Genomic instability induced in distant progeny of bystander cells depends on the connexins expressed in the irradiated cells

References

• Autsavapromporn N, de Toledo SM, Buonanno M, Jay-Gerin JP, Harris AL, Azzam EI. 2011a. Intercellular communication amplifies stressful effects in high-charge, high-energy (HZE) particle-irradiated human cells. JRR. 52:408–414.
   PubMed Web of Science ®Google Scholar
• Autsavapromporn N, de Toledo SM, Jay-Gerin JP, Harris AL, Azzam EI. 2013a. Human cell responses to ionizing radiation are differentially affected by the expressed connexins. J Radiat Res (Tokyo). 54:251–259.
   PubMed Web of Science ®Google Scholar
• Autsavapromporn N, de Toledo SM, Little JB, Jay-Gerin J-P, Harris AL, Azzam EI. 2011b. The role of gap junction communication and oxidative stress in the propagation of toxic effects among high-dose α-particle-irradiated human cells. Radiat Res. 175:347–357.
   PubMed Web of Science ®Google Scholar
• Autsavapromporn N, Suzuki M, Funayama T, Usami N, Plante I, Yokota Y, Mutou Y, Ikeda H, Kobayashi K, Kobayashi Y, et al. 2013b. Gap junction communication and the propagation of bystander effects induced by microbeam irradiation in human fibroblast cultures: the impact of radiation quality. Radiat Res. 180:367–375.
   PubMed Web of Science ®Google Scholar
• Ayad WA, Locke D, Koreen IV, Harris AL. 2006. Heteromeric, but not homomeric, connexin channels are selectively permeable to inositol phosphates. J Biol Chem. 281:16727–16739.
   PubMed Web of Science ®Google Scholar
• Azzam EI, de Toledo SM, Gooding T, Little JB. 1998. Intercellular communication is involved in the bystander regulation of gene expression in human cells exposed to very low fluences of alpha particles. Radiat Res. 150:497–504.
   PubMed Web of Science ®Google Scholar
• Azzam EI, De Toledo SM, Harris AL, Ivanov V, Zhou H, Amundson SA, Lieberman HB, Hei TK. 2013. The ionizing radiation-induced bystander effect: evidence, mechanism and significance. In: Pathobiology of cancer regimen-related toxicities. New York, NY: Springer; pp. 42–68.
   Google Scholar
• Azzam EI, de Toledo SM, Little JB. 2001. Direct evidence for the participation of gap-junction mediated intercellular communication in the transmission of damage signals from alpha-particle irradiated to non-irradiated cells. Proc Natl Acad Sci USA. 98:473–478.
   PubMed Web of Science ®Google Scholar
• Azzam EI, de Toledo SM, Little JB. 2003a. Expression of connexin43 is highly sensitive to ionizing radiation and environmental stresses. Cancer Res. 63:7128–7135.
   PubMed Web of Science ®Google Scholar
• Azzam EI, de Toledo SM, Little JB. 2003b. Oxidative metabolism, gap junctions and the ionizing radiation-induced bystander effect. Oncogene. 22:7050–7057.
   PubMed Web of Science ®Google Scholar
• Azzam EI, de Toledo SM, Spitz DR, Little JB. 2002. Oxidative metabolism modulates signal transduction and micronucleus formation in bystander cells from alpha-particle-irradiated normal human fibroblast cultures. Cancer Res. 62:5436–5442.
   PubMed Web of Science ®Google Scholar
• Bevans CG, Kordel M, Rhee SK, Harris AL. 1998. Isoform composition of connexin channels determines selectivity among second messengers and uncharged molecules. J Biol Chem. 273:2808–2816.
   PubMed Web of Science ®Google Scholar
• Braby LA. 1992. Microbeam studies of the sensitivity of structures within living cells. Scanning Microsc. 6:167–174. Discussion 174–175.
   PubMedGoogle Scholar
• Brisset AC, Isakson BE, Kwak BR. 2009. Connexins in vascular physiology and pathology. Antioxid Redox Signal. 11:267–282.
   PubMed Web of Science ®Google Scholar
• Brooks AL. 2015. Dr William F. Morgan 1952–2015. Int J Radiat Biol. 91:913
   PubMed Web of Science ®Google Scholar
• Bruzzone R, Meda P. 1988. The gap junction: a channel for multiple functions? Eur J Clin Invest. 18:444–453.
   PubMed Web of Science ®Google Scholar
• Buonanno M, de Toledo SM, Azzam EI. 2011a. Increased frequency of spontaneous neoplastic transformation in progeny of bystander cells from cultures exposed to densely-ionizing radiation. PLoS One. 6:e21540.
   PubMed Web of Science ®Google Scholar
• Buonanno M, De Toledo SM, Pain D, Azzam EI. 2011b. Long-term consequences of radiation-induced bystander effects depend on radiation quality and dose and correlate with oxidative stress. Radiat Res. 175:405–415.
   PubMed Web of Science ®Google Scholar
• Cadet J, Ravanat JL, TavernaPorro M, Menoni H, Angelov D. 2012. Oxidatively generated complex DNA damage: tandem and clustered lesions. Cancer Lett. 327:5–15.
   PubMed Web of Science ®Google Scholar
• Chai Y, Calaf GM, Zhou H, Ghandhi SA, Elliston CD, Wen G, Nohmi T, Amundson SA, Hei TK. 2013. Radiation induced COX-2 expression and mutagenesis at non-targeted lung tissues of gpt delta transgenic mice. Br J Cancer. 108:91–98.
   PubMed Web of Science ®Google Scholar
• Charlton DE, Sephton R. 1991. A relationship between microdosimetric spectra and cell survival for high-LET irradiation. Int J Radiat Biol. 59:447–457.
   PubMed Web of Science ®Google Scholar
• Coates PJ, Lorimore SA, Wright EG. 2004. Damaging and protective cell signalling in the untargeted effects of ionizing radiation. Mutat Res. 568:5–20.
   PubMed Web of Science ®Google Scholar
• Cronier L, Crespin S, Strale PO, Defamie N, Mesnil M. 2009. Gap junctions and cancer: new functions for an old story. Antioxid Redox Signal. 11:323–338.
   PubMed Web of Science ®Google Scholar
• Cucinotta F, Nikjoo H, Goodhead DT. 1998. The effect of delta rays on the number of particle traversals per cell in laboratory and space exposures. Radiat Res. 150:115–119.
   PubMed Web of Science ®Google Scholar
• Davidson JS, Baumgarten IM, Harley EH. 1986. Reversible inhibition of intercellular junctional communication by glycyrrhetinic acid. Biochem Biophys Res Commun. 134:29–36.
   PubMed Web of Science ®Google Scholar
• Desai S, Kobayashi A, Konishi T, Oikawa M, Pandey BN. 2014. Damaging and protective bystander cross-talk between human lung cancer and normal cells after proton microbeam irradiation. Mutat Res. 763–764:39–44.
   PubMed Web of Science ®Google Scholar
• Desai S, Srambikkal N, Yadav HD, Shetake N, Balla MM, Kumar A, Ray P, Ghosh A, Pandey BN. 2016. Molecular understanding of growth inhibitory effect from irradiated to bystander tumor cells in mouse fibrosarcoma tumor model. PLoS One. 11:e0161662.
   PubMed Web of Science ®Google Scholar
• Domoguaer J, De Toledo SM, Azzam EI. 2016. A mimic of the tumor microenvironment: a simple method for generating enriched cell populations and investigating intercellular communication. J Vis Exp. 115:e54429.
   Google Scholar
• Elfgang C, Eckert R, Lichtenberg-Frate H, Butterweck A, Traub O, Klein RA, Hulser DF, Willecke K. 1995. Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. J Cell Biol. 129:805–817.
   PubMed Web of Science ®Google Scholar
• Elmore E, Lao XY, Kapadia R, Redpath JL. 2009. Threshold-type dose response for induction of neoplastic transformation by 1 GeV/nucleon iron ions. Radiat Res. 171:764–770.
   PubMed Web of Science ®Google Scholar
• Elsayed W, Harris AL. 2004. Selective permeability of connexin channels among inositol phosphates. Biophys J. 86:583a.
   Web of Science ®Google Scholar
• Elsayed WA, Koreen IV, Liu YL, Harris AL. 2004. Inositol phosphates are selectively permeable through heteromeric connexin channels. Mol Biol Cell. 15:183a.
   Web of Science ®Google Scholar
• Fenech M, Morley AA. 1985. Measurement of micronuclei in lymphocytes. Mutat Res. 147:29–36.
   PubMed Web of Science ®Google Scholar
• Gaillard S, Pusset D, de Toledo SM, Fromm M, Azzam EI. 2009. Propagation distance of the alpha-particle-induced bystander effect: the role of nuclear traversal and gap junction communication. Radiat Res. 171:513–520.
   PubMed Web of Science ®Google Scholar
• Gerashchenko BI, Howell RW. 2003. Flow cytometry as a strategy to study radiation-induced bystander effects in co-culture systems. Cytometry A. 54:1–7.
   PubMed Web of Science ®Google Scholar
• Gonon G, Groetz JE, de Toledo SM, Howell RW, Fromm M, Azzam EI. 2013. Non-targeted stressful effects in normal human fibroblast cultures exposed to low fluences of high charge, High Energy (HZE) particles: kinetics of biologic responses and significance of secondary radiations. Radiat Res. 179:444–457.
   PubMed Web of Science ®Google Scholar
• Gray LH, Conger AD, Ebert M, Hornsey S, Scott OC. 1953. The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy. BJR. 26:638–648.
   PubMed Web of Science ®Google Scholar
• Hamada N, Hei TK, Bouffler S, Woloschak GE. 2016. William F. Morgan (1952–2015). Mutat Res. 770:387–388.
   Web of Science ®Google Scholar
• Hamada N, Matsumoto H, Hara T, Kobayashi Y. 2007. Intercellular and intracellular signaling pathways mediating ionizing radiation-induced bystander effects. JRR. 48:87–95.
   PubMed Web of Science ®Google Scholar
• Harris AL. 2001. Emerging issues of connexin channels: biophysics fills the gap. Q Rev Biophys. 34:325–472.
   PubMed Web of Science ®Google Scholar
• Harris AL. 2007. Connexin channel permeability to cytoplasmic molecules. Prog Biophys Mol Biol. 94:120–143.
   PubMed Web of Science ®Google Scholar
• Harris AL, Contreras JE. 2014. Motifs in the permeation pathway of connexin channels mediate voltage and Ca (2+) sensing. Front Physiol. 5:113.
   PubMed Web of Science ®Google Scholar
• Hei TK, Wu LJ, Liu SX, Vannais D, Waldren CA, Randers-Pehrson G. 1997. Mutagenic effects of a single and an exact number of alpha particles in mammalian cells. Proc Natl Acad Sci USA. 94:3765–3770.
   PubMed Web of Science ®Google Scholar
• Hei TK, Zhou H, Chai Y, Ponnaiya B, Ivanov VN. 2011. Radiation induced non-targeted response: mechanism and potential clinical implications. Curr Mol Pharmacol. 4: 96–105.
   PubMedGoogle Scholar
• Held KD. 2009. Effects of low fluences of radiations found in space on cellular systems. Int J Radiat Biol. 85:379–390.
   PubMed Web of Science ®Google Scholar
• Hong X, Sin WC, Harris AL, Naus CC. 2015. Gap junctions modulate glioma invasion by direct transfer of microRNA. Oncotarget. 6:15566–15577.
   PubMed Web of Science ®Google Scholar
• International Commission on Radiation Units and Measurements (ICRU). 1993. Stopping powers and ranges for protons and alpha particles. (Report 49).
   Google Scholar
• Jain MR, Li M, Chen W, Liu T, De Toledo SM, Pandey BN, Li H, Rabin BM, Azzam EI. 2011. In vivo space radiation-induced non-targeted responses: late effects on molecular signaling in mitochondria. CMP. 4:106–114.
   Google Scholar
• John SA, Kondo R, Wang SY, Goldhaber JI, Weiss JN. 1999. Connexin-43 hemichannels opened by metabolic inhibition. J Biol Chem. Jan 1274:236–240.
   PubMed Web of Science ®Google Scholar
• Kadhim MA, Macdonald DA, Goodhead DT, Lorimore SA, Marsden SJ, Wright EG. 1992. Transmission of chromosomal instability after plutonium α-particle irradiation [see comments]. Nature 355:738–740.
   PubMed Web of Science ®Google Scholar
• Koreen IV, Elsayed WA, Liu YJ, Harris AL. 2004. Tetracycline-regulated expression enables purification and functional analysis of recombinant connexin channels from mammalian cells. Biochem J. 383:111–119.
   PubMed Web of Science ®Google Scholar
• Lehnert BE, Goodwin EH. 1997. Extracellular factor(s) following exposure to alpha particles can cause sister chromatid exchanges in normal human cells. Cancer Res. 57:2164–2171.
   PubMed Web of Science ®Google Scholar
• Li M, Gonon G, Buonanno M, Autsavapromporn N, De Toledo SM, Pain D, Azzam EI. 2014. Health risks of space exploration: targeted and non-targeted oxidative injury by high charge and high energy particles. Antioxid Redox Signal. 20:1501–1523.
   PubMed Web of Science ®Google Scholar
• Lim PK, Bliss SA, Patel SA, Taborga M, Dave MA, Gregory LA, Greco SJ, Bryan M, Patel PS, Rameshwar P. 2011. Gap junction-mediated import of microRNA from bone marrow stromal cells can elicit cell cycle quiescence in breast cancer cells. Cancer Res. 71:1550–1560.
   PubMed Web of Science ®Google Scholar
• Little JB. 2003. Genomic instability and bystander effects: a historical perspective. Oncogene. 22:6978–6987.
   PubMed Web of Science ®Google Scholar
• Locke D, Stein T, Davies C, Morris J, Harris AL, Evans WH, Monaghan P, Gusterson B. 2004. Altered permeability and modulatory character of connexin channels during mammary gland development. Exp Cell Res. 298:643–660.
   PubMed Web of Science ®Google Scholar
• Lorimore SA, Chrystal JA, Robinson JI, Coates PJ, Wright EG. 2008. Chromosomal instability in unirradiated hemaopoietic cells induced by macrophages exposed in vivo to ionizing radiation. Cancer Res. 68:8122–8126.
   PubMed Web of Science ®Google Scholar
• Lorimore SA, Coates PJ, Wright EG. 2003. Radiation-induced genomic instability and bystander effects: inter-related nontargeted effects of exposure to ionizing radiation. Oncogene. 22:7058–7069.
   PubMed Web of Science ®Google Scholar
• Mancuso M, Pasquali E, Leonardi S, Tanori M, Rebessi S, Di Majo V, Pazzaglia S, Toni MP, Pimpinella M, Covelli V, et al. 2008. Oncogenic bystander radiation effects in patched heterozygous mouse cerebellum. Proc Natl Acad Sci U S A. 105:12445–12450.
   PubMed Web of Science ®Google Scholar
• Manthey D, Bukauskas F, Lee CG, Kozak CA, Willecke K. 1999. Molecular cloning and functional expression of the mouse gap junction gene connexin-57 in human HeLa cells. J Biol Chem. 274:14716–14723.
   PubMed Web of Science ®Google Scholar
• Marder BA, Morgan WF. 1993. Delayed chromosomal instability induced by DNA damage. Mol Cell Biol. 13:6667–6677.
   PubMed Web of Science ®Google Scholar
• Mehta PP, Bertram JS, Loewenstein WR. 1986. Growth inhibition of transformed cells correlates with their junctional communication with normal cells. Cell. 44:187–196.
   PubMed Web of Science ®Google Scholar
• Mesnil M, Krutovskikh V, Piccoli C, Elfgang C, Traub O, Willecke K, Yamasaki H. 1995. Negative growth control of HeLa cells by connexin genes: connexin species specificity. Cancer Res. 55:629–639.
   PubMed Web of Science ®Google Scholar
• Morgan WF. 2003a. Is there a common mechanism underlying genomic instability, bystander effects and other nontargeted effects of exposure to ionizing radiation? Oncogene 22:7094–7099.
   PubMed Web of Science ®Google Scholar
• Morgan WF. 2003b. Non-targeted and delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro. Radiat Res 159:567–580.
   PubMed Web of Science ®Google Scholar
• Morgan WF. 2003c. Non-targeted and delayed effects of exposure to ionizing radiation: II. Radiation-induced genomic instability and bystander effects in vivo, clastogenic factors and transgenerational effects. Radiat Res 159:581–596.
   PubMed Web of Science ®Google Scholar
• Morgan WF, Bair WJ. 2013. Issues in low dose radiation biology: the controversy continues. A perspective. Radiat Res. 179:501–510.
   PubMed Web of Science ®Google Scholar
• Morgan WF, Sowa MB. 2015. Non-targeted effects induced by ionizing radiation: mechanisms and potential impact on radiation induced health effects. Cancer Lett. 356:17–21.
   PubMed Web of Science ®Google Scholar
• Mothersill C, Kadhim MA, O’Reilly S, Papworth D, Marsden SJ, Seymour CB, Wright EG. 2000. Dose- and time-response relationships for lethal mutations and chromosomal instability induced by ionizing radiation in an immortalized human keratinocyte cell line. Int J Radiat Biol. 76:799–806.
   PubMed Web of Science ®Google Scholar
• Mothersill C, Seymour C. 1997. Medium from irradiated human epithelial cells but not human fibroblasts reduces the clonogenic survival of unirradiated cells. Int J Radiat Biol. 71:421–427.
   PubMed Web of Science ®Google Scholar
• Mothersill C, Seymour CB. 1998. Cell-cell contact during gamma irradiation is not required to induce a bystander effect in normal human keratinocytes: evidence for release during irradiation of a signal controlling survival into the medium. Radiat Res. 149:252–262.
   Web of Science ®Google Scholar
• Mothersill C, Seymour CB. 2004. Radiation-induced bystander effects – implications for cancer. Nat Rev Cancer. 4:158–164.
   PubMed Web of Science ®Google Scholar
• Nagasawa H, Cremesti A, Kolesnick R, Fuks Z, Little JB. 2002. Involvement of membrane signaling in the bystander effect in irradiated cells. Cancer Res. 62:2531–2534.
   PubMed Web of Science ®Google Scholar
• Nagasawa H, Little JB. 1992. Induction of sister chromatid exchanges by extremely low doses of α-particles. Cancer Res. 52:6394–6396.
   PubMed Web of Science ®Google Scholar
• Neti PV, de Toledo SM, Perumal V, Azzam EI, Howell RW. 2004. A multi-port low-fluence alpha-particle irradiator: fabrication, testing and benchmark radiobiological studies. Radiat Res. 161:732–738.
   PubMed Web of Science ®Google Scholar
• Nikjoo H, Uehara S, Khvostunov IG, Cucinotta FA, Wilson WE, Goodhead DT. 2001. Monte Carlo track structure for radiation biology and space applications. Phys Med. 17(Suppl.1):38–44.
   PubMed Web of Science ®Google Scholar
• Norbury JW, Schimmerling W, Slaba TC, Azzam EI, Badavi FF, Baiocco G, Benton E, Bindi V, Blakely EA, Blattnig SR, et al. 2016. Galactic cosmic ray simulation at the NASA Space Radiation Laboratory. Life Sci Space Res. 8:38–51.
   Google Scholar
• Ponomarev AL, Cucinotta FA. 2006. Nuclear fragmentation and the number of particle tracks in tissue. Radiat Prot Dosimetry. 122:354–361.
   PubMed Web of Science ®Google Scholar
• Prise KM, O’Sullivan JM. 2009. Radiation-induced bystander signalling in cancer therapy. Nat Rev Cancer. 9:351–360.
   PubMed Web of Science ®Google Scholar
• Raaphorst GP, Azzam EI, Borsa J, Sargent MD. 1984. Modification by anisotonic treatment of repair and fixation of radiation damage in cell killing and transformation. Br J Cancer. (Suppl.6):239–242.
   Google Scholar
• Rueckert RR, Mueller GC. 1960. Effect of oxygen tension on HeLa cell growth. Cancer Res. 20:944–949.
   PubMed Web of Science ®Google Scholar
• Saez JC, Leybaert L. 2014. Hunting for connexin hemichannels. FEBS Lett. 588:1205–1211.
   PubMed Web of Science ®Google Scholar
• Schubert AL, Schubert W, Spray DC, Lisanti MP. 2002. Connexin family members target to lipid raft domains and interact with caveolin-1. Biochemistry. 41:5754–5764.
   PubMed Web of Science ®Google Scholar
• Schwartz JL. 2016. Dr William Francis (Bill) Morgan (1952–2015). Environ Mol Mutagen. 57:416–417.
   PubMed Web of Science ®Google Scholar
• Seymour CB, Mothersill C. 2000. Relative contribution of bystander and targeted cell killing to the low-dose region of the radiation dose-response curve. Radiat Res. 153:508–511.
   PubMed Web of Science ®Google Scholar
• Shao C, Folkard M, Michael BD, Prise KM. 2004. Targeted cytoplasmic irradiation induces bystander responses. Proc Natl Acad Sci USA. 101:13495–13500.
   PubMed Web of Science ®Google Scholar
• Shao C, Furusawa Y, Aoki M, Ando K. 2003a. Role of gap junctional intercellular communication in radiation-induced bystander effects in human fibroblasts. Radiat Res. 160:318–323.
   PubMed Web of Science ®Google Scholar
• Shao C, Stewart V, Folkard M, Michael BD, Prise KM. 2003b. Nitric oxide-mediated signaling in the bystander response of individually targeted glioma cells. Cancer Res. 63:8437–8442.
   PubMed Web of Science ®Google Scholar
• Sigurdson AJ, Jones IM. 2003. Second cancers after radiotherapy: any evidence for radiation-induced genomic instability? Oncogene. 22:7018–7027.
   PubMed Web of Science ®Google Scholar
• Sowa MB, Goetz W, Baulch JE, Lewis AJ, Morgan WF. 2011. No evidence for a low linear energy transfer adaptive response in irradiated Rko cells. Radiat Prot Dosimetry. 143:311–314.
   PubMed Web of Science ®Google Scholar
• Sowa MB, Goetz W, Baulch JE, Pyles DN, Dziegielewski J, Yovino S, Snyder AR, de Toledo SM, Azzam EI, Morgan WF. 2010. Lack of evidence for low-LET radiation induced bystander response in normal human fibroblasts and colon carcinoma cells. Int J Radiat Biol. 86:102–113.
   PubMed Web of Science ®Google Scholar
• Stadtman ER. 1993. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu Rev Biochem. 62:797–821.
   PubMed Web of Science ®Google Scholar
• Terasima T, Tolmach LJ. 1961. Changes in X-ray sensitivity of HeLa cells during the division cycle. Nature. 190:1210–1211.
   PubMed Web of Science ®Google Scholar
• Voulgaridou GP, Anestopoulos I, Franco R, Panayiotidis MI, Pappa A. 2011. DNA damage induced by endogenous aldehydes: current state of knowledge. Mutat Res. 711:13–27.
   PubMed Web of Science ®Google Scholar
• Wang N, De Bock M, Decrock E, Bol M, Gadicherla A, Vinken M, Rogiers V, Bukauskas FF, Bultynck G, Leybaert L. 2013. Paracrine signaling through plasma membrane hemichannels. Biochim Biophys Acta. 1828:35–50.
   PubMed Web of Science ®Google Scholar
• Willecke K, Eiberger J, Degen J, Eckardt D, Romualdi A, Guldenagel M, Deutsch U, Sohl G. 2002. Structural and functional diversity of connexin genes in the mouse and human genome. Biol Chem. 383:725–737.
   PubMed Web of Science ®Google Scholar
• Wolff S. 1992. Failla Memorial Lecture. Is radiation all bad? The search for adaptation. Radiat Res. 131:117–123.
   PubMed Web of Science ®Google Scholar
• Zhao Y, De Toledo SM, Hu G, Hei TK, Azzam EI. 2014. Connexins and Cyclooxygenase-2 Crosstalk in the expression of radiation-induced bystander effects. Br J Cancer. 111:125–131.
   PubMed Web of Science ®Google Scholar
• Zhou H, Randers-Pehrson G, Waldren CA, Vannais D, Hall EJ, Hei TK. 2000. Induction of a bystander mutagenic effect of alpha particles in mammalian cells. Proc Natl Acad Sci USA. 97:2099–2104.
   PubMed Web of Science ®Google Scholar
• Zhou HN, Suzuki M, Randers-Pehrson R, Chen G, Trosko J, Vannais D, Waldren CA, Hall EJ, Hei TK. 2001. Radiation risk at low fluences of alpha particles may be greater than we thought. Proc Natl Acad Sci USA. 98:14410–14415.
   PubMed Web of Science ®Google Scholar