Relationship between radioadaptive response and individual radiosensitivity to low doses of gamma radiation: an extended study of chromosome damage in blood lymphocytes of three donors

References

• Al-Fageeh MB, Marchant RJ, Carden MJ, Smales CM. 2005. The cold-shock response in cultured mammalian cells: harnessing the response for the improvement of recombinant protein production. Biotechnol Bioeng. 93:829–835.
   Web of Science ®Google Scholar
• Atkuri KR, Herzenberg LA, Niemi AK, Cowan T, Herzenberg LA. 2007. Importance of culturing primary lymphocytes at physiological oxygen levels. Proc Natl Acad Sci USA. 104:4547–4552.
   PubMed Web of Science ®Google Scholar
• Azzam EI, Jay-Gerin JP, Pain D. 2012. Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury. Cancer Lett. 327:48–60.
   PubMed Web of Science ®Google Scholar
• Babini G, Morini J, Baiocco G, Mariotti L, Ottolenghi A. 2015. In vitro γ-ray-induced inflammatory response is dominated by culturing conditions rather than radiation exposures. Sci Rep. 5:9343.
   PubMed Web of Science ®Google Scholar
• Barry SP, Townsend PA, Knight RA, Scarabelli TM, Latchman DS, Stephanou A. 2010. STAT3 modulates the DNA damage response pathway. Int J Exp Pathol. 91:506–514.
   PubMed Web of Science ®Google Scholar
• Bosi A, Olivieri G. 1989. Variability of the adaptive response to ionizing radiations in humans. Mutat Res. 211:13–17.
   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
• Carloni M, Meschini R, Ovidi L, Palitti F. 2001. PHA-induced cell proliferation rescues human peripheral blood lymphocytes from X-ray-induced apoptosis. Mutagenesis. 16:115–120.
   PubMed Web of Science ®Google Scholar
• Chen Y, Li Y, Zhang H, Xie Y, Chen X, Ren J, Zhang X, Zhu Z, Liu H, Zhang Y. 2010. Early effects of low dos C ion or X-ray irradiation on human peripheral blood lymphocytes . Adv Space Res. 45:832–838.
   PubMed Web of Science ®Google Scholar
• Cregan SP, Brown DL, Mitchel RE. 1999. Apoptosis and the adaptive response in human lymphocytes. Int J Radiat Biol. 75:1087–1094.
   PubMed Web of Science ®Google Scholar
• Di Maggio FM, Minafra L, Forte GI, Cammarata FP, Lio D, Messa C, Gilardi MC, Bravatà V. 2015. Portrait of inflammatory response to ionizing radiation treatment. J Inflamm (Lond). 12:14.
   PubMed Web of Science ®Google Scholar
• El-Saghire H, Michaux A, Thierens H, Baatout S. 2013. Low doses of ionizing radiation induce immune-stimulatory responses in isolated human primary monocytes. Int J Mol Med. 32:1407–1414.
   PubMed Web of Science ®Google Scholar
• El-Saghire H, Thierens H, Monsieurs P, Michaux A, Vandevoorde C, Baatout S. 2013. Gene set enrichment analysis highlights different gene expression profiles in whole blood samples X-rradiated with low and high doses. Int J Radiat Biol. 89:628–638.
   PubMed Web of Science ®Google Scholar
• Elston R, Inman GJ. 2012. Crosstalk between p53 and TGF-β Signalling. J Signal Transduct. 2012:294097.
   PubMedGoogle Scholar
• Fan J, Nishanian P, Breen EC, McDonald M, Fahey JL. 1998. Cytokine gene expression in normal human lymphocytes in response to stimulation. Clin Diagn Lab Immunol. 5:335–340.
   PubMedGoogle Scholar
• Frati DL, Bunge MM, Durand JL, Gillette V. 2002. Radio-adaptive response in human lymphocytes. Radiobiologia. 2:38–43.
   Google Scholar
• Galdiero M, Cipollaro de l’Ero G, Folgore A, Cappello M, Giobbe A, Sasso FS. 1994. Effects of irradiation doses on alterations in cytokine release by monocytes and lymphocytes. J Med. 25:23–40.
   PubMedGoogle Scholar
• Geraskin SA, Sevankaev AV. 1996. [The cytogenetic effects of low doses: the results of N. V. Luchnik and the current status of the problem]. Radiats Biol Radioecol. 36:860–864.
   PubMedGoogle Scholar
• Geva-Zatorsky N, Rosenfeld N, Itzkovitz S, Milo R, Sigal A, Dekel E, Yarnitzky T, Liron Y, Polak P, Lahav G, et al. 2006. Oscillations and variability in the p53 system. Mol Syst Biol. 2:0033.
   PubMed Web of Science ®Google Scholar
• Hain J, Jaussi R, Burkart W. 1992. Lack of adaptive response to low doses of ionizing radiation in human lymphocytes from five different donors. Mutat Res. 283:137–144.
   PubMedGoogle Scholar
• Han Q, Bagheri N, Bradshaw EM, Hafler DA, Lauffenburger DA, Love JC. 2012. Polyfunctional responses by human T cells result from sequential release of cytokines. Proc Natl Acad Sci USA. 109:1607–1612.
   PubMed Web of Science ®Google Scholar
• Han Q, Bradshaw EM, Nilsson B, Hafler DA, Love JC. 2011. Multidimensional analysis of the frequencies and rates of cytokine secretion from single cells by quantitative microengraving. Lab Chip. 10:1391–1400.
   Web of Science ®Google Scholar
• Hao N, O’Shea EK. 2012. Signal-dependent dynamics of transcription factor translocation controls gene expression. Nat Struct Mol Biol. 19:31–40.
   Web of Science ®Google Scholar
• Kalina I, Némethová G. 1997. Variability of the adaptive response to low dose radiation in peripheral blood lymphocytes of twins and unrelated donors. Folia Biol (Praha). 43:91–95.
   PubMed Web of Science ®Google Scholar
• Katial RK, Sachanandani D, Pinney C, Lieberman MM. 1998. Cytokine production in cell culture by peripheral blood mononuclear cells from immunocompetent hosts. Clin Diagn Lab Immunol. 5:78–81.
   PubMedGoogle Scholar
• Khandogina EK, Mutovin GR, Zvereva SV, Antipov AV, Zverev DO, Akifyev AP. 1991. Adaptive response in irradiated human lymphocytes: radiobiological and genetical aspects. Mutat Res. 51:181–186.
   Google Scholar
• Krieger JA, Landsiedel JC, Lawrence DA. 1996. Differential in vitro effects of physiological and atmospheric oxygen tension on normal human peripheral blood mononuclear cell proliferation, cytokine and immunoglobulin production. Int J Immunopharmacol. 18:545–552.
   PubMed Web of Science ®Google Scholar
• Laiakis EC, Baulch JE, Morgan WF. 2007. Cytokine and chemokine responses after exposure to ionizing radiation: implications for the astronauts. Adv Space Res. 39:1019–1025.
   Web of Science ®Google Scholar
• Lefrançois D, al Achkar W, Aurias A, Couturier J, Dutrillaux AM, Dutrillaux B, Flüry-Herard A, Gerbault-Seureau M, Hoffschir F, Lamoliatte E. 1989. Chromosomal aberrations induced by low-dose gamma-irradiation. Study of R-banded chromosomes of human lymphocytes . Mutat Res. 212:167–172.
   PubMedGoogle Scholar
• Levine JH, Lin Y, Elowitz MB. 2013. Functional roles of pulsing in genetic circuits. Science. 6163:1193–1200.
   Google Scholar
• Li HH, Wang YW, Chen R, Zhou B, Jonathan D, Ashwell JD, Albert J, Fornace AJ Jr. 2015. Ionizing radiation impairs T cell activation by affecting metabolic reprogramming. Int J Biol Sci. 11:726–736.
   PubMed Web of Science ®Google Scholar
• Li Y, Wong KK, Matsueda S, Efferson CL, Chang DZ, Ioannides CG, Tsuda N. 2006. Mitogen stimulation activates different signaling pathways in early- and late-divided T cells as revealed by cDNA microarray analysis. Int J Mol Med. 18:1127–1139.
   PubMed Web of Science ®Google Scholar
• Lin Z, Fillmore GC, Um TH, Elenitoba-Johnson KS, Lim MS. 2003. Comparative microarray analysis of gene expression during activation of human peripheral blood T cells and leukemic Jurkat T cells. Lab Invest. 83:765–776.
   PubMedGoogle Scholar
• Lloyd DC, Edwards AA, Leonard A, Deknudt GL, Verschaeve L, Natarajan AT, Darroudi F, Obe G, Palitti F, Tanzarella C, et al. 1992. Chromosomal aberrations in human lymphocytes induced in vitro by very low doses of X-rays. Int J Radiat Biol. 61:335–343.
   PubMed Web of Science ®Google Scholar
• Loewer A, Karanam K, Mock C, Lahav G. 2013. The p53 response in single cells is linearly correlated to the number of DNA breaks without a distinct threshold. BMC Biol. 11:114.
   PubMed Web of Science ®Google Scholar
• Mayringer I, Reindl M, Berger T. 2000. A critical comparison of frequently used methods for the analysis of tumor necrosis factor-alpha expression by human immune cells. J Immunol Methods. 235:33–40.
   PubMed Web of Science ®Google Scholar
• Menendez D, Shatz M, Azzam K, Garantziotis S, Fessler MB, Resnick MA. 2011. The Toll-like receptor gene family is integrated into human DNA damage and p53 networks. PloS Genet. 7:e1001360.
   PubMed Web of Science ®Google Scholar
• Mikkelsen RB, Wardman P. 2003. Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms. Oncogene. 22:5734–5754.
   PubMed Web of Science ®Google Scholar
• Mitchel RE. 2010. The dose window for radiation-induced protective adaptive responses. Dose Response. 8:192–208.
   Web of Science ®Google Scholar
• Naik E, Dixit VM. 2011. Mitochondrial reactive oxygen species drive proinflammatory cytokine production. J Exp Med. 208:417–420.
   PubMed Web of Science ®Google Scholar
• Nakad R, Schumacher B. 2016. DNA damage response and immune defense: links and mechanisms. Front Genet. 7:147.
   PubMed Web of Science ®Google Scholar
• Nasonova EA, Shmakova NL, Komova OV, Mel’nikova LA, Fadeeva TA, Krasavin EA, Ritter S. 2006. Cytogenetic effects of low-dose radiation with different LET in human peripheral blood lymphocytes. Radiat Environ Biophys. 45:307–312.
   PubMed Web of Science ®Google Scholar
• Nelson DE, Ihekwaba AE, Elliott M, Johnson JR, Gibney CA, Foreman BE, Nelson G, See V, Horton CA, Spiller DG, et al. 2004. Oscillations in NF-kappaB signaling control the dynamics of gene expression. Science. 306:704–708.
   PubMed Web of Science ®Google Scholar
• Olivieri G, Bosi A. 1990. Possible causes of variability of the adaptive response in human lymphocytes. In: Natarajan AT, Obe G, editors. Chromosome aberrations. Berlin: Springer; p. 130–140.
   Google Scholar
• Pavlović D, Đorđević V, Kocić G. 2002. A “cross-talk” between oxidative stress and redox cell signaling. FU Med Biol. 9:131–137.
   Google Scholar
• Pelevina II, Aleshchenko AA, Antoshchina MM, Riabchenko NI, Semenova LP, Serebrianyi AM. 2007. [An individual variability of the adaptive response to irradiation in human cells. Approach to its determination]. Radiats Biol Radioecol. 47:658–666.
   PubMedGoogle Scholar
• Polonsky M, Zaretsky I, Friedman N. 2013. Dynamic single-cell measurements of gene expression in primary lymphocytes: challenges, tools and prospects. Brief Funct Genomics. 12:99–108.
   PubMed Web of Science ®Google Scholar
• Purvis JE, Karhohs KW, Mock C, Batchelor E, Loewer A, Lahav G. 2012. p53 dynamics control cell fate. Science. 336:1440–1444.
   PubMed Web of Science ®Google Scholar
• Rabender CS, Alam A, Mikkelsen RB. 2014. Ionizing radiation induced nitric oxide signaling. Austin J Nucl Med Radiother. 1:5.
   Google Scholar
• Rand U, Rinas M, Schwerk J, Nöhren G, Linnes M, Kröger A, Flossdorf M, Kály-Kullai K, Hauser H, Höfer T, et al. 2012. Multi-layered stochasticity and paracrine signal propagation shape the type-I interferon response. Mol Syst Biol. 8:584.
   PubMed Web of Science ®Google Scholar
• Reuter S, Gupta SC, Chaturvedi MM, Aggarval BB. 2010. Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med. 49:1603–1616.
   PubMed Web of Science ®Google Scholar
• Ryabchenko NI, Antoshchina MM, Fesenko EV, Ivanova TI, Kondrashva TV, Nasonova VA. 1998. Cytogenetic adaptive response in cultured human lymphocytes: dependence on the time of exposure to adapting and challenging of X-rays. Mutat Res. 418:7–19.
   PubMed Web of Science ®Google Scholar
• Ryu H, Chung M, Dobrzyński M, Fey D, Blum Y, Lee SS, Peter M, Kholodenko BN, Jeon NL, Pertz O. 2015. Frequency modulation of ERK activation dynamics rewires cell fate. Mol Syst Biol. 11:838.
   PubMed Web of Science ®Google Scholar
• Sankaranarayanan K, von DA, Loos MJ, Natarajan AT. 1989. Adaptive response of human lymphocytes to low-level radiation from radioisotopes or X-rays. Mutat Res. 211:7–12.
   PubMed Web of Science ®Google Scholar
• Schaue D, Kachikwu EL, McBride WH. 2012. Cytokines in radiobiological responses: a review. Radiat Res. 178:505–523.
   PubMed Web of Science ®Google Scholar
• Selvan GT, Bhavani M, Vijayalakshmi J, Paul Solomon FD, Chaudhury NK, Venkatachalam P. 2014. Delayed mitogenic stimulation decreases DNA damage assessed by micronucleus assay in human peripheral blood lymphocytes after 60Co irradiation. Dose Response. 12:498–508.
   PubMed Web of Science ®Google Scholar
• Sevankaev AV, Khvostunov IK, Potetnia VI. 2012. [The low dose and low dose rate cytogenetic effects induced by gamma-radiation in human blood lymphocytes in vitro. II. The results of cytogenetic study]. Radiats Biol Radioecol. 52:11–24.
   PubMedGoogle Scholar
• Shankaran H, Chrisler WB, Sontag RL, Weber TJ. 2011. Inhibition of ERK oscillations by ionizing radiation and reactive oxygen species. Mol Carcinog. 50:424–432.
   PubMed Web of Science ®Google Scholar
• Shankaran H, Ippolito DL, Chrisler WB, Resat H, Bollinge N, Opresko LK, Wiley HS. 2009. Rapid and sustained nuclear-cytoplasmic ERK oscillations induced by epidermal growth factor. Mol Syst Biol. 5:332.
   PubMed Web of Science ®Google Scholar
• Shvartsman SY, Hagan MP, Yacoub A, Dent P, Wiley HS, Lauffenburger DA. 2002. Autocrine loops with positive feedback enable context-dependent cell signaling. Am J Physiol Cell Physiol. 282:C545–C559.
   PubMed Web of Science ®Google Scholar
• Slonina D, Biesaga B, Urbanski K, Kojs Z. 2006. Low-dose radiation response of primary keratinocytes and fibroblasts from patients with cervix cancer. Radiat Res. 167:251–259.
   Web of Science ®Google Scholar
• Spary LK, Al-Taei S, Salimu J, Cook AD, Ager A, Watson HA, Clayton A, Staffurth J, Mason MD, Tabi Z. 2014. Enhancement of T cell responses as a result of synergy between lower doses of radiation and T cell stimulation. J Immunol. 192:3101–3110.
   PubMed Web of Science ®Google Scholar
• Tapio S, Jacob V. 2007. Radioadaptive response revisited. Radiat Environ Biophys. 46:1–12.
   PubMed Web of Science ®Google Scholar
• Tay S, Hughey JJ, Lee TK, Lipniacki T, Quake SR, Covert MW. 2010. Single-cell NF-kappaB dynamics reveal digital activation and analogue information processing. Nature. 466:267–271.
   PubMed Web of Science ®Google Scholar
• Tomida T, Takekawa M, Saito H. 2015. Oscillation of p38 activity controls efficient pro-inflammatory gene expression. Nat Commun. 6:8350.
   PubMed Web of Science ®Google Scholar
• Vijayalaxmi Lial 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. 384:45–50.
   Google Scholar
• Wang J, Tham D, Wei W, Shin YS, Ma C, Ahmad H, Shi Q, Yu J, Levine RD, Heath JR. 2012. Quantitating cell-cell interaction functions with applications to glioblastoma multiforme cancer cells. Nano Lett. 12:6101–6106.
   PubMed Web of Science ®Google Scholar
• Wang P, Guo F, Han L, Wang X, Li J, Guo Y, Lü Y. 2014. X-ray-induced changes in the expression of inflammation-related genes in human peripheral blood. Int J Mol Sci. 15:19516–19534.
   PubMed Web of Science ®Google Scholar
• Wang T, Zhang X, Li JJ. 2002. The role of NF-kappaB in the regulation of cell stress responses. Int Immunopharmacol. 2:1509–1520.
   PubMed Web of Science ®Google Scholar
• Waters KM, Cummings BS, Shankaran H, Scholpa NE, Weber TJ. 2014. ERK oscillation-dependent gene expression patterns and deregulation by stress response. Chem Res Toxicol. 27:1496–1503.
   PubMed Web of Science ®Google Scholar
• Wojcik A, Streffer C. 1995. Application of a multiple fixation regimen to study the adaptive response to ionizing radiation in lymphocytes of two human donors. Mutat Res. 326:109–116.
   PubMed Web of Science ®Google Scholar
• Xue Q, Lu Y, Eisele MR, Sulistijo ES, Khan N, Fan R, Miller-Jensen K. 2015. Analysis of single-cell cytokine secretion reveals a role for paracrine signaling in coordinating macrophage responses to TLR4 stimulation. Sci Signal. 8:ra59.
   PubMed Web of Science ®Google Scholar
• Youk H, Lim WA. 2014. Secreting and sensing the same molecule allows cells to achieve versatile social behaviors. Science. 343:1242782.
   PubMed Web of Science ®Google Scholar
• Yu H. 2012. Typical cell signaling response to ionizing radiation: DNA damage and extranuclear damage. Chin J Cancer Res. 24:83–89.
   PubMed Web of Science ®Google Scholar
• Zaichkina SI, Rozanova OM, Aptikaeva GF, Achmadieva AC, Klokov DY. 2004. Low doses of gamma-radiation induce nonlinear dose responses in mammalian and plant cells. Nonlinearity Biol Toxicol Med. 2:213–221.
   PubMedGoogle Scholar
• Zhan M, Han ZC. 2004. Phosphatidylinositide 3-kinase/AKT in radiation responses. Histol Histopathol. 19:915–923.
   PubMed Web of Science ®Google Scholar
• Zhang J, Wang X, Vikash V, Ye Q, Wu D, Liu Y, Dong W. 2016. ROS and ROS-mediated cellular signaling. Oxid Med Cell Longev. 2016:4350965.
   PubMed Web of Science ®Google Scholar
• Zhang K, Han J, Groesser T, Fontenay G, Parvin B. 2012. Inference of causal networks from time-varying transcriptome data via sparse coding. PLoS One. 7:e42306.
   PubMed Web of Science ®Google Scholar