.

  31. Gandhi S, Chandna S. Radiation-induced inflammatory cascade and its reverberating crosstalks as potential cause of post-radiotherapy second malignancies. Cancer Metastasis Rev. 2017;36(2):375-93.

  32. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer. 2006;6(1):24-37.

  33. Gupta A, Probst HC, Vuong V, Landshammer A, Muth S, Yagita H, Schwendener R, Pruschy M, Knuth A, van den Broek M. Radiotherapy promotes tumor-specific effector CD8+ T cells via dendritic cell activation. J Immunol. 2012;189(2):558-66.

  34. Lee Y, Auh SL, Wang Y, Burnette B, Wang Y, Meng Y, Beckett M, Sharma R, Chin R, Tu T, Weichselbaum RR, Fu YX. Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: Changing strategies for cancer treatment. Blood. 2009;114(3):589-95.

  35. Lugade AA, Moran JP, Gerber SA, Rose RC, Frelinger JG, Lord EM. Local radiation therapy of B16 melanoma tumors increases the generation of tumor antigen-specific effector cells that traffic to the tumor. J Immunol. 2005;174(12):7516-23.

  36. Schaue D, McBride WH. Links between innate immunity and normal tissue radiobiology. Radiat Res. 2010;173(4):406-17.

  37. Burnette BC, Liang H, Lee Y, Chlewicki L, Khodarev NN, Weichselbaum RR, Fu YX, Auh SL. The efficacy of radiotherapy relies upon induction of type I interfer-on-dependent innate and adaptive immunity. Cancer Res. 2011;71(7):2488-96.

  38. Gough MJ, Crittenden MR, Sarff M, Pang P, Seung SK, Vetto JT, Hu HM, Redmond WL, Holland J, Weinberg AD. Adjuvant therapy with agonistic antibodies to CD134 (0X40) increases local control after surgical or radiation therapy of cancer in mice. J Immunother. 2010;33(8):798-809.

  39. Arina A, Beckett M, Fernandez C, Zheng W, Pitroda S, Chmura SJ, Luke JJ, Forde M, Hou Y, Burnette B, Mauceri H, Lowy I, Sims T, Khodarev N, Fu YX, Weichselbaum RR. Tumor-reprogrammed resident T cells resist radiation to control tumors. Nat Commun. 2019;10(1):3959.

  40. Brent L, Medawar P. Quantitative studies on tissue trans-plantation immunity 8. The effects of irradiation. Proc R Soc Lond B Biol Sci. 1966;165(1001):413-23.

  41. Dunn PL, North RJ. Selective radiation resistance of immunologically induced T cells as the basis for irradiation-induced T-cell-mediated regression of immunogenic tumor. J Leukoc Biol. 1991;49(4):388-96.

  42. Grayson JM, Harrington LE, Lanier JG, Wherry EJ, Ahmed R. Differential sensitivity of naive and memory CD8+ T cells to apoptosis in vivo. J Immunol. 2002;169(7):3760-70.

  43. Zaid A, Mackay LK, Rahimpour A, Braun A, Veldhoen M, Carbone FR, Manton JH, Heath WR, Mueller SN. Persistence of skin-resident memory T cells within an epidermal niche. Proc Natl Acad Sci U S A. 2014;111(14):5307-12.

  44. Kammertoens T, Friese C, Arina A, Idel C, Briesemeister D, Rothe M, Ivanov A, Szymborska A, Patone G, Kunz S, Sommermeyer D, Engels B, Leisegang M, Textor A, Fehling HJ, Fruttiger M, Lohoff M, Herrmann A, Yu H, Weichselbaum R, Uckert W, Hubner N, Gerhardt H, Beule D, Schreiber H, Blankenstein T. Tumour ischaemia by interferon-y resembles physiological blood vessel regression. Nature. 2017;545(7652):98-102.

  45. Sun C, Colman M, Redpath JL. Suppression of the radiation-induced expression of a tumor-associated antigen in human cell hybrids by the protease inhibitor antipain. Carcinogenesis. 1988;9(12):2333-5.

  46. Chakraborty M, Abrams SI, Coleman CN, Camphausen K, Schlom J, Hodge JW. External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing. Cancer Res. 2004;64(12):4328-37.

  47. Newcomb EW, Demaria S, Lukyanov Y, Shao Y, Schnee T, Kawashima N, Lan L, Dewyngaert JK, Zagzag D, Mc-Bride WH, Formenti SC. The combination of ionizing radiation and peripheral vaccination produces long-term survival of mice bearing established invasive GL261 gliomas. Clin Cancer Res. 2006;12(15):4730-7.

  48. Reits EA, Hodge JW, Herberts CA, Groothuis TA, Chakraborty M, Wansley EK, Camphausen K, Luiten RM, de Ru AH, Neijssen J, Griekspoor A, Mesman E, Verreck FA, Spits H, Schlom J, van Veelen P, Neefjes JJ. Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J Exp Med. 2006;203(5):1259-71.

  49. Chiriva-Internati M, Grizzi F, Pinkston J, Morrow KJ, D'Cunha N, Frezza EE, Muzzio PC, Kast WM, Cobos E. Gamma-radiation upregulates MHC class I/II and ICAM-I molecules in multiple myeloma cell lines and primary tumors. In Vitro Cell Dev Biol Anim. 2006;42(3-4):89-95.

  50. Hallahan DE, Spriggs DR, Beckett MA, Kufe DW, Weichselbaum RR. Increased tumor necrosis factor alpha mRNA after cellular exposure to ionizing radiation. Proc Natl Acad Sci U S A. 1989;86(24):10104-7.

  51. Calveley VL, Khan MA, Yeung IWT, Vandyk J, Hill RP. Partial volume rat lung irradiation: Temporal fluctuations of in-field and out-of-field DNA damage and inflammatory cytokines following irradiation. Int J Radiat Biol. 2005;81(12):887-99.

  52. Matsumura S, Demaria S. Upregulation of the proinflammatory chemokine CXCL16 is a common response of tumor cells to ionizing radiation. Radiat Res. 2010;173(4):418-25.

  53. Matsumura S, Wang B, Kawashima N, Braunstein S, Badura M, Cameron TO, Babb JS, Schneider RJ, Formenti SC, Dustin ML, Demaria S. Radiation-induced CXCL16 release by breast cancer cells attracts effector T cells. J Immunol. 2008;181(5):3099-107.

  54. Shiao SL, Coussens LM. The tumor-immune microenvironment and response to radiation therapy. J Mammary Gland Biol Neoplasia. 2010;15(4):411-21.

  55. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, Mignot G, Maiuri MC, Ullrich E, Saulnier P, Yang H, Amigorena S, Ryffel B, Barrat FJ, Saftig P, Levi F, Lidereau R, Nogues C, Mira JP, Chompret A, Joulin V, Clavel-Chapelon F, Bourhis J, Andre F, Delaloge S, Tursz T, Kroemer G, Zitvogel L. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemo-therapy and radiotherapy. Nat Med. 2007;13(9):1050-9.

  56. Wu Q, Allouch A, Martins I, Modjtahedi N, Deutsch E, Perfettini JL. Macrophage biology plays a central role during ionizing radiation-elicited tumor response. Biomed J. 2017;40(4):200-11.

  57. Ashrafizadeh M, Farhood B, Eleojo Musa A, Taeb S, Najafi M. Damage-associated molecular patterns in tumor radiotherapy. Int Immunopharmacol. 2020;86:106761.

  58. Liu P, Zhao L, Kepp O, Kroemer G. Quantitation of calreticulin exposure associated with immunogenic cell death. Methods Enzymol. 2020;632:1-13.

  59. Perez CA, Fu A, Onishko H, Hallahan DE, Geng L. Radiation induces an antitumour immune response to mouse melanoma. Int J Radiat Biol. 2009;85(12):1126-36.

  60. Demaria S, Ng B, Devitt ML, Babb JS, Kawashima N, Liebes L, Formenti SC. Ionizing radiation inhibition of distant untreated tumors (Abscopal effect) is immune mediated. Int J Radiat Oncol Biol Phys. 2004;58(3):862-70.

  61. Dewan MZ, Galloway AE, Kawashima N, Dewyngaert JK, Babb JS, Formenti SC, Demaria S. Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody. Clin Cancer Res. 2009;15(17):5379-88.

  62. Park SS, Dong H, Liu X, Harrington SM, Krco CJ, Grams MP, Mansfield AS, Furutani KM, Olivier KR, Kwon ED. PD-1 restrains radiotherapy-induced abscopal effect. Cancer Immunol Res. 2015;3(6):610-9.

  63. Luke JJ, Lemons JM, Karrison TG, Pitroda SP, Melotek JM, Zha Y, Al-Hallaq HA, Arina A, Khodarev NN, Janisch L, Chang P, Patel JD, Fleming GF, Moroney J, Sharma MR, White JR, Ratain MJ, Gajewski TF, Weichselbaum RR, Chmura SJ. Safety and clinical activity of pem- brolizumab and multisite stereotactic body radiotherapy in patients with advanced solid tumors. J Clin Oncol. 2018;36(16):1611-8.

  64. Zhou H, Randers-Pehrson G, Waldren CA, Vannais D, Hall EJ, Hei TK. Induction of a bystander mutagenic effect of alpha particles in mammalian cells. Proc Natl Acad Sci U S A. 2000;97(5):2099-104.

  65. Nagasawa H, Little JB. Induction of sister chromatid exchanges by extremely low doses of alpha-particles. Cancer Res. 1992;52(22):6394-6.

  66. Azzam EI, de Toledo SM, Gooding T, Little JB. Intercellular communication is involved in the bystander regulation of gene expression in human cells exposed to very low fluences of alpha particles. Radiat Res. 1998;150(5):497-504.

  67. Azzam EI, De Toledo SM, Spitz DR, Little JB. Oxidative metabolism modulates signal transduction and micronucleus formation in bystander cells from alpha-particle-irradiated normal human fibroblast cultures. Cancer Res. 2002;62(19):5436-42.

  68. Azzam EI, de Toledo SM, Little JB. Stress signaling from irradiated to non-irradiated cells. Curr Cancer Drug Targets. 2004;4(1):53-64.

  69. Higgins JP, Bernstein MB, Hodge JW. Enhancing immune responses to tumor-associated antigens. Cancer Biol Ther. 2009;8(15):1440-9.

  70. Gannage M, Buzyn A, Bogiatzi SI, Lambert M, Soumelis V, Dal Cortivo L, Cavazzana-Calvo M, Brousse N, Caillat-Zucman S. Induction of NKG2D ligands by gamma radiation and tumor necrosis factor-alpha may participate in the tissue damage during acute graft-versus-host disease. Transplantation. 2008;85(6):911-5.

  71. Yamazaki T, Vanpouille-Box C, Demaria S, Galluzzi L. Immunogenic cell death driven by radiation: Impact on the tumor microenvironment. In: Lee PP, Marincola FM, editors. Tumor Microenvironment [Internet]. Cham: Springer International Publishing; 2020 [cited 2021 Sep 27]. p. 281-96. (Cancer Treatment and Research). Available from: https://doi.org/10.1007/978-3-030-38862-1_10.

  72. Lim JYH, Gerber SA, Murphy SP, Lord EM. Type I interferons induced by radiation therapy mediate recruitment and effector function of CD8(+) T cells. Cancer Immunol Immunother. 2014;63(3):259-71.

  73. Ferreira VL, Borba HHL, Bonetti A de F, P.Leonart L, Pontarolo R. Cytokines and Interferons: Types and Functions [Internet]. Autoantibodies and Cytokines. IntechOpen; 2018 [cited 2021 Jun 16]. Available from: https://www. intechopen.com/books/autoantibodies-and-cytokines/ cytokines-and-interferons-types-and-functions.

  74. Leichtle A, Hernandez M, Lee J, Pak K, Webster NJ, Wollenberg B, Wasserman SI, Ryan AF. The role of DNA sensing and innate immune receptor TLR9 in otitis media. Innate Immun. 2012;18(1):3-13.

  75. Maelfait J, Liverpool L, Bridgeman A, Ragan KB, Upton JW, Rehwinkel J. Sensing of viral and endogenous RNA by ZBP1/DAI induces necroptosis. EMBO J. 2017;36(17):2529-43.

  76. Thapa RJ, Ingram JP, Ragan KB, Nogusa S, Boyd DF, Benitez AA, Sridharan H, Kosoff R, Shubina M, Landsteiner VJ, Andrake M, Vogel P, Sigal LJ, tenOever BR, Thomas PG, Upton JW, Balachandran S. DAI senses influenza A virus genomic RNA and activates RIPK3-dependent cell death. Cell Host Microbe. 2016;20(5): 674-81.

  77. Placido D, Brown BA, Lowenhaupt K, Rich A, Athanasiadis A. A left-handed RNA double helix bound by the Z alpha domain of the RNA-editing enzyme ADAR1. Structure. 2007;15(4):395-404.

  78. Kuriakose T, Man SM, Malireddi RK, Karki R, Kesavardhana S, Place DE, Neale G, Vogel P, Kanneganti TD. ZBP1/DAI is an innate sensor of influenza virus triggering the NLRP3 inflammasome and programmed cell death pathways. Sci Immunol. 2016;1(2):aag2045.

  79. Upton JW, Kaiser WJ, Mocarski ES. DAI/ZBP1/DLM-1 complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalo-virus vIRA. Cell Host Microbe. 2012;11(3):290-7.

  80. Daniels BP, Kofman SB, Smith JR, Norris GT, Snyder AG, Kolb JP, Gao X, Locasale JW, Martinez J, Gale M Jr, Loo YM, Oberst A. The nucleotide sensor ZBP1 and kinase RIPK3 induce the enzyme IRG1 to promote an antiviral metabolic state in neurons. Immunity. 2019;50(1):64-76. e4.

  81. Sun L, Wu J, Du F, Chen X, Chen ZJ. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science. 2013;339(6121):786-91.

  82. Ergun SL, Fernandez D, Weiss TM, Li L. STING polymer structure reveals mechanisms for activation, hyperactivation, and inhibition. Cell. 2019;178(2):290-301.e10.

  83. Zhang C, Shang G, Gui X, Zhang X, Bai X-C, Chen ZJ. Structural basis of STING binding with and phosphorylation by TBK1. Nature. 2019;567(7748):394-8.

  84. Dobbs N, Burnaevskiy N, Chen D, Gonugunta VK, Alto NM, Yan N. STING activation by translocation from the ER is associated with infection and autoinflammatory disease. Cell Host Microbe. 2015;18(2):157-68.

  85. Mukai K, Konno H, Akiba T, Uemura T, Waguri S, Kobayashi T, Barber GN, Arai H, Taguchi T. Activation of STING requires palmitoylation at the Golgi. Nat Com mun. 2016;7:11932.

  86. Tanaka Y, Chen ZJ. STING Specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci Signal. 2012;5(214):ra20.

  87. Liu S, Cai X, Wu J, Cong Q, Chen X, Li T, Du F, Ren J, Wu YT, Grishin NV, Chen ZJ. Phosphorylation of innate immune adaptor proteins MAVS, STING, and TRIF induces IRF3 activation. Science. 2015;347(6227): aaa2630.

  88. Barber GN. STING: Infection, inflammation and cancer. Nat Rev Immunol. 2015;15(12):760-70.

  89. Wu J, Sun L, Chen X, Du F, Shi H, Chen C, Chen ZJ. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science. 2013;339(6121):826-30.

  90. Ablasser A, Chen ZJ. cGAS in action: Expanding roles in immunity and inflammation. Science. 2019;363(6431):eaat8657.

  91. Ablasser A, Schmid-Burgk JL, Hemmerling I, Horvath GL, Schmidt T, Latz E, Hornung V. Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature. 2013;503(7477):530-4.

  92. Lahaye X, Satoh T, Gentili M, Cerboni S, Conrad C, Hurbain I, El Marjou A, Lacabaratz C, Lelievre JD, Manel N. The capsids of HIV-1 and HIV-2 determine immune detection of the viral cDNA by the innate sensor cGAS in dendritic cells. Immunity. 2013;39(6):1132-42.

  93. Li X-D, Wu J, Gao D, Wang H, Sun L, Chen ZJ. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science. 2013;341(6152):1390-4.

  94. Liang H, Deng L, Chmura S, Burnette B, Liadis N, Darga T, Beckett MA, Lingen MW, Witt M, Weichselbaum RR, Fu YX. Radiation-induced equilibrium is a balance between tumor cell proliferation and T cell-mediated killing. J Immunol. 2013;190(11):5874-81.

  95. Wu J, Chen ZJ. Innate immune sensing and signaling of cytosolic nucleic acids. Annu Rev Immunol. 2014;32:461-88.

  96. Kondo T, Kobayashi J, Saitoh T, Maruyama K, Ishii KJ, Barber GN, Komatsu K, Akira S, Kawai T. DNA damage sensor MRE11 recognizes cytosolic double-stranded DNA and induces type I interferon by regulating STING traf-ficking. Proc Natl Acad Sci U S A. 2013;110(8):2969-74.

  97. Stavrou S, Blouch K, Kotla S, Bass A, Ross SR. Nucleic acid recognition orchestrates the antiviral response to retroviruses. Cell Host Microbe. 2015;17(4):478-88.

  98. Stavrou S, Aguilera AN, Blouch K, Ross SR. DDX41 Recognizes RNA/DNA retroviral reverse transcripts and is critical for in vivo control of murine leukemia virus infection. mBio. 9(3):e00923-18.

  99. Dunphy G, Flannery SM, Almine JF, Connolly DJ, Paulus C, Jensson KL, Jakobsen MR, Nevels MM, Bowie AG, Unterholzner L. Non-canonical activation of the DNA sensing adaptor STING by ATM and IFI16 mediates NF-KB signaling after nuclear DNA damage. Mol Cell. 2018;71(5):745-60.e5.

  100. Suschak J, Wang S, Fitzgerald KA, Lu S. A cGAS-independent STING-IRF7 pathway mediates the immunogenicity of DNA vaccines. J Immunol. 2016;196(1):310-6.

  101. Deng L, Liang H, Xu M, Yang X, Burnette B, Arina A, Li XD, Mauceri H, Beckett M, Darga T, Huang X, Gajewski TF, Chen ZJ, Fu YX, Weichselbaum RR. STING-dependent cytosolic DNA sensing promotes radiation-induced type I interferon-dependent antitumor immunity in immunogenic tumors. Immunity. 2014;41(5):843-52.

  102. Storozynsky Q, Hitt MM. The impact of radiation-induced DNA damage on cGAS-STING-mediated immune responses to cancer. Int J Mol Sci. 2020;21(22):8877.

  103. Zheng Z, Jia S, Shao C, Shi Y. Irradiation induces cancer lung metastasis through activation of the cGAS-STING-CCL5 pathway in mesenchymal stromal cells. Cell Death Dis. 2020;11(5):1-10.

  104. Peters M, Shareef M, Gupta S, Zagurovskaya-Sultanov M, Kadhim M, Mohiuddin M, Ahmed MM. Potential utilization of bystander/abscopal-mediated signal transduction events in the treatment of solid tumors. Curr Signal Transduct Ther. 2007;2(2):129-43.

  105. Yan W, Khan MK, Wu X, Simone CB 2nd, Fan J, Gressen E, Zhang X, Limoli CL, Bahig H, Tubin S, Mourad WF. Spatially fractionated radiation therapy: History, present and the future. Clin Transl Radiat Oncol. 2019;20:30-8.

  106. Chin JE, Winterrowd GE, Hatfield CA, Brashler JR, Griffin RL, Vonderfecht SL, Kolbasa KP, Fidler SF, Shull KL, Krzesicki RF, Ready KA, Dunn CJ, Sly LM, Staite ND, Richards IM. Involvement of intercellular adhesion molecule-1 in the antigen-induced infiltration of eosinophils and lymphocytes into the airways in a murine model of pulmonary inflammation. Am J Respir Cell Mol Biol. 1998;18(2):158-67.

  107. Jenkinson SR, Williams NA, Morgan DJ. The role of intercellular adhesion molecule-1/LFA-1 interactions in the generation of tumor-specific CD8+ T Cell responses. J Immunol. 2005;174(6):3401-7.

  108. Chen H, Xu L, Li L, Liu X, Gao J, Bai Y. Inhibiting the CD8+ T cell infiltration in the tumor microenvironment after radiotherapy is an important mechanism of radioresistance. Sci Rep. 2018;8(1):11934.

  109. Gupta A, Probst HC, Vuong V, Landshammer A, Muth S, Yagita H, Schwendener R, Pruschy M, Knuth A, van den Broek M. Radiotherapy promotes tumor-specific effector CD8+ T cells via dendritic cell activation. J Immunol. 2012;189(2):558-66.

  110. Deng L, Liang H, Burnette B, Beckett M, Darga T, Weichselbaum RR, Fu YX. Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice. J Clin Invest. 2014;124(2):687-95.

  111. Hou Y, Liang HL, Yu X, Liu Z, Cao X, Rao E, Huang X, Wang L, Li L, Bugno J, Fu Y, Chmura SJ, Wu W, Luo SZ, Zheng W, Arina A, Jutzy J, McCall AR, Vokes EE, Pitroda SP, Fu YX, Weichselbaum RR. Radiotherapy and immunotherapy converge on elimination of tumor-promoting erythroid progenitor cells through adaptive immunity. Sci Transl Med. 2021;13(582):eabb0130.

  112. Hezam K, Jiang J, Sun F, Zhang X, Zhang J. Artemin promotes oncogenicity, metastasis and drug resistance in cancer cells. Rev Neurosci. 2018;29(1):93-8.

  113. Han Y, Liu Q, Hou J, Gu Y, Zhang Y, Chen Z, Fan J, Zhou W, Qiu S, Zhang Y, Dong T, Li N, Jiang Z, Zhu H, Zhang Q, Ma Y, Zhang L, Wang Q, Yu Y, Li N, Cao X. Tumor-induced generation of splenic erythroblast-like Ter-cells promotes tumor progression. Cell. 2018;173(3):634-48. e12.

  114. Paillas S, Ladjohounlou R, Lozza C, Pichard A, Boudousq V, Jarlier M, Sevestre S, Le Blay M, Deshayes E, Sosabowski J, Chardes T, Navarro-Teulon I, Mairs RJ, Pouget JP. Localized irradiation of cell membrane by auger electrons is cytotoxic through oxidative stress-mediated nontargeted effects. Antioxid Redox Signal. 2016;25(8):467-84.

  115. Paris F, Fuks Z, Kang A, Capodieci P, Juan G, Ehleiter D, Haimovitz-Friedman A, Cordon-Cardo C, Kolesnick R. Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science. 2001;293(5528):293-7.

  116. Nugent S, Mothersill CE, Seymour C, McClean B, Lyng FM, Murphy JEJ. Altered mitochondrial function and genome frequency post exposure to y-radiation and by-stander factors. Int J Radiat Biol. 2010;86(10):829-41.

  117. Walsh DWM, Siebenwirth C, Greubel C, Ilicic K, Reindl J, Girst S, Muggiolu G, Simon M, Barberet P, Seznec H, Zischka H, Multhoff G, Schmid TE, Dollinger G. Live cell imaging of mitochondria following targeted irradiation in situ reveals rapid and highly localized loss of membrane potential. Sci Rep. 2017;7:46684.

  118. Persson HL, Kurz T, Eaton JW, Brunk UT. Radiation-induced cell death: Importance of lysosomal destabilization. Biochem J. 2005;389(Pt 3):877-84.

  119. Baskar R, Lee KA, Yeo R, Yeoh KW. Cancer and radiation therapy: Current advances and future directions. Int J Med Sci. 2012;9(3):193-9.

  120. Wilson JD, Hammond EM, Higgins GS, Petersson K. Ultra-high dose rate (FLASH) radiotherapy: Silver bullet or fool's gold? Front Oncol. 2020;9:1563.

  121. Loo BW, Schuler E, Lartey FM, Rafat M, King GJ, Trovati S, Koong AC, Maxim PG. (P003) Delivery of ultrarapid flash radiation therapy and demonstration of normal tissue sparing after abdominal irradiation of mice. Int J Radiat Oncol. 2017;98(2):E16.

  122. Hughes JR, Parsons JL. FLASH radiotherapy: Current knowledge and future insights using proton-beam therapy. Int J Mol Sci. 2020;21(18):6492.

  123. Blanco Suarez JM, Amendola BE, Perez N, Amendola M, Wu X. The use of lattice radiation therapy (LRT) in the treatment of bulky tumors: A case report of a large metastatic mixed Mullerian ovarian tumor. Cureus. 2015;7(11):e389.

  124. Duriseti S, Kavanaugh J, Goddu S, Price A, Knutson N, Reynoso F, Michalski J, Mutic S, Robinson C,Spraker MB. Spatially fractionated stereotactic body radiotherapy (Lattice SBRT) for large tumors. medRxiv [Preprint] 2020; https://doi.org/10.1101/2020.03.09.20033332.

  125. Amendola BE, Perez NC, Amendola MA, Wu X. The use of lattice radiation therapy in patients with voluminous tumors. Int J Radiat Oncol. 2020;108(3):e520.

  126. Liberson F. The value of a multi-perforated screen in deep x-ray therapy. Radiology. 1933;20(3):186-95.

  127. Freid JR, Lipman A, Jacobson LE. Roentgen therapy through a grid for advanced carcinoma. Am J Roentgenol Radium Ther Nucl Med. 1953;70(3):460-76.

  128. Marks H. Clinical experience with irradiation through a grid. Radiology. 1952;58(3):338-42.

  129. Mohiuddin M, Stevens JH, Reiff JE, Huq MS, Suntharalingam N. Spatially fractionated (GRID) radiation for palliative treatment of advanced cancer. Radiat Oncol Investig. 1996;4(1):41-7.

  130. Mohiuddin M, Fujita M, Regine WF, Megooni AS, Ibbott GS, Ahmed MM. High-dose spatially-fractionated radiation (GRID): A new paradigm in the management of advanced cancers. Int J Radiat Oncol Biol Phys. 1999;45(3):721-7.

  131. Zwicker RD, Meigooni A, Mohiuddin M. Therapeutic advantage of grid irradiation for large single fractions. Int J Radiat Oncol. 2004;58(4):1309-15.

  132. Neuner G, Mohiuddin MM, Vander Walde N, Goloubeva O, Ha J, Yu CX, Regine WF. High-dose spatially fractionated GRID radiation therapy (SFGRT): A comparison of treatment outcomes with Cerrobend vs. MLC SFGRT. Int J Radiat Oncol Biol Phys. 2012;82(5):1642-9.

  133. Wu X, Ahmed MM, Wright J, Gupta S, Pollack A. On modern technical approaches of three-dimensional high-dose lattice radiotherapy (LRT). Cureus [Internet]. 2010 Mar 5 [cited 2021 Jun 9];2(3). Available from: https:// www.cureus.com/articles/13-on-modern-technical-approaches-of-three-dimensional-high-dose-lattice-radio-therapy-lrt.

  134. Amendola BE, Perez NC, Wu X, Amendola MA, Qureshi IZ. Safety and efficacy of lattice radiotherapy in voluminous non-small cell lung cancer. Cureus. 2019;11(3):e4263.

  135. Amendola BE, Perez NC, Wu X, Blanco Suarez JM, Lu JJ, Amendola M. Improved outcome of treating locally advanced lung cancer with the use of lattice radiotherapy (LRT): A case report. Clin Transl Radiat Oncol. 2018;9:68-71.

  136. De Martino M, Daviaud C, Diamond JM, Kraynak J, Alard A, Formenti SC, Miller LD, Demaria S, Vanpouille-Box C. Activin A promotes regulatory T-cell-mediated immunosuppression in irradiated breast cancer. Cancer Immunol Res. 2021;9(1):89-102.

  137. Sia J, Hagekyriakou J, Chindris I, Albarakati H, Leong T, Schlenker R, Keam SP, Williams SG, Neeson PJ, Johnstone RW, Haynes NM. Regulatory T cells shape the differential impact of radiation dose-fractionation schedules on host innate and adaptive antitumor immune defenses. Int J Radiat Oncol Biol Phys. 2021;111(2):502-14.

  138. Barcellos-Hoff MH, Derynck R, Tsang ML, Weatherbee JA. Transforming growth factor-beta activation in irradiated murine mammary gland. J Clin Invest. 1994;93(2):892-9.

  139. Barker HE, Paget JTE, Khan AA, Harrington KJ. The tumour microenvironment after radiotherapy: Mechanisms of resistance and recurrence. Nat Rev Cancer. 2015;15(7):409-25.

  140. de Leve S, Wirsdorfer F, Jendrossek V. Targeting the immunomodulatory CD73/adenosine system to improve the therapeutic gain of radiotherapy. Front Immunol. 2019;10:698.

  141. Vanpouille-Box C, Diamond JM, Pilones KA, Zavadil J, Babb JS, Formenti SC, Barcellos-Hoff MH, Demaria S. TGFp is a master regulator of radiation therapy-induced antitumor immunity. Cancer Res. 2015;75(11):2232-42.

  142. Wennerberg E, Lhuillier C, Vanpouille-Box C, Pilones KA, Garcia-Martinez E, Rudqvist NP, Formenti SC, Demaria S. Barriers to radiation-induced in situ tumor vaccination. Front Immunol. 2017;8:229.

  143. Darragh LB, Oweida AJ, Karam SD. Overcoming resistance to combination radiation-immunotherapy: A focus on contributing pathways within the tumor microenvironment. Front Immunol. 2018;9:3154.

  144. Marciscano AE, Haimovitz-Friedman A, Lee P, Tran PT, Tome WA, Guha C, Spring Kong FM, Sahgal A, El Naqa I, Rimner A, Marks LB, Formenti SC, DeWeese TL. Immunomodulatory effects of stereotactic body radiation therapy: Preclinical insights and clinical opportunities. Int J Radiat Oncol Biol Phys. 2021;110(1):35-52.

  145. Yahyapour R, Amini P, Rezapour S, Cheki M, Rezaeyan A, Farhood B, Shabeeb D, Musa AE, Fallah H, Najafi M. Radiation-induced inflammation and autoimmune diseases. Mil Med Res. 2018;5(1):9.

  146. Haddadi GH, Rezaeyan A, Mosleh-Shirazi MA, Hosseinzadeh M, Fardid R, Najafi M, Salajegheh A. Hesperidin as radioprotector against radiation-induced lung damage in rat: A histopathological study. J Med Phys. 2017;42(1):25-32.

  147. Yahyapour R, Motevaseli E, Rezaeyan A, Abdollahi H, Farhood B, Cheki M, Najafi M, Villa V. Mechanisms of radiation bystander and non-targeted effects: Implications to radiation carcinogenesis and radiotherapy. Curr Radiopharm. 2018;11(1):34-45.

  148. Multhoff G, Molls M, Radons J. Chronic inflammation in cancer development. Front Immunol. 2012;2:98.

  149. Mavragani IV, Nikitaki Z, Souli MP, Aziz A, Nowsheen S, Aziz K, Rogakou E, Georgakilas AG. Complex DNA damage: A route to radiation-induced genomic instability and carcinogenesis. Cancers. 2017;9(7):91.

  150. Son Y, Lee HJ, Rho JK, Chung SY, Lee CG, Yang K, Kim SH, Lee M, Shin IS, Kim JS. The ameliorative effect of silibinin against radiation-induced lung injury: Protection of normal tissue without decreasing therapeutic efficacy in lung cancer. BMC Pulm Med. 2015;15:68.

  151. Sieber F, Muir SA, Cohen EP, North PE, Fish BL, Irving AA, Mader M, Moulder JE. High-dose selenium for the mitigation of radiation injury: A pilot study in a rat model. Radiat Res. 2009;171(3):368-73.

  152. Sieber F, Muir SA, Cohen EP, Fish BL, Mader M, Schock AM, Althouse BJ, Moulder JE. Dietary selenium for the mitigation of radiation injury: Effects of selenium dose escalation and timing of supplementation. Radiat Res. 2011;176(3):366-74.

  153. Yahyapour R, Amini P, Rezapoor S, Rezaeyan A, Farhood B, Cheki M, Fallah H, Najafi M. Targeting of inflammation for radiation protection and mitigation. Curr Mol Pharmacol. 2018;11(3):203-10.

  154. Ben-Amotz A, Yatziv S, Sela M, Greenberg S, Rachmilevich B, Shwarzman M, Weshler Z. Effect of natural beta-carotene supplementation in children exposed to radiation from the Chernobyl accident. Radiat Environ Biophys. 1998;37(3):187-93.

  155. Sylvester CB, Abe J, Patel ZS, Grande-Allen KJ. Radiation-induced cardiovascular disease: Mechanisms and importance of linear energy transfer. Front Cardiovasc Med. 2018;5:5.

  156. Ruparelia N, Chai JT, Fisher EA, Choudhury RP. Inflammatory processes in cardiovascular disease: A route to targeted therapies. Nat Rev Cardiol. 2017;14(3):133-44.

  157. Magenta A, Greco S, Gaetano C, Martelli F. Oxidative stress and microRNAs in vascular diseases. Int J Mol Sci. 2013;14(9):17319-46.

  158. Christersdottir T, Pirault J, Gistera A, Bergman O, Gallina AL, Baumgartner R, Lundberg AM, Eriksson P, Yan ZQ, Paulsson-Berne G, Hansson GK, Olofsson PS, Halle M. Prevention of radiotherapy-induced arterial inflammation by interleukin-1 blockade. Eur Heart J. 2019;40(30):2495-503.

  159. Nepali PR, Mathieu M, Kitz S, Nakauchi C, Gabriels K, Russell J, Monette S, Rimner A, Kurland IJ, Stewart FA, Jaimes EA, Haimovitz-Friedman A. Radiation exposure of the base of the heart accelerates coronary atherosclerosis. bioRxiv [Preprint] 2021; https://doi. org/10.1101/2021.04.08.438992.

  160. Korpela E, Liu SK. Endothelial perturbations and therapeutic strategies in normal tissue radiation damage. Radiat Oncol. 2014;9:266.

  161. Stewart FA, Seemann I, Hoving S, Russell NS. Under-standing radiation-induced cardiovascular damage and strategies for intervention. Clin Oncol (R Coll Radiol). 2013;25(10):617-24.

  162. Rannou E, Francois A, Toullec A, Guipaud O, Buard V, Tarlet G, Mintet E, Jaillet C, Iruela-Arispe ML, Benderitter M, Sabourin JC, Milliat F. In vivo evidence for an endothelium-dependent mechanism in radiation-induced normal tissue injury. Sci Rep. 2015;5:15738.

  163. Wiesemann A, Ketteler J, Slama A, Wirsdorfer F, Hager T, Rock K, Engel DR, Fischer JW, Aigner C, Jendrossek V, Klein D. Inhibition of radiation-induced Ccl2 signaling protects lungs from vascular dysfunction and endothelial cell loss. Antioxid Redox Signal. 2019;30(2):213-31.

  164. Hallahan DE, Virudachalam S. Intercellular adhesion molecule 1 knockout abrogates radiation induced pulmonary inflammation. Proc Natl Acad Sci. 1997;94(12):6432-7.

  165. Ishii Y, Kitamura S. Soluble intercellular adhesion molecule-1 as an early detection marker for radiation pneumonitis. Eur Respir J. 1999;13(4):733-8.

  166. Philipp J, Le Gleut R, Toerne CV, Subedi P, Azimzadeh O, Atkinson MJ, Tapio S. Radiation response of human cardiac endothelial cells reveals a central role of the cGAS-STING pathway in the development of inflammation. Proteomes. 2020;8(4):30.

  167. Zhang Y, Chen W, Wang Y. STING is an essential regulator of heart inflammation and fibrosis in mice with pathological cardiac hypertrophy via endoplasmic reticulum (ER) stress. Biomed Pharmacother. 2020;125:110022.

  168. Liu Y, Jesus AA, Marrero B, Yang D, Ramsey SE, Sanchez GAM, Tenbrock K, Wittkowski H, Jones OY, Kuehn HS, Lee CR, DiMattia MA, Cowen EW, Gonzalez B, Palmer I, DiGiovanna JJ, Biancotto A, Kim H, Tsai WL, Trier AM, Huang Y, Stone DL, Hill S, Kim HJ, St Hilaire C, Gurprasad S, Plass N, Chapelle D, Horkayne-Szakaly I, Foell D, Barysenka A, Candotti F, Holland SM, Hughes JD, Mehmet H, Issekutz AC, Raffeld M, McElwee J, Fontana JR, Minniti CP, Moir S, Kastner DL, Gadina M, Steven AC, Wingfield PT, Brooks SR, Rosenzweig SD, Fleisher TA, Deng Z, Boehm M, Paller AS, Goldbach-Mansky R. Activated STING in a vascular and pulmonary syndrome. N Engl J Med. 2014;371(6):507-18.

  169. Campisi M, Sundararaman SK, Shelton SE, Knelson EH, Mahadevan NR, Yoshida R, Tani T, Ivanova E, Canadas I, Osaki T, Lee SWL, Thai T, Han S, Piel BP, Gilhooley S, Paweletz CP, Chiono V, Kamm RD, Kitajima S, Barbie DA. Tumor-derived cGAMP regulates activation of the vasculature. Front Immunol. 2020;11:2090.

Портал Begell Электронная Бибилиотека e-Книги Журналы Справочники и Сборники статей Коллекции Цены и условия подписки Begell House Контакты Language English 中文 Русский Português German French Spain