Involvement of MAPK signalling in radioadaptive response in BALB/c mice exposed to low dose ionizing radiation

References

• Ahmed KM, Nantajit D, Fan M, Murley JS, Grdina DJ, Li JJ. 2009. Coactivation of ATM/ERK/NF-kappaB in the low-dose radiation-induced radioadaptive response in human skin keratinocytes. Free Radic Biol Med. 46:1543–1550.
   PubMed Web of Science ®Google Scholar
• Alexandrou AT, Li JJ. 2014. Cell cycle regulators guide mitochondrial activity in radiation-induced adaptive response. Antioxid Redox Signal. 20:1463–1480.
   PubMed Web of Science ®Google Scholar
• Amorino GP, Hamilton VK, Valerie K, Dent P, Lammering G, Schmidt-Ullrich RK. 2002. Epidermal growth factor receptor dependence of radiation-induced transcription factor activation in human breast carcinoma cells. Mol Biol Cell. 13:2233–2244.
   PubMed Web of Science ®Google Scholar
• Azzam EI, Raaphorst GP, Mitchel RE. 1994. Radiation-induced adaptive response for protection against micronucleus formation and neoplastic transformation in C3H 10T1/2 mouse embryo cells. Radiat Res. 138:S28–31.
   PubMed Web of Science ®Google Scholar
• Barquinero JF, Barrios L, Caballín MR, Miró R, Ribas M, Subias A, Egozcue J. 1995. Occupational exposure to radiation induces an adaptive response in human lymphocytes. Int J Radiat Biol. 67:187–191.
   PubMed Web of Science ®Google Scholar
• Blimkie MS, Fung LC, Petoukhov ES, Girard C, Klokov D. 2014. Repair of DNA double-strand breaks is not modulated by low-dose gamma radiation in C57BL/6J mice. Radiat Res. 181:548–559.
   PubMed Web of Science ®Google Scholar
• Borges O, Borchard G, de Sousa A, Junginger HE, Cordeiro-da-Silva A. 2007. Induction of lymphocytes activated marker CD69 following exposure to chitosan and alginate biopolymers. Int J Pharm. 337:254–264.
   PubMed Web of Science ®Google Scholar
• Bowers G, Reardon D, Hewitt T, Dent P, Mikkelsen RB, Valerie K, Lammering G, Amir C, Schmidt-Ullrich RK. 2001. The relative role of ErbB1-4 receptor tyrosine kinases in radiation signal transduction responses of human carcinoma cells. Oncogene. 20:1388–1397.
   PubMed Web of Science ®Google Scholar
• Bravard A, Luccioni C, Moustacchi E, Rigaud O. 1999. Contribution of antioxidant enzymes to the adaptive response to ionizing radiation of human lymphoblasts. Int J Radiat Biol. 75:639–645.
   PubMed Web of Science ®Google Scholar
• Cai L, Liu SZ. 1990. Induction of cytogenetic adaptive response of somatic and germ cells in vivo and in vitro by low-dose X-irradiation. Int J Radiat Biol. 58:187–194.
   PubMed Web of Science ®Google Scholar
• Candas D, Fan M, Nantajit D, Vaughan AT, Murley JS, Woloschak GE, Grdina DJ, Li JJ. 2013. CyclinB1/Cdk1 phosphorylates mitochondrial antioxidant MnSOD in cell adaptive response to radiation stress. J Mol Cell Biol. 5:166–175.
   PubMed Web of Science ®Google Scholar
• Canney PA, Dean S. 1990. Transforming growth factor beta: A promotor of late connective tissue injury following radiotherapy? Br J Radiol. 63:620–623.
   PubMed Web of Science ®Google Scholar
• Carr EL, Kelman A, Wu GS, Gopaul R, Senkevitch E, Aghvanyan A, Turay AM, Frauwirth KA. 2010. Glutamine uptake and metabolism are coordinately regulated by ERK/MAPK during T lymphocyte activation. J Immunol. 185:1037–1044.
   PubMed Web of Science ®Google Scholar
• Carter S, Auer KL, Reardon DB, Birrer M, Fisher PB, Valerie K, Schmidt-Ullrich RK, Mikkelsen R, Dent P. 1998. Inhibition of the mitogen activated protein (MAP) kinase cascade potentiates cell killing by low dose ionizing radiation in A431 human squamous carcinoma cells. Oncogene. 16:2787–2796.
   PubMed Web of Science ®Google Scholar
• Cheda A, Wrembel-Wargocka J, Lisiak E, Nowosielska EM, Marciniak M, Janiak MK. 2004. 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.
   PubMed Web of Science ®Google Scholar
• Chen D, Wei L. 1991. Chromosome aberration, cancer mortality and hormetic phenomena among inhabitants in areas of high background radiation in China. J Radiat Res. 32(Suppl. 2):46–53.
   PubMed Web of Science ®Google Scholar
• Chen JC, Davis BH, Leon MA, Leong LC. 1997. Gamma radiation induces CD69 expression on lymphocytes. Cytometry. 30:304–312.
   PubMedGoogle Scholar
• Coleman MA, Yin E, Peterson LE, Nelson D, Sorensen K, Tucker JD, Wyrobek AJ. 2005. Low-dose irradiation alters the transcript profiles of human lymphoblastoid cells including genes associated with cytogenetic radioadaptive response. Radiat Res. 164:369–382.
   PubMed Web of Science ®Google Scholar
• D’Souza WN, Chang CF, Fischer AM, Li M, Hedrick SM. 2008. The Erk2 MAPK regulates CD8 T cell proliferation and survival. J Immunol. 181:7617–7629.
   PubMed Web of Science ®Google Scholar
• Esplugues E, Sancho D, Vega-Ramos J, Martínez C, Syrbe U, Hamann A, Engel P, Sánchez-Madrid F, Lauzurica P. 2003. Enhanced antitumor immunity in mice deficient in CD69. J Exp Med. 197:1093–1106.
   PubMed Web of Science ®Google Scholar
• Gourabi H, Mozdarani H. 1998. A cytokinesis-blocked micronucleus study of the radioadaptive response of lymphocytes of individuals occupationally exposed to chronic doses of radiation. Mutagenesis. 13:475–480.
   PubMed Web of Science ®Google Scholar
• Griffith CE, Zhang W, Wange RL. 1998. ZAP-70-dependent and -independent activation of Erk in Jurkat T cells. Differences in signaling induced by H2O2 and CD3 cross-linking. J Biol Chem. 273:10771–10776.
   PubMed Web of Science ®Google Scholar
• Hamann J, Fiebig H, Strauss M. 1993. Expression cloning of the early activation antigen CD69, a type II integral membrane protein with a C-type lectin domain. J Immunol. 150:4920–4927.
   PubMed Web of Science ®Google Scholar
• Hashimoto S, Shirato H, Hosokawa M, Nishioka T, Kuramitsu Y, Matushita K, Kobayashi M, Miyasaka K. 1999. The suppression of metastases and the change in host immune response after low-dose total-body irradiation in tumor-bearing rats. Radiat Res. 151:717–724.
   PubMed Web of Science ®Google Scholar
• Ikushima T, Aritomi H, Morisita J. 1996. Radioadaptive response: Efficient repair of radiation-induced DNA damage in adapted cells. Mutat Res. 358:193–198.
   PubMed Web of Science ®Google Scholar
• Ina Y, Sakai K. 2005a. Activation of immunological network by chronic low-dose-rate irradiation in wild-type mouse strains: Analysis of immune cell populations and surface molecules. Int J Radiat Biol. 81:721–729.
   PubMed Web of Science ®Google Scholar
• Ina Y, Sakai K. 2005b. Further study of prolongation of life span associated with immunological modification by chronic low-dose-rate irradiation in MRL-lpr/lpr mice: Effects of whole-life irradiation. Radiat Res. 163:418–423.
   PubMed Web of Science ®Google Scholar
• Ina Y, Tanooka H, Yamada T, Sakai K. 2005. Suppression of thymic lymphoma induction by life-long low-dose-rate irradiation accompanied by immune activation in C57BL/6 mice. Radiat Res. 163:153–158.
   PubMed Web of Science ®Google Scholar
• Ito M, Shibamoto Y, Ayakawa S, Tomita N, Sugie C, Ogino H. 2007. Low-dose whole-body irradiation induced radioadaptive response in C57BL/6 mice. J Radiat Res. 48:455–460.
   PubMed Web of Science ®Google Scholar
• Jin C, Qin L, Shi Y, Candas D, Fan M, Lu CL, Vaughan AT, Shen R, Wu LS, Liu R, et al. 2015. CDK4-mediated MnSOD activation and mitochondrial homeostasis in radioadaptive protection. Free Radic Biol Med. 81:77–87.
   PubMed Web of Science ®Google Scholar
• Kadhim M, Salomaa S, Wright E, Hildebrandt G, Belyakov OV, Prise KM, Little MP. 2013. Non-targeted effects of ionising radiation – implications for low dose risk. Mutat Res. 752:84–98.
   PubMed Web of Science ®Google Scholar
• Kakinuma S, Yamauchi K, Amasaki Y, Nishimura M, Shimada Y. 2009. Low-dose radiation attenuates chemical mutagenesis in vivo. J Radiat Res. 50:401–405.
   PubMed Web of Science ®Google Scholar
• Kang CM, Park KP, Cho CK, Seo JS, Park WY, Lee SJ, Lee YS. 2002. Hspa4 (HSP70) is involved in the radioadaptive response: Results from mouse splenocytes. Radiat Res. 157:650–655.
   PubMed Web of Science ®Google Scholar
• Kapur S, Baylink DJ, Lau KH. 2003. Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduction pathways. Bone. 32:241–251.
   PubMed Web of Science ®Google Scholar
• Kim JM, White JM, Shaw AS, Sleckman BP. 2005. MAPK p38 alpha is dispensable for lymphocyte development and proliferation. J Immunol. 174:1239–1244.
   PubMed Web of Science ®Google Scholar
• Kim CS, Kim JM, Nam SY, Yang KH, Jeong M, Kim HS, Lim YK, Kim CS, Jin YW, Kim J. 2007. Low-dose of ionizing radiation enhances cell proliferation via transient ERK1/2 and p38 activation in normal human lung fibroblasts. J Radiat Res. 48:407–415.
   PubMed Web of Science ®Google Scholar
• Końca K, Lankoff A, Banasik A, Lisowska H, Kuszewski T, Góźdź S, Koza Z, Wojcik A. 2003. A cross-platform public domain PC image-analysis program for the comet assay. Mutat Res. 534:15–20.
   PubMed Web of Science ®Google Scholar
• Kumar PR, Seshadri M, Jaikrishan G, Das B. 2015. Effect of chronic low dose natural radiation in human peripheral blood mononuclear cells: Evaluation of DNA damage and repair using the alkaline comet assay. Mutat Res. 775:59–65.
   PubMed Web of Science ®Google Scholar
• Leach JK, Van Tuyle G, Lin PS, Schmidt-Ullrich R, Mikkelsen RB. 2001. Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res. 61:3894–3901.
   PubMed Web of Science ®Google Scholar
• Lee EK, Kim JA, Park SJ, Kim JK, Heo K, Yang KM, Son TG. 2013. Low-dose radiation activates Nrf1/2 through reactive species and the Ca(2+)/ERK1/2 signaling pathway in human skin fibroblast cells. BMB Rep. 46:258–263.
   PubMed Web of Science ®Google Scholar
• Liang X, So YH, Cui J, Ma K, Xu X, Zhao Y, Cai L, Li W. 2011. The low-dose ionizing radiation stimulates cell proliferation via activation of the MAPK/ERK pathway in rat cultured mesenchymal stem cells. J Radiat Res. 52:380–386.
   PubMed Web of Science ®Google Scholar
• Lum JB, Infante AJ, Makker DM, Yang F, Bowman BH. 1986. Transferrin synthesis by inducer T lymphocytes. J Clin Invest. 77:841–849.
   PubMed Web of Science ®Google Scholar
• Matsumoto H, Takahashi A, Ohnishi T. 2007. Nitric oxide radicals choreograph a radioadaptive response. Cancer Res. 67:8574–8579.
   PubMed Web of Science ®Google Scholar
• McCubrey JA, Steelman LS, Franklin RA, Abrams SL, Chappell WH, Wong EW, Lehmann BD, Terrian DM, Basecke J, Stivala F, et al. 2007. Targeting the RAF/MEK/ERK, PI3K/AKT and p53 pathways in hematopoietic drug resistance. Adv Enzyme Regul. 47:64–103.
   PubMedGoogle Scholar
• Mendiola-Cruz MT, Morales-Ramírez P. 1999. Damage-repair kinetics and early adaptive response induced by gamma rays in murine leukocytes in vivo. Somat Cell Mol Genet. 25:287–299.
   PubMedGoogle Scholar
• Milisav I, Poljsak B, Suput D. 2012. Adaptive response, evidence of cross-resistance and its potential clinical use. Int J Mol Sci. 13:10771–10806.
   PubMed Web of Science ®Google Scholar
• Mitchel RE, Jackson JS, Morrison DP, Carlisle SM. 2003. Low doses of radiation increase the latency of spontaneous lymphomas and spinal osteosarcomas in cancer-prone, radiation-sensitive Trp53 heterozygous mice. Radiat Res. 159:320–327.
   PubMed Web of Science ®Google Scholar
• Mohammadi S, Taghavi-Dehaghani M, Gharaati MR, Masoomi R, Ghiassi-Nejad M. 2006. Adaptive response of blood lymphocytes of inhabitants residing in high background radiation areas of Ramsar – micronuclei, apoptosis and comet assays. J Radiat Res. 47:279–285.
   PubMed Web of Science ®Google Scholar
• Mullenders L, Atkinson M, Paretzke H, Sabatier L, Bouffler S. 2009. Assessing cancer risks of low-dose radiation. Nat Rev Cancer. 9:596–604.
   PubMed Web of Science ®Google Scholar
• Okazaki R, Ootsuyama A, Norimura T. 2007. TP53 and TP53-related genes associated with protection from apoptosis in the radioadaptive response. Radiat Res. 167:51–57.
   PubMed Web of Science ®Google Scholar
• Olivieri G, Bodycote J, Wolff S. 1984. Adaptive response of human lymphocytes to low concentrations of radioactive thymidine. Science. 223:594–597.
   PubMed Web of Science ®Google Scholar
• Park SH, Lee SJ, Chung HY, Kim TH, Cho CK, Yoo SY, Lee YS. 2000. Inducible heat-shock protein 70 is involved in the radioadaptive response. Radiat Res. 153:318–326.
   PubMed Web of Science ®Google Scholar
• Phan N, De Lisio M, Parise G, Boreham DR. 2012. Biological effects and adaptive response from single and repeated computed tomography scans in reticulocytes and bone marrow of C57BL/6 mice. Radiat Res. 177:164–175.
   PubMed Web of Science ®Google Scholar
• Rincón M, Flavell RA, Davis RJ. 2001. Signal transduction by MAP kinases in T lymphocytes. Oncogene. 20:2490–2497.
   PubMed Web of Science ®Google Scholar
• Rodgers BE, Holmes KM. 2008. Radio-adaptive response to environmental exposures at Chernobyl. Dose Response. 6:209–221.
   PubMed Web of Science ®Google Scholar
• Salmerón A, Borroto A, Fresno M, Crumpton MJ, Ley SC, Alarcón B. 1995. Transferrin receptor induces tyrosine phosphorylation in T cells and is physically associated with the TCR zeta-chain. J Immunol. 154:1675–1683.
   PubMed Web of Science ®Google Scholar
• Sancho D, Gómez M, Viedma F, Esplugues E, Gordón-Alonso M, García-López MA, de la Fuente H, Martínez-AC, Lauzurica P, Sánchez-Madrid F. 2003. CD69 downregulates autoimmune reactivity through active transforming growth factor-beta production in collagen-induced arthritis. J Clin Invest. 112:872–882.
   PubMed Web of Science ®Google Scholar
• Sawant SG, Randers-Pehrson G, Metting NF, Hall EJ. 2001. Adaptive response and the bystander effect induced by radiation in C3H 10T(1/2) cells in culture. Radiat Res. 156:177–180.
   PubMed Web of Science ®Google Scholar
• Schmidt-Ullrich RK, Mikkelsen RB, Dent P, Todd DG, Valerie K, Kavanagh BD, Contessa JN, Rorrer WK, Chen PB. 1997. Radiation-induced proliferation of the human A431 squamous carcinoma cells is dependent on EGFR tyrosine phosphorylation. Oncogene. 15:1191–1197.
   PubMed Web of Science ®Google Scholar
• Shankar B, Pandey R, Sainis K. 2006. Radiation-induced bystander effects and adaptive response in murine lymphocytes. Int J Radiat Biol. 82:537–548.
   PubMed Web of Science ®Google Scholar
• Shankar B, Premachandran S, Bharambe SD, Sundaresan P, Sainis KB. 1999. Modification of immune response by low dose ionizing radiation: Role of apoptosis. Immunol Lett. 68:237–245.
   PubMed Web of Science ®Google Scholar
• Shelke S, Das B. 2015. Dose response and adaptive response of non-homologous end joining repair genes and proteins in resting human peripheral blood mononuclear cells exposed to γ radiation. Mutagenesis. 30:365–379.
   PubMed Web of Science ®Google Scholar
• Shimizu T, Kato T, Tachibana A, Sasaki MS. 1999. Coordinated regulation of radioadaptive response by protein kinase C and p38 mitogen-activated protein kinase. Exp Cell Res. 251:424–432.
   PubMed Web of Science ®Google Scholar
• Singh NP, McCoy MT, Tice RR, Schneider EL. 1988. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res. 175:184–191.
   PubMed Web of Science ®Google Scholar
• Tamemoto H, Kadowaki T, Tobe K, Ueki K, Izumi T, Chatani Y, Kohno M, Kasuga M, Yazaki Y, Akanuma Y. 1992. Biphasic activation of two mitogen-activated protein kinases during the cell cycle in mammalian cells. J Biol Chem. 267:20293–20297.
   PubMed Web of Science ®Google Scholar
• Testi R, D’Ambrosio D, De Maria R, Santoni A. 1994. The CD69 receptor: A multipurpose cell-surface trigger for hematopoietic cells. Immunol Today. 15:479–483.
   PubMedGoogle Scholar
• Thierens H, Vral A, Barbé M, Meijlaers M, Baeyens A, Ridder LD. 2002. Chromosomal radiosensitivity study of temporary nuclear workers and the support of the adaptive response induced by occupational exposure. Int J Radiat Biol. 78:1117–1126.
   PubMed Web of Science ®Google Scholar
• Toprani SM, Das B. 2015. Radio-adaptive response of base excision repair genes and proteins in human peripheral blood mononuclear cells exposed to gamma radiation. Mutagenesis. 30:663–676.
   PubMed Web of Science ®Google Scholar
• Vijayalaxmi, Leal BZ, Deahl TS, Meltz ML. 1995. Variability in adaptive response to low dose radiation in human blood lymphocytes: Consistent results from chromosome aberrations and micronuclei. Mutat Res. 348:45–50.
   PubMed Web of Science ®Google Scholar
• Wolff S, Afzal V, Jostes RF, Wiencke JK. 1993. Indications of repair of radon-induced chromosome damage in human lymphocytes: An adaptive response induced by low doses of X-rays. Environ Health Perspect. 101(Suppl. 3):73–77.
   PubMed Web of Science ®Google Scholar
• Wolff S, Afzal V, Wiencke JK, Olivieri G, Michaeli A. 1988. Human lymphocytes exposed to low doses of ionizing radiations become refractory to high doses of radiation as well as to chemical mutagens that induce double-strand breaks in DNA. Int J Radiat Biol Relat Stud Phys Chem Med. 53:39–47.
   PubMedGoogle Scholar
• Yacoub A, McKinstry R, Hinman D,Chung T, Dent P, Hagan MP. 2003. Epidermal growth factor and ionizing radiation up-regulate the DNA repair genes XRCC1 and ERCC1 in DU145 and LNCaP prostate carcinoma through MAPK signaling. Radiat Res. 159:439–452.
   PubMed Web of Science ®Google Scholar
• Yan YX, Gong YW, Guo Y, Lv Q, Guo C, Zhuang Y, Zhang Y, Li R, Zhang XZ. 2012. Mechanical strain regulates osteoblast proliferation through integrin-mediated ERK activation. PLoS One. 7:e35709.
   PubMed Web of Science ®Google Scholar
• Yonezawa M, Horie K, Kondo H, Kubo K. 2004. Increase in endogenous spleen colonies without recovery of blood cell counts in radioadaptive survival response in C57BL/6 mice. Radiat Res. 161:161–167.
   PubMed Web of Science ®Google Scholar
• Yonezawa M, Misonoh J, Hosokawa Y. 1996. Two types of X-ray-induced radioresistance in mice: Presence of 4 dose ranges with distinct biological effects. Mutat Res. 358:237–243.
   PubMed Web of Science ®Google Scholar
• Youngblom JH, Wiencke JK, Wolff S. 1989. Inhibition of the adaptive response of human lymphocytes to very low doses of ionizing radiation by the protein synthesis inhibitor cycloheximide. Mutat Res. 227:257–261.
   PubMed Web of Science ®Google Scholar
• Zielinski JM, Ashmore PJ, Band PR, Jiang H, Shilnikova NS, Tait VK, Krewski D. 2009. Low dose ionizing radiation exposure and cardiovascular disease mortality: Cohort study based on Canadian national dose registry of radiation workers. Int J Occup Med Environ Health. 22:27–33.
   PubMed Web of Science ®Google Scholar