Immunological modulation of the Th1/Th2 shift by ionizing radiation in tumors (Review)
- Authors:
- Jiali Li
- Zihang Zeng
- Qiuji Wu
- Jiarui Chen
- Xingyu Liu
- Jianguo Zhang
- Yuan Luo
- Wenjie Sun
- Zhengrong Huang
- Junhong Zhang
- Yan Gong
- Conghua Xie
-
Affiliations: Department of Radiation and Medical Oncology, Zhongnan Hospital of Wuhan University, Wuhan, Hubei 430071, P.R. China, Department of Biological Repositories, Zhongnan Hospital of Wuhan University, Wuhan, Hubei 430071, P.R. China - Published online on: June 7, 2021 https://doi.org/10.3892/ijo.2021.5230
- Article Number: 50
This article is mentioned in:
Abstract
Binnewies M, Roberts EW, Kersten K, Chan V, Fearon DF, Merad M, Coussens LM, Gabrilovich DI, Ostrand-Rosenberg S, Hedrick CC, et al: Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat Med. 24:541–550. 2018. View Article : Google Scholar : PubMed/NCBI | |
Borst J, Ahrends T, Bąbała N, Melief CJM and Kastenmüller W: CD4+ T cell help in cancer immunology and immunotherapy. Nat Rev Immunol. 18:635–647. 2018. View Article : Google Scholar : PubMed/NCBI | |
Linehan WM and Ricketts CJ: The cancer genome atlas of renal cell carcinoma: Findings and clinical implications. Nat Rev Urol. 16:539–552. 2019. View Article : Google Scholar : PubMed/NCBI | |
Skinnider BF and Mak TW: The role of cytokines in classical Hodgkin lymphoma. Blood. 99:4283–4297. 2002. View Article : Google Scholar : PubMed/NCBI | |
Liu Z, Fan H and Jiang S: CD4(+) T-cell subsets in transplantation. Immunol Rev. 252:183–191. 2013. View Article : Google Scholar : PubMed/NCBI | |
Formenti SC and Demaria S: Combining radiotherapy and cancer immunotherapy: A paradigm shift. J Natl Cancer Inst. 105:256–265. 2013. View Article : Google Scholar : PubMed/NCBI | |
Masjedi A, Hashemi V, Hojjat-Farsangi M, Ghalamfarsa G, Azizi G, Yousefi M and Jadidi-Niaragh F: The significant role of interleukin-6 and its signaling pathway in the immunopathogenesis and treatment of breast cancer. Biomed Pharmacother. 108:1415–1424. 2018. View Article : Google Scholar : PubMed/NCBI | |
Zhu J and Paul WE: CD4 T cells: Fates, functions, and faults. Blood. 112:1557–1569. 2008. View Article : Google Scholar : PubMed/NCBI | |
Wan YY: GATA3: A master of many trades in immune regulation. Trends Immunol. 35:233–242. 2014. View Article : Google Scholar : PubMed/NCBI | |
Maazi H and Akbari O: Type two innate lymphoid cells: The Janus cells in health and disease. Immunol Rev. 278:192–206. 2017. View Article : Google Scholar : PubMed/NCBI | |
Afkarian M, Sedy JR, Yang J, Jacobson NG, Cereb N, Yang SY, Murphy TL and Murphy KM: T-bet is a STAT1-induced regulator of IL-12R expression in naïve CD4+ T cells. Nat Immunol. 3:549–557. 2002. View Article : Google Scholar : PubMed/NCBI | |
Tian L, Goldstein A, Wang H, Ching Lo H, Sun Kim I, Welte T, Sheng K, Dobrolecki LE, Zhang X, Putluri N, et al: Mutual regulation of tumour vessel normalization and immunostimulatory reprogramming. Nature. 544:250–254. 2017. View Article : Google Scholar : PubMed/NCBI | |
El-Darawish Y, Li W, Yamanishi K, Pencheva M, Oka N, Yamanishi H, Matsuyama T, Tanaka Y, Minato N and Okamura H: Frontline Science: IL-18 primes murine NK cells for proliferation by promoting protein synthesis, survival, and autophagy. J Leukoc Biol. 104:253–264. 2018. View Article : Google Scholar : PubMed/NCBI | |
Gupta S and Gollapudi S: Molecular mechanisms of TNF-alpha-induced apoptosis in naïve and memory T cell subsets. Autoimmun Rev. 5:264–268. 2006. View Article : Google Scholar : PubMed/NCBI | |
van Horssen R, Ten Hagen TL and Eggermont AM: TNF-alpha in cancer treatment: Molecular insights, antitumor effects, and clinical utility. Oncologist. 11:397–408. 2006. View Article : Google Scholar : PubMed/NCBI | |
Vadevoo SMP, Kim JE, Gunassekaran GR, Jung HK, Chi L, Kim DE, Lee SH, Im SH and Lee B: IL4 receptor-targeted proapoptotic peptide blocks tumor growth and metastasis by enhancing antitumor immunity. Mol Cancer Ther. 16:2803–2816. 2017. View Article : Google Scholar : PubMed/NCBI | |
Oft M: Immune regulation and cytotoxic T cell activation of IL-10 agonists-preclinical and clinical experience. Semin Immunol. 44:1013252019. View Article : Google Scholar | |
Urosevic M and Dummer R: HLA-G and IL-10 expression in human cancer-different stories with the same message. Semin Cancer Biol. 13:337–342. 2003. View Article : Google Scholar | |
Sallusto F, Lenig D, Mackay CR and Lanzavecchia A: Flexible programs of chemokine receptor expression on human polarized T helper 1 and 2 lymphocytes. J Exp Med. 187:875–883. 1998. View Article : Google Scholar : PubMed/NCBI | |
Annunziato F, Galli G, Cosmi L, Romagnani P, Manetti R, Maggi E and Romagnani S: Molecules associated with human Th1 or Th2 cells. Eur Cytokine Netw. 9(3 Suppl): S12–S16. 1998. | |
Annunziato F, Manetti R, Tomasévic I, Guidizi MG, Biagiotti R, Giannò V, Germano P, Mavilia C, Maggi E and Romagnani S: Expression and release of LAG-3-encoded protein by human CD4+ T cells are associated with IFN-gamma production. FASEB J. 10:769–776. 1996. View Article : Google Scholar : PubMed/NCBI | |
Szabo SJ, Dighe AS, Gubler U and Murphy KM: Regulation of the interleukin (IL)-12R beta 2 subunit expression in developing T helper 1 (Th1) and Th2 cells. J Exp Med. 185:817–824. 1997. View Article : Google Scholar : PubMed/NCBI | |
Loetscher P, Uguccioni M, Bordoli L, Baggiolini M, Moser B, Chizzolini C and Dayer JM: CCR5 is characteristic of Th1 lymphocytes. Nature. 391:344–345. 1998. View Article : Google Scholar : PubMed/NCBI | |
Qin S, Rottman JB, Myers P, Kassam N, Weinblatt M, Loetscher M, Koch AE, Moser B and Mackay CR: The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions. J Clin Invest. 101:746–754. 1998. View Article : Google Scholar : PubMed/NCBI | |
Sabatos CA, Chakravarti S, Cha E, Schubart A, Sánchez-Fueyo A, Zheng XX, Coyle AJ, Strom TB, Freeman GJ and Kuchroo VK: Interaction of Tim-3 and Tim-3 ligand regulates T helper type 1 responses and induction of peripheral tolerance. Nat Immunol. 4:1102–1110. 2003. View Article : Google Scholar : PubMed/NCBI | |
Xu D, Chan WL, Leung BP, Hunter D, Schulz K, Carter RW, McInnes IB, Robinson JH and Liew FY: Selective expression and functions of interleukin 18 receptor on T helper (Th) type 1 but not Th2 cells. J Exp Med. 188:1485–1492. 1998. View Article : Google Scholar : PubMed/NCBI | |
D'Ambrosio D, Iellem A, Bonecchi R, Mazzeo D, Sozzani S, Mantovani A and Sinigaglia F: Selective up-regulation of chemokine receptors CCR4 and CCR8 upon activation of polarized human type 2 Th cells. J Immunol. 161:5111–5115. 1998.PubMed/NCBI | |
Cosmi L, Annunziato F, Galli MIG, Maggi RME, Nagata K and Romagnani S: CRTH2 is the most reliable marker for the detection of circulating human type 2 Th and type 2 T cytotoxic cells in health and disease. Eur J Immunol. 30:2972–2979. 2000. View Article : Google Scholar : PubMed/NCBI | |
Groux H, Sornasse T, Cottrez F, de Vries JE, Coffman RL, Roncarolo MG and Yssel H: Induction of human T helper cell type 1 differentiation results in loss of IFN-gamma receptor beta-chain expression. J Immunol. 158:5627–5631. 1997.PubMed/NCBI | |
Jourdan P, Abbal C, Noraz N, Hori T, Uchiyama T, Vendrell JP, Bousquet J, Taylor N, Pène J and Yssel H: IL-4 induces functional cell-surface expression of CXCR4 on human T cells. J Immunol. 160:4153–4157. 1998.PubMed/NCBI | |
Xu D, Chan WL, Leung BP, Huang Fp, Wheeler R, Piedrafita D, Robinson JH and Liew FY: Selective expression of a stable cell surface molecule on type 2 but not type 1 helper T cells. J Exp Med. 187:787–794. 1998. View Article : Google Scholar : PubMed/NCBI | |
Del Prete G, De Carli M, D'Elios MM, Daniel KC, Almerigogna F, Alderson M, Smith CA, Thomas E and Romagnani S: CD30-mediated signaling promotes the development of human T helper type 2-like T cells. J Exp Med. 182:1655–1661. 1995. View Article : Google Scholar : PubMed/NCBI | |
Sallusto F, Mackay CR and Lanzavecchia A: Selective expression of the eotaxin receptor CCR3 by human T helper 2 cells. Science. 277:2005–2007. 1997. View Article : Google Scholar : PubMed/NCBI | |
Weinstein JS, Laidlaw BJ, Lu Y, Wang JK, Schulz VP, Li N, Herman EI, Kaech SM, Gallagher PG and Craft J: STAT4 and T-bet control follicular helper T cell development in viral infections. J Exp Med. 215:337–355. 2018. View Article : Google Scholar : | |
Christodoulopoulos P, Cameron L, Nakamura Y, Lemière C, Muro S, Dugas M, Boulet LP, Laviolette M, Olivenstein R and Hamid Q: TH2 cytokine-associated transcription factors in atopic and nonatopic asthma: Evidence for differential signal transducer and activator of transcription 6 expression. J Allergy Clin Immunol. 107:586–591. 2001. View Article : Google Scholar : PubMed/NCBI | |
Zheng W and Flavell RA: The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell. 89:587–596. 1997. View Article : Google Scholar : PubMed/NCBI | |
Kaplan MH, Schindler U, Smiley ST and Grusby MJ: Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity. 4:313–319. 1996. View Article : Google Scholar : PubMed/NCBI | |
Ho IC, Hodge MR, Rooney JW and Glimcher LH: The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell. 85:973–983. 1996. View Article : Google Scholar : PubMed/NCBI | |
Han SK, Song JY, Yun YS and Yi SY: Effect of gamma radiation on cytokine expression and cytokine-receptor mediated STAT activation. Int J Radiat Biol. 82:686–697. 2006. View Article : Google Scholar : PubMed/NCBI | |
Ridnour LA, Cheng RY, Weiss JM, Kaur S, Soto-Pantoja DR, Basudhar D, Heinecke JL, Stewart CA, DeGraff W, Sowers AL, et al: NOS inhibition modulates immune polarization and improves radiation-induced tumor growth delay. Cancer Res. 75:2788–2799. 2015. View Article : Google Scholar : PubMed/NCBI | |
Attar M, Molaie Kondolousy Y and Khansari N: Effect of high dose natural ionizing radiation on the immune system of the exposed residents of Ramsar Town, Iran. Iran J Allergy Asthma Immunol. 6:73–78. 2007.PubMed/NCBI | |
Karkanitsa L, Mitskevitch P, Uss A, Ostapenko V and Dainiak N: Elevated levels of cytokine gene expression in leukemic hemopoietic cells of belorussians exposed to ionizing radiation (IR) following the chernobyl catastrophe. Blood. 96:295A2000. | |
Han SK, Song JY, Yun YS and Yi SY: Ginsan improved Th1 immune response inhibited by gamma radiation. Arch Pharm Res. 28:343–350. 2005. View Article : Google Scholar : PubMed/NCBI | |
Kunwar A, Bag PP, Chattopadhyay S, Jain VK and Priyadarsini KI: Anti-apoptotic, anti-inflammatory, and immunomodulatory activities of 3,3′-diselenodipropionic acid in mice exposed to whole body γ-radiation. Arch Toxicol. 85:1395–1405. 2011. View Article : Google Scholar : PubMed/NCBI | |
Liu H, Li B, Jia X, Ma Y, Gu Y, Zhang P, Wei Q, Cai J, Cui J, Gao F and Yang Y: Radiation-induced decrease of CD8+ dendritic cells contributes to Th1/Th2 shift. Int Immunopharmacol. 46:178–185. 2017. View Article : Google Scholar : PubMed/NCBI | |
Mishra S, Patel DD, Bansal DD and Kumar R: Semiquinone glucoside derivative provides protection against γ-radiation by modulation of immune response in murine model. Environ Toxicol. 31:478–488. 2016. View Article : Google Scholar | |
Malhotra P, Adhikari M, Mishra S, Singh S, Kumar P, Singh SK and Kumar R: N-acetyl tryptophan glucopyranoside (NATG) as a countermeasure against gamma radiation-induced immunosuppression in murine macrophage J774A.1 cells. Free Radic Res. 50:1265–1278. 2016. View Article : Google Scholar : PubMed/NCBI | |
Nadella V, Ranjan R, Senthilkumaran B, Qadri SSYH, Pothani S, Singh AK, Gupta ML and Prakash H: Podophyllotoxin and rutin modulate M1 (iNOS+) macrophages and mitigate lethal radiation (LR) induced inflammatory responses in mice. Front Immunol. 10:1062019. View Article : Google Scholar : PubMed/NCBI | |
Liu XD, Ma SM and Liu SZ: Effects of 0.075 Gy x-ray irradiation on the expression of IL-10 and IL-12 in mice. Phys Med Biol. 48:2041–2049. 2003. View Article : Google Scholar : PubMed/NCBI | |
Gao H, Dong Z, Gong X, Dong J, Zhang Y, Wei W, Wang R and Jin S: Effects of various radiation doses on induced T-helper cell differentiation and related cytokine secretion. J Radiat Res. 59:395–403. 2018. View Article : Google Scholar : PubMed/NCBI | |
Karimi G, Balali-Mood M, Alamdaran SA, Badie-Bostan H, Mohammadi E, Ghorani-Azam A, Sadeghi M and Riahi-Zanjani B: Increase in the Th1-cell-based immune response in healthy workers exposed to low-dose radiation-immune system status of radiology staff. J Pharmacopuncture. 20:107–111. 2017.PubMed/NCBI | |
Cho SJ, Kang H, Hong EH, Kim JY and Nam SY: Transcriptome analysis of low-dose ionizing radiation-impacted genes in CD4+ T-cells undergoing activation and regulation of their expression of select cytokines. J Immunotoxicol. 15:137–146. 2018. View Article : Google Scholar | |
Bogdándi EN, Balogh A, Felgyinszki N, Szatmári T, Persa E, Hildebrandt G, Sáfrány G and Lumniczky K: Effects of low-dose radiation on the immune system of mice after total-body irradiation. Radiat Res. 174:480–489. 2010. View Article : Google Scholar : PubMed/NCBI | |
Elhadary AA, Marzook EA and Abdelmonem HA: Evaluation of the level of gamma radiation dose on some immune system parameters against cancer. Biosci J. 35:307–316. 2019. View Article : Google Scholar | |
Ghazy AA, Abu El-Nazar SY, Ghoneim HE, Taha AR and Abouelella AM: Effect of murine exposure to gamma rays on the interplay between Th1 and Th2 lymphocytes. Front Pharmacol. 6:742015. View Article : Google Scholar : PubMed/NCBI | |
Liu X, Liu Z, Wang D, Han Y, Hu S, Xie Y, Liu Y, Zhu M, Guan H, Gu Y and Zhou PK: Effects of low dose radiation on immune cells subsets and cytokines in mice. Toxicol Res (Camb). 9:249–262. 2020. View Article : Google Scholar | |
Steinman RM: Decisions about dendritic cells: Past, present, and future. Annu Rev Immunol. 30:1–22. 2012. View Article : Google Scholar | |
Arpinati M, Green CL, Heimfeld S, Heuser JE and Anasetti C: Granulocyte-colony stimulating factor mobilizes T helper 2-inducing dendritic cells. Blood. 95:2484–2490. 2000. View Article : Google Scholar | |
Jutel M and Akdis CA: T-cell subset regulation in atopy. Curr Allergy Asthma Rep. 11:139–145. 2011. View Article : Google Scholar : PubMed/NCBI | |
Merrick A, Errington F, Milward K, O'Donnell D, Harrington K, Bateman A, Pandha H, Vile R, Morrison E, Selby P and Melcher A: Immunosuppressive effects of radiation on human dendritic cells: Reduced IL-12 production on activation and impairment of naive T-cell priming. Br J Cancer. 92:1450–1458. 2005. View Article : Google Scholar : PubMed/NCBI | |
Clerici M, Shearer GM and Clerici E: Cytokine dysregulation in invasive cervical carcinoma and other human neoplasias: Time to consider the TH1/TH2 paradigm. J Natl Cancer Inst. 90:261–263. 1998. View Article : Google Scholar : PubMed/NCBI | |
Lappin MB and Campbell JD: The Th1-Th2 classification of cellular immune responses: Concepts, current thinking and applications in haematological malignancy. Blood Rev. 14:228–239. 2000. View Article : Google Scholar : PubMed/NCBI | |
Backer RA, Diener N and Clausen BE: Langerin+CD8+ dendritic cells in the splenic marginal zone: Not so marginal after all. Front Immunol. 10:7412019. View Article : Google Scholar | |
Prendergast KA, Daniels NJ, Petersen TR, Hermans IF and Kirman JR: Langerin+ CD8α+ dendritic cells drive early CD8+ T cell activation and IL-12 production during systemic bacterial infection. Front Immunol. 9:9532018. View Article : Google Scholar | |
Yu N, Wang S, Song X, Gao L, Li W, Yu H, Zhou C, Wang Z, Li F and Jiang Q: Low-dose radiation promotes dendritic cell migration and IL-12 production via the ATM/NF-kappaB pathway. Radiat Res. 189:409–417. 2018. View Article : Google Scholar : PubMed/NCBI | |
Shigematsu A, Adachi Y, Koike-Kiriyama N, Suzuki Y, Iwasaki M, Koike Y, Nakano K, Mukaide H, Imamura M and Ikehara S: Effects of low-dose irradiation on enhancement of immunity by dendritic cells. J Radiat Res. 48:51–55. 2007. View Article : Google Scholar | |
Murray PJ: Macrophage polarization. Annu Rev Physiol. 79:541–566. 2017. View Article : Google Scholar | |
Orecchioni M, Ghosheh Y, Pramod AB and Ley K: Macrophage polarization: Different gene signatures in M1(LPS+) vs. classically and M2(LPS-) vs. alternatively activated macrophages. Front Immunol. 10:10842019. View Article : Google Scholar : PubMed/NCBI | |
Shapouri-Moghaddam A, Mohammadian S, Vazini H, Taghadosi M, Esmaeili SA, Mardani F, Seifi B, Mohammadi A, Afshari JT and Sahebkar A: Macrophage plasticity, polarization, and function in health and disease. J Cell Physiol. 233:6425–6440. 2018. View Article : Google Scholar : PubMed/NCBI | |
Shiratori H, Feinweber C, Luckhardt S, Wallner N, Geisslinger G, Weigert A and Parnham MJ: An in vitro test system for compounds that modulate human inflammatory macrophage polarization. Eur J Pharmacol. 833:328–338. 2018. View Article : Google Scholar : PubMed/NCBI | |
Nadella V, Singh S, Jain A, Jain M, Vasquez KM, Sharma A, Tanwar P, Rath GK and Prakash H: Low dose radiation primed iNOS + M1macrophages modulate angiogenic programming of tumor derived endothelium. Mol Carcinog. 57:1664–1671. 2018. View Article : Google Scholar : PubMed/NCBI | |
Knoops L, Haas R, de Kemp S, Majoor D, Broeks A, Eldering E, de Boer JP, Verheij M, van Ostrom C, de Vries A, et al: In vivo p53 response and immune reaction underlie highly effective low-dose radiotherapy in follicular lymphoma. Blood. 110:1116–1122. 2007. View Article : Google Scholar : PubMed/NCBI | |
Seifert L, Werba G, Tiwari S, Giao Ly NN, Nguy S, Alothman S, Alqunaibit D, Avanzi A, Daley D, Barilla R, et al: Radiation therapy induces macrophages to suppress T-cell responses against pancreatic tumors in mice. Gastroenterology. 150:1659–1672.e5. 2016. View Article : Google Scholar : PubMed/NCBI | |
Okubo M, Kioi M, Nakashima H, Sugiura K, Mitsudo K, Aoki I, Taniguchi H and Tohnai I: M2-polarized macrophages contribute to neovasculogenesis, leading to relapse of oral cancer following radiation. Sci Rep. 6:275482016. View Article : Google Scholar : PubMed/NCBI | |
Fu E, Liu T, Yu S, Chen X, Song L, Lou H, Ma F, Zhang S, Hussain S, Guo J, et al: M2 macrophages reduce the radiosensitivity of head and neck cancer by releasing HB-EGF. Oncol Rep. 44:698–710. 2020. View Article : Google Scholar : PubMed/NCBI | |
Reading JL, Gálvez-Cancino F, Swanton C, Lladser A, Peggs KS and Quezada SA: The function and dysfunction of memory CD8+ T cells in tumor immunity. Immunol Rev. 283:194–212. 2018. View Article : Google Scholar : PubMed/NCBI | |
Crespo J, Sun H, Welling TH, Tian Z and Zou W: T cell anergy, exhaustion, senescence, and stemness in the tumor microenvironment. Curr Opin Immunol. 25:214–221. 2013. View Article : Google Scholar : PubMed/NCBI | |
Lee Y, Auh SL, Wang Y, Burnette B, Wang Y, Meng Y, Beckett M, Sharma R, Chin R, Tu T, et al: Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: Changing strategies for cancer treatment. Blood. 114:589–595. 2009. View Article : Google Scholar : PubMed/NCBI | |
Lugade AA, Moran JP, Gerber SA, Rose RC, Frelinger JG and 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. 174:7516–7523. 2005. View Article : Google Scholar : PubMed/NCBI | |
Takeshima T, Chamoto K, Wakita D, Ohkuri T, Togashi Y, Shirato H, Kitamura H and Nishimura T: Local radiation therapy inhibits tumor growth through the generation of tumor-specific CTL: Its potentiation by combination with Th1 cell therapy. Cancer Res. 70:2697–2706. 2010. View Article : Google Scholar : PubMed/NCBI | |
Chattopadhyay S and Chakraborty NG: Continuous presence of Th1 conditions is necessary for longer lasting tumor-specific CTL activity in stimulation cultures with PBL. Hum Immunol. 66:884–891. 2005. View Article : Google Scholar : PubMed/NCBI | |
Harada M, Matsueda S, Yao A, Noguchi M and Itoh K: Vaccination of cytotoxic T lymphocyte-directed peptides elicited and spread humoral and Th1-type immune responses to prostate-specific antigen protein in a prostate cancer patient. J Immunother. 28:368–375. 2005. View Article : Google Scholar : PubMed/NCBI | |
Yokouchi H, Chamoto K, Wakita D, Yamazaki K, Shirato H, Takeshima T, Dosaka-Akita H, Nishimura M, Yue Z, Kitamura H and Nishimura T: Combination tumor immunotherapy with radiotherapy and Th1 cell therapy against murine lung carcinoma. Clin Exp Metastasis. 24:533–540. 2007. View Article : Google Scholar : PubMed/NCBI | |
Terrén I, Orrantia A, Vitallé J, Zenarruzabeitia O and Borrego F: NK cell metabolism and tumor microenvironment. Front Immunol. 10:22782019. View Article : Google Scholar : PubMed/NCBI | |
Hodgins JJ, Khan ST, Park MM, Auer RC and Ardolino M: Killers 2.0: NK cell therapies at the forefront of cancer control. J Clin Invest. 129:3499–3510. 2019. View Article : Google Scholar : PubMed/NCBI | |
Wei H, Zheng X, Lou D, Zhang L, Zhang R, Sun R and Tian Z: Tumor-induced suppression of interferon-gamma production and enhancement of interleukin-10 production by natural killer (NK) cells: Paralleled to CD4+ T cells. Mol Immunol. 42:1023–1031. 2005. View Article : Google Scholar : PubMed/NCBI | |
Yang G, Kong Q, Wang G, Jin H, Zhou L, Yu D, Niu C, Han W, Li W and Cui J: Low-dose ionizing radiation induces direct activation of natural killer cells and provides a novel approach for adoptive cellular immunotherapy. Cancer Biother Radiopharm. 29:428–434. 2014. View Article : Google Scholar : PubMed/NCBI | |
Cheda A, Wrembel-Wargocka J, Lisiak E, Nowosielska EM, Marciniak M and Janiak MK: Single low doses of X rays inhibit the development of experimental tumor metastases and trigger the activities of NK cells in mice. Radiat Res. 161:335–340. 2004. View Article : Google Scholar : PubMed/NCBI | |
Miller GM, Andres ML and Gridley DS: NK cell depletion results in accelerated tumor growth and attenuates the antitumor effect of total body irradiation. Int J Oncol. 23:1585–1592. 2003.PubMed/NCBI | |
Park HR, Jung U and Jo SK: Impairment of natural killer (NK) cells is an important factor in a weak Th1-like response in irradiated mice. Radiat Res. 168:446–452. 2007. View Article : Google Scholar : PubMed/NCBI | |
Zarcone D, Tilden AB, Lane VG and Grossi CE: Radiation sensitivity of resting and activated nonspecific cytotoxic cells of T lineage and NK lineage. Blood. 73:1615–1621. 1989. View Article : Google Scholar : PubMed/NCBI | |
Zhou L, Zhang X, Li H, Niu C, Yu D, Yang G, Liang X, Wen X, Li M and Cui J: Validating the pivotal role of the immune system in low-dose radiation-induced tumor inhibition in Lewis lung cancer-bearing mice. Cancer Med. 7:1338–1348. 2018. View Article : Google Scholar : PubMed/NCBI | |
Zhou J, Zhang J, Lichtenheld MG and Meadows GG: A role for NF-kappa B activation in perforin expression of NK cells upon IL-2 receptor signaling. J Immunol. 169:1319–1325. 2002. View Article : Google Scholar : PubMed/NCBI | |
Herrera FG, Bourhis J and Coukos G: Radiotherapy combination opportunities leveraging immunity for the next oncology practice. CA Cancer J Clin. 67:65–85. 2017. View Article : Google Scholar | |
Demaria S, Golden EB and Formenti SC: Role of local radiation therapy in cancer immunotherapy. JAMA Oncol. 1:1325–1332. 2015. View Article : Google Scholar : PubMed/NCBI | |
Simon PS, Bardhan K, Chen MR, Paschall AV, Lu C, Bollag RJ, Kong FC, Jin J, Kong FM, Waller JL, et al: NF-κB functions as a molecular link between tumor cells and Th1/Tc1 T cells in the tumor microenvironment to exert radiation-mediated tumor suppression. Oncotarget. 7:23395–23415. 2016. View Article : Google Scholar : PubMed/NCBI | |
Matsumura S, Wang B, Kawashima N, Braunstein S, Badura M, Cameron TO, Babb JS, Schneider RJ, Formenti SC, Dustin ML and Demaria S: Radiation-induced CXCL16 release by breast cancer cells attracts effector T cells. J Immunol. 181:3099–3107. 2008. View Article : Google Scholar : PubMed/NCBI | |
Song KH, Jung SY, Kang SM, Kim MH, Ahn J, Hwang SG, Lee JH, Lim DS, Nam SY and Song JY: Induction of immunogenic cell death by radiation-upregulated karyopherin alpha 2 in vitro. Eur J Cell Biol. 95:219–227. 2016. View Article : Google Scholar : PubMed/NCBI | |
Song KH, Jung SY, Park JI, Ahn J, Park JK, Um HD, Park IC, Hwang SG, Ha H and Song JY: Inhibition of karyopherin-α2 augments radiation-induced cell death by perturbing BRCA1-mediated DNA repair. Int J Mol Sci. 20:28432019. View Article : Google Scholar | |
Huettner C, Paulus W and Roggendorf W: Messenger RNA expression of the immunosuppressive cytokine IL-10 in human gliomas. Am J Pathol. 146:317–322. 1995.PubMed/NCBI | |
Hao C, Parney IF, Roa WH, Turner J, Petruk KC and Ramsay DA: Cytokine and cytokine receptor mRNA expression in human glioblastomas: Evidence of Th1, Th2 and Th3 cytokine dysregulation. Acta Neuropathol. 103:171–178. 2002. View Article : Google Scholar : PubMed/NCBI | |
Chen B, Alvarado DM, Iticovici M, Kau NS, Park H, Parikh PJ, Thotala D and Ciorba MA: Interferon-induced IDO1 mediates radiation resistance and is a therapeutic target in colorectal cancer. Cancer Immunol Res. 8:451–464. 2020. View Article : Google Scholar : PubMed/NCBI | |
Hanania AN, Mainwaring W, Ghebre YT, Hanania NA and Ludwig M: Radiation-induced lung injury: Assessment and management. Chest. 156:150–162. 2019. View Article : Google Scholar : PubMed/NCBI | |
Giuranno L, Ient J, De Ruysscher D and Vooijs MA: Radiation-induced lung injury (RILI). Front Oncol. 9:8772019. View Article : Google Scholar : PubMed/NCBI | |
Stenmark MH, Cai XW, Shedden K, Hayman JA, Yuan S, Ritter T, Ten Haken RK, Lawrence TS and Kong FM: Combining physical and biologic parameters to predict radiation-induced lung toxicity in patients with non-small-cell lung cancer treated with definitive radiation therapy. Int J Radiat Oncol Biol Phys. 84:e217–e222. 2012. View Article : Google Scholar : PubMed/NCBI | |
Rübe CE, Rodemann HP and Rübe C: The relevance of cytokines in the radiation-induced lung reaction. Experimental basis and clinical significance. Strahlenther Onkol. 180:541–549. 2004.In German. View Article : Google Scholar | |
Arpin D, Perol D, Blay JY, Falchero L, Claude L, Vuillermoz-Blas S, Martel-Lafay I, Ginestet C, Alberti L, Nosov D, et al: Early variations of circulating interleukin-6 and interleukin-10 levels during thoracic radiotherapy are predictive for radiation pneumonitis. J Clin Oncol. 23:8748–8756. 2005. View Article : Google Scholar : PubMed/NCBI | |
Büttner C, Skupin A, Reimann T, Rieber EP, Unteregger G, Geyer P and Frank KH: Local production of interleukin-4 during radiation-induced pneumonitis and pulmonary fibrosis in rats: Macrophages as a prominent source of interleukin-4. Am J Respir Cell Mol Biol. 17:315–325. 1997. View Article : Google Scholar : PubMed/NCBI | |
Chen Y, Rubin P, Williams J, Hernady E, Smudzin T and Okunieff P: Circulating IL-6 as a predictor of radiation pneumonitis. Int J Radiat Oncol Biol Phys. 49:641–648. 2001. View Article : Google Scholar : PubMed/NCBI | |
Tang Y, Yang L, Qin W, Yi M, Liu B and Yuan X: Validation study of the association between genetic variant of IL4 and severe radiation pneumonitis in lung cancer patients treated with radiation therapy. Radiother Oncol. 141:86–94. 2019. View Article : Google Scholar : PubMed/NCBI | |
Li Y, Guan X, Liu W, Chen HL, Truscott J, Beyatli S, Metwali A, Weiner GJ, Zavazava N, Blumberg RS, et al: Helminth-induced production of TGF-β and suppression of graft-versus-host disease is dependent on IL-4 production by host cells. J Immunol. 201:2910–2922. 2018. View Article : Google Scholar : PubMed/NCBI | |
Groves AM, Johnston CJ, Misra RS, Williams JP and Finkelstein JN: Effects of IL-4 on pulmonary fibrosis and the accumulation and phenotype of macrophage subpopulations following thoracic irradiation. Int J Radiat Biol. 92:754–765. 2016. View Article : Google Scholar : PubMed/NCBI | |
Han G, Zhang H, Xie CH and Zhou YF: Th2-like immune response in radiation-induced lung fibrosis. Oncol Rep. 26:383–388. 2011.PubMed/NCBI | |
Paun A, Bergeron ME and Haston CK: The Th1/Th17 balance dictates the fibrosis response in murine radiation-induced lung disease. Sci Rep. 7:115862017. View Article : Google Scholar : PubMed/NCBI | |
Xu L, Xiong S, Guo R, Yang Z, Wang Q, Xiao F, Wang H, Pan X and Zhu M: Transforming growth factor β3 attenuates the development of radiation-induced pulmonary fibrosis in mice by decreasing fibrocyte recruitment and regulating IFN-gamma/IL-4 balance. Immunol Lett. 162:27–33. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chiang CS, Liu WC, Jung SM, Chen FH, Wu CR, McBride WH, Lee CC and Hong JH: Compartmental responses after thoracic irradiation of mice: Strain differences. Int J Radiat Oncol Biol Phys. 62:862–871. 2005. View Article : Google Scholar : PubMed/NCBI | |
Zhang C, Zhao H, Li BL, Fu-Gao, Liu H, Cai JM and Zheng M: CpG-oligodeoxynucleotides may be effective for preventing ionizing radiation induced pulmonary fibrosis. Toxicol Lett. 292:181–189. 2018. View Article : Google Scholar : PubMed/NCBI | |
Huang Y, Liu W, Liu H, Yang Y, Cui J, Zhang P, Zhao H, He F, Cheng Y, Ni J, et al: Grape seed pro-anthocyanidins ameliorates radiation-induced lung injury. J Cell Mol Med. 18:1267–1277. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chen J, Wang Y, Mei Z, Zhang S, Yang J, Li X, Yao Y and Xie C: Radiation-induced lung fibrosis in a tumor-bearing mouse model is associated with enhanced Type-2 immunity. J Radiat Res. 57:133–141. 2016. View Article : Google Scholar : | |
Oh K, Seo MW, Kim YW and Lee DS: Osteopontin potentiates pulmonary inflammation and fibrosis by modulating IL-17/IFN-γ-secreting T-cell ratios in bleomycin-treated mice. Immune Netw. 15:142–149. 2015. View Article : Google Scholar : PubMed/NCBI | |
Lei L, Zhao C, Qin F, He ZY, Wang X and Zhong XN: Th17 cells and IL-17 promote the skin and lung inflammation and fibrosis process in a bleomycin-induced murine model of systemic sclerosis. Clin Exp Rheumatol. 34(Suppl 100): S14–S22. 2016. | |
Li Y, Zou L, Yang X, Chu L, Ni J, Chu X, Guo T and Zhu Z: Identification of lncRNA, MicroRNA, and mRNA-associated CeRNA network of radiation-induced lung injury in a mice model. Dose Response. 17:15593258198910122019. View Article : Google Scholar : PubMed/NCBI | |
Hauer-Jensen M, Denham JW and Andreyev HJ: Radiation enteropathy-pathogenesis, treatment and prevention. Nat Rev Gastroenterol Hepatol. 11:470–479. 2014. View Article : Google Scholar : PubMed/NCBI | |
Zheng J, Wang J, Pouliot M, Authier S, Zhou D, Loose DS and Hauer-Jensen M: Gene expression profiling in non-human primate jejunum, ileum and colon after total-body irradiation: A comparative study of segment-specific molecular and cellular responses. BMC Genomics. 16:9842015. View Article : Google Scholar : PubMed/NCBI | |
Huang Z, Epperly M, Watkins SC, Greenberger JS, Kagan VE and Bayır H: Necrostatin-1 rescues mice from lethal irradiation. Biochim Biophys Acta. 1862:850–856. 2016. View Article : Google Scholar : PubMed/NCBI | |
Kim JS, Ryoo SB, Heo K, Kim JG, Son TG, Moon C and Yang K: Attenuating effects of granulocyte-colony stimulating factor (G-CSF) in radiation induced intestinal injury in mice. Food Chem Toxicol. 50:3174–3180. 2012. View Article : Google Scholar : PubMed/NCBI | |
Kim JS, Yang M, Lee CG, Kim SD, Kim JK and Yang K: In vitro and in vivo protective effects of granulocyte colony-stimulating factor against radiation-induced intestinal injury. Arch Pharm Res. 36:1252–1261. 2013. View Article : Google Scholar : PubMed/NCBI | |
Symon Z, Goldshmidt Y, Picard O, Yavzori M, Ben-Horin S, Alezra D, Barshack I and Chowers Y: A murine model for the study of molecular pathogenesis of radiation proctitis. Int J Radiat Oncol Biol Phys. 76:242–250. 2010. View Article : Google Scholar | |
Sha H, Gu Y, Shen W, Zhang L, Qian F, Zhao Y, Li H, Zhang T and Lu W: Rheinic acid ameliorates radiation-induced acute enteritis in rats through PPAR-γ/NF-κB. Genes Genomics. 41:909–917. 2019. View Article : Google Scholar : PubMed/NCBI | |
Lu L, Li W, Sun C, Kang S, Li J, Luo X, Su Q, Liu B and Qin S: Phycocyanin ameliorates radiation-induced acute intestinal toxicity by regulating the effect of the gut microbiota on the TLR4/Myd88/NF-κB pathway. JPEN J Parenter Enteral Nutr. 44:1308–1317. 2020. View Article : Google Scholar | |
Wei YL, Xu JY, Zhang R, Zhang Z, Zhao L and Qin LQ: Effects of lactoferrin on X-ray-induced intestinal injury in Balb/C mice. Appl Radiat Isot. 146:72–77. 2019. View Article : Google Scholar : PubMed/NCBI | |
Radwan RR and Karam HM: Resveratrol attenuates intestinal injury in irradiated rats via PI3K/Akt/mTOR signaling pathway. Environ Toxicol. 35:223–230. 2020. View Article : Google Scholar | |
Wang H, Sun RT, Li Y, Yang YF, Xiao FJ, Zhang YK, Wang SX, Sun HY, Zhang QW, Wu CT and Wang LS: HGF gene modification in mesenchymal stem cells reduces radiation-induced intestinal injury by modulating immunity. PLoS One. 10:e01244202015. View Article : Google Scholar : PubMed/NCBI | |
Chang P, Qu Y, Liu Y, Cui S, Zhu D, Wang H and Jin X: Multi-therapeutic effects of human adipose-derived mesenchymal stem cells on radiation-induced intestinal injury. Cell Death Dis. 4:e6852013. View Article : Google Scholar : PubMed/NCBI | |
Linard C, Strup-Perrot C, Lacave-Lapalun JV and Benderitter M: Flagellin preconditioning enhances the efficacy of mesenchymal stem cells in an irradiation-induced proctitis model. J Leukoc Biol. 100:569–580. 2016. View Article : Google Scholar : PubMed/NCBI | |
Akpolat M, Gulle K, Topcu-Tarladacalisir Y, Safi Oz Z, Bakkal BH, Arasli M and Ozel Turkcu U: Protection by L-carnitine against radiation-induced ileal mucosal injury in the rat: Pattern of oxidative stress, apoptosis and cytokines. Int J Radiat Biol. 89:732–740. 2013. View Article : Google Scholar : PubMed/NCBI | |
Bessout R, Demarquay C, Moussa L, René A, Doix B, Benderitter M, Sémont A and Mathieu N: TH17 predominant T-cell responses in radiation-induced bowel disease are modulated by treatment with adipose-derived mesenchymal stromal cells. J Pathol. 237:435–446. 2015. View Article : Google Scholar : PubMed/NCBI | |
Balentova S and Adamkov M: Molecular, cellular and functional effects of radiation-induced brain injury: A review. Int J Mol Sci. 16:27796–27815. 2015. View Article : Google Scholar : PubMed/NCBI | |
Deng Z, Sui G, Rosa PM and Zhao W: Radiation-induced c-Jun activation depends on MEK1-ERK1/2 signaling pathway in microglial cells. PLoS One. 7:e367392012. View Article : Google Scholar : PubMed/NCBI | |
Xue J, Dong JH, Huang GD, Qu XF, Wu G and Dong XR: NF-κB signaling modulates radiation-induced microglial activation. Oncol Rep. 31:2555–2560. 2014. View Article : Google Scholar : PubMed/NCBI | |
Dong X, Luo M, Huang G, Zhang J, Tong F, Cheng Y, Cai Q, Dong J, Wu G and Cheng J: Relationship between irradiation-induced neuro-inflammatory environments and impaired cognitive function in the developing brain of mice. Int J Radiat Biol. 91:224–239. 2015. View Article : Google Scholar | |
Chen LJ, Zhang RG, Yu DD, Wu G and Dong XR: Shenqi fuzheng injection ameliorates radiation-induced brain injury. Curr Med Sci. 39:965–971. 2019. View Article : Google Scholar : PubMed/NCBI | |
Xin N, Li YJ, Li X, Wang X, Li Y, Zhang X, Dai RJ, Meng WW, Wang HL, Ma H, et al: Dragon's blood may have radioprotective effects in radiation-induced rat brain injury. Radiat Res. 178:75–85. 2012. View Article : Google Scholar : PubMed/NCBI | |
Chiang CS, Hong JH, Stalder A, Sun JR, Withers HR and McBride WH: Delayed molecular responses to brain irradiation. Int J Radiat Biol. 72:45–53. 1997. View Article : Google Scholar : PubMed/NCBI | |
Vozenin-Brotons MC, Gault N, Sivan V, Tricaud Y, Dubray B, Clough K, Cosset JM, Lefaix JL and Martin M: Histopathological and cellular studies of a case of cutaneous radiation syndrome after accidental chronic exposure to a cesium source. Radiat Res. 152:332–337. 1999. View Article : Google Scholar : PubMed/NCBI | |
Lee JW, Zoumalan RA, Valenzuela CD, Nguyen PD, Tutela JP, Roman BR, Warren SM and Saadeh PB: Regulators and mediators of radiation-induced fibrosis: Gene expression profiles and a rationale for Smad3 inhibition. Otolaryngol Head Neck Surg. 143:525–530. 2010. View Article : Google Scholar : PubMed/NCBI | |
Blétry O and Somogyi A: Do the interferons have an antifibrotic action? The internist's point of view. Rev Med Interne. 23(Suppl 4): 511s–515s. 2002.In French. View Article : Google Scholar | |
Peter RU, Gottlöber P, Nadeshina N, Krähn G, Braun-Falco O and Plewig G: Interferon gamma in survivors of the Chernobyl power plant accident: New therapeutic option for radiation-induced fibrosis. Int J Radiat Oncol Biol Phys. 45:147–152. 1999. View Article : Google Scholar : PubMed/NCBI | |
Oliva D, Nilsson M, Strandéus M, Andersson BÅ, Sharp L, Laytragoon-Lewin N and Lewin F: Individual genetic variation might predict acute skin reactions in women undergoing adjuvant breast cancer radiotherapy. Anticancer Res. 38:6763–6770. 2018. View Article : Google Scholar : PubMed/NCBI | |
Takeda I, Kizu Y, Yoshitaka O, Saito I and Yamane GY: Possible role of nitric oxide in radiation-induced salivary gland dysfunction. Radiat Res. 159:465–470. 2003. View Article : Google Scholar : PubMed/NCBI | |
Moura JF, Mota JM, Leite CA, Wong DV, Bezerra NP, Brito GA, Lima V, Cunha FQ and Ribeiro RA: A novel model of megavoltage radiation-induced oral mucositis in hamsters: Role of inflammatory cytokines and nitric oxide. Int J Radiat Biol. 91:500–509. 2015. View Article : Google Scholar : PubMed/NCBI | |
Chung YL, Lee MY and Pui NN: Epigenetic therapy using the histone deacetylase inhibitor for increasing therapeutic gain in oral cancer: Prevention of radiation-induced oral mucositis and inhibition of chemical-induced oral carcinogenesis. Carcinogenesis. 30:1387–1397. 2009. View Article : Google Scholar : PubMed/NCBI | |
Epperly MW, Gretton JA, DeFilippi SJ, Greenberger JS, Sikora CA, Liggitt D and Koe G: Modulation of radiation-induced cytokine elevation associated with esophagitis and esophageal stricture by manganese superoxide dismutase-plasmid/liposome (SOD2-PL) gene therapy. Radiat Res. 155:2–14. 2001. View Article : Google Scholar | |
Moreb J and Zucali JR: The therapeutic potential of interleukin-1 and tumor necrosis factor on hematopoietic stem cells. Leuk Lymphoma. 8:267–275. 1992. View Article : Google Scholar : PubMed/NCBI | |
Boniver J, Humblet C, Rongy AM, Delvenne C, Delvenne P, Greimers R, Thiry A, Courtoy R and Defresne MP: Cellular aspects of the pathogenesis of radiation-induced thymic lymphomas in C57 BL mice (review). In Vivo. 4:41–43. 1990.PubMed/NCBI |