The Translationally Controlled Tumor Protein and the Cellular Response to Ionizing Radiation-Induced DNA Damage

  • Jie ZhangEmail author
  • Grace Shim
  • Sonia M. de Toledo
  • Edouard I. AzzamEmail author
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 64)


The absorption of ionizing radiation by living cells can directly disrupt atomic structures, producing chemical and biological changes. It can also act indirectly through radiolysis of water, thereby generating reactive chemical species that may damage nucleic acids, proteins, and lipids. Together, the direct and indirect effects of radiation initiate a series of biochemical and molecular signaling events that may repair the damage or culminate in permanent physiological changes or cell death. In efforts to gain insight into the mechanisms underlying these effects, we observed a prominent upregulation of the Translationally Controlled Tumor Protein (TCTP) in low dose/low dose rate 137Cs γ-irradiated cells that was associated with adaptive responses that reduced chromosomal damage to a level lower than what occurs spontaneously. Therefore, TCTP may support the survival and genomic integrity of irradiated cells through a role in the DNA damage response. Consistent with this postulate, TCTP was shown to physically interact with ATM, an early sensor of DNA damage, and to exist in a complex with γH2A.X, in agreement with its distinct localization with the foci of the DNA damage marker proteins γH2A.X, 53BP1, and P-ATM. Cells lacking TCTP failed to repair chromosomal damage induced by γ-rays. Further, TCTP was shown to interact with the DNA-binding subunits, Ku70 and Ku80, of DNA-PK, a major participant in nonhomologous end joining of DNA double strand breaks. Moreover, TCTP physically interacted with p53, and its knockdown attenuated the radiation-induced G1 delay, but prolonged the G2 delay. Here, we briefly review the biochemical events leading to DNA damage by ionizing radiation and to its sensing and repair, and highlight TCTP’s critical role in maintaining genomic integrity in response to DNA-damaging agents.



This work was supported by grant CA049062 from the National Institutes of Health, grant NNX15AD62G from the National Aeronautics and Space Administration, and the Program for Changjiang Scholars and Innovative Research Team, University of Ministry of Education, China.


  1. Abbas T, Dutta A (2009) p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer 9:400–414PubMedPubMedCentralCrossRefGoogle Scholar
  2. Ames BN (1989) Endogenous oxidative DNA damage, aging, and cancer. Free Radic Res Commun 7:121–128PubMedCrossRefGoogle Scholar
  3. Amson R, Pece S, Lespagnol A et al (2012) Reciprocal repression between P53 and TCTP. Nat Med 18:91–99CrossRefGoogle Scholar
  4. Amson R, Pece S, Marine JC et al (2013) TPT1/TCTP-regulated pathways in phenotypic reprogramming. Trends Cell Biol 23:37–46PubMedCrossRefGoogle Scholar
  5. Azzam EI (2011) Exposure to low level environmental agents: the induction of hormesis. Mutat Res 726:89–90PubMedPubMedCentralCrossRefGoogle Scholar
  6. Azzam EI, de Toledo SM, Raaphorst GP et al (1996) Low-dose ionizing radiation decreases the frequency of neoplastic transformation to a level below the spontaneous rate in C3H 10T1/2 cells. Radiat Res 146:369–373PubMedCrossRefGoogle Scholar
  7. Azzam EI, de Toledo SM, Little JB (2003) Oxidative metabolism, gap junctions and the ionizing radiation-induced bystander effect. Oncogene 22:7050–7057PubMedCrossRefGoogle Scholar
  8. Azzam EI, Jay-Gerin JP, Pain D (2012) Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury. Cancer Lett 327:48–60PubMedCrossRefGoogle Scholar
  9. Azzam EI, Colangelo NW, Domogauer JD et al (2016) Is ionizing radiation harmful at any exposure? An echo that continues to vibrate. Health Phys 110:249–251PubMedPubMedCentralCrossRefGoogle Scholar
  10. Badie S, Carlos AR, Folio C et al (2015) BRCA1 and CtIP promote alternative non-homologous end-joining at uncapped telomeres. EMBO J 34:410–424PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bakkenist CJ, Kastan MB (2004) Initiating cellular stress responses. Cell 118:9–17PubMedCrossRefGoogle Scholar
  12. Barendsen GW (1964) Impairment of the proliferative capacity of human cells in cultures by a particles of differing linear energy transfer. Int J Radiat Biol 8:453–466Google Scholar
  13. Baumstark-Khan C (1993) X-ray-induced DNA double-strand breaks as lethal lesions in diploid human fibroblasts compared to Chinese hamster ovary cells. Int J Radiat Biol 63:305–311PubMedCrossRefGoogle Scholar
  14. Bazile F, Pascal A, Arnal I et al (2009) Complex relationship between TCTP, microtubules and actin microfilaments regulates cell shape in normal and cancer cells. Carcinogenesis 30:555–565PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bohm H, Benndorf R, Gaestel M et al (1989) The growth-related protein P23 of the Ehrlich ascites tumor: translational control, cloning and primary structure. Biochem Int 19:277–286PubMedGoogle Scholar
  16. Bommer UA (2012) Several nuclear proteins involved in mitotic progression have been proposed to interact with TCTP, either regulating or being regulated by TCTP. Open Allergy J 5:19–32CrossRefGoogle Scholar
  17. Bommer UA, Thiele BJ (2004) The translationally controlled tumour protein (TCTP). Int J Biochem Cell Biol 36:379–385PubMedCrossRefGoogle Scholar
  18. Bommer UA, Heng C, Perrin A et al (2010) Roles of the translationally controlled tumour protein (TCTP) and the double-stranded RNA-dependent protein kinase, PKR, in cellular stress responses. Oncogene 29:763–773PubMedCrossRefGoogle Scholar
  19. Branzei D, Foiani M (2008) Regulation of DNA repair throughout the cell cycle. Nat Rev 9:297–308CrossRefGoogle Scholar
  20. Brioudes F, Thierry AM, Chambrier P et al (2010) Translationally controlled tumor protein is a conserved mitotic growth integrator in animals and plants. Proc Natl Acad Sci USA 107:16384–16389PubMedPubMedCentralCrossRefGoogle Scholar
  21. Burgess A, Labbe JC, Vigneron S et al (2008) Chfr interacts and colocalizes with TCTP to the mitotic spindle. Oncogene 27:5554–5566PubMedCrossRefGoogle Scholar
  22. Cadet J, Douki T, Ravanat JL (2011) Measurement of oxidatively generated base damage in cellular DNA. Mutat Res 711:3–12PubMedCrossRefGoogle Scholar
  23. Cans C, Passer BJ, Shalak V et al (2003) Translationally controlled tumor protein acts as a guanine nucleotide dissociation inhibitor on the translation elongation factor eEF1A. Proc Natl Acad Sci USA 100:13892–13897PubMedPubMedCentralCrossRefGoogle Scholar
  24. Chan TH, Chen L, Liu M et al (2012) Translationally controlled tumor protein induces mitotic defects and chromosome missegregation in hepatocellular carcinoma development. Hepatology 55:491–505PubMedCrossRefGoogle Scholar
  25. Chatterjee A, Schaefer HJ (1976) Microdosimetric structure of heavy ion tracks in tissue. Radiat Environ Biophys 13:215–227PubMedCrossRefGoogle Scholar
  26. Chen SH, Wu PS, Chou CH et al (2007a) A knockout mouse approach reveals that TCTP functions as an essential factor for cell proliferation and survival in a tissue- or cell type-specific manner. Mol Biol Cell 18:2525–2532PubMedPubMedCentralCrossRefGoogle Scholar
  27. Chen Z, Zhang H, Yang H et al (2007b) The expression of AmphiTCTP, a TCTP orthologous gene in amphioxus related to the development of notochord and somites. Comp Biochem Physiol B Biochem Mol Biol 147:460–465PubMedCrossRefGoogle Scholar
  28. Chitpatima ST, Makrides S, Bandyopadhyay R et al (1988) Nucleotide sequence of a major messenger RNA for a 21 kilodalton polypeptide that is under translational control in mouse tumor cells. Nucleic Acids Res 16:2350PubMedPubMedCentralCrossRefGoogle Scholar
  29. Chou WC, Hu LY, Hsiung CN et al (2015) Initiation of the ATM-Chk2 DNA damage response through the base excision repair pathway. Carcinogenesis 36:832–840PubMedCrossRefGoogle Scholar
  30. Coutard H (1937) The results and methods of treatment of cancer by radiation. Ann Surg 106:584–598PubMedPubMedCentralCrossRefGoogle Scholar
  31. Cucchi U, Gianellini LM, De Ponti A et al (2010) Phosphorylation of TCTP as a marker for polo-like kinase-1 activity in vivo. Anticancer Res 30:4973–4985PubMedGoogle Scholar
  32. de Toledo SM, Asaad N, Venkatachalam P et al (2006) Adaptive responses to low-dose/low-dose-rate gamma rays in normal human fibroblasts: the role of growth architecture and oxidative metabolism. Radiat Res 166:849–857PubMedCrossRefGoogle Scholar
  33. Decottignies A (2013) Alternative end-joining mechanisms: a historical perspective. Front Genet 4:48PubMedPubMedCentralCrossRefGoogle Scholar
  34. Delaney G, Jacob S, Featherstone C et al (2005) The role of radiotherapy in cancer treatment: estimating optimal utilization from a review of evidence-based clinical guidelines. Cancer 104:1129–1137PubMedCrossRefGoogle Scholar
  35. Dizdaroglu M (2012) Oxidatively induced DNA damage: mechanisms, repair and disease. Cancer Lett 327:26–47PubMedCrossRefGoogle Scholar
  36. Downs JA, Jackson SP (2004) A means to a DNA end: the many roles of Ku. Nat Rev 5:367–378CrossRefGoogle Scholar
  37. Fenech M, Morley AA (1985) Measurement of micronuclei in lymphocytes. Mutat Res 147:29–36PubMedCrossRefGoogle Scholar
  38. Gachet Y, Tournier S, Lee M et al (1999) The growth-related, translationally controlled protein P23 has properties of a tubulin binding protein and associates transiently with microtubules during the cell cycle. J Cell Sci 112(Pt 8):1257–1271PubMedGoogle Scholar
  39. Georgakilas AG (2011) From chemistry of DNA damage to repair and biological significance. Comprehending the future. Mutat Res 711:1–2PubMedCrossRefGoogle Scholar
  40. Gnanasekar M, Ramaswamy K (2007) Translationally controlled tumor protein of Brugia malayi functions as an antioxidant protein. Parasitol Res 101:1533–1540PubMedPubMedCentralCrossRefGoogle Scholar
  41. Gnanasekar M, Dakshinamoorthy G, Ramaswamy K (2009) Translationally controlled tumor protein is a novel heat shock protein with chaperone-like activity. Biochem Biophys Res Commun 386:333–337PubMedPubMedCentralCrossRefGoogle Scholar
  42. Goodhead DT (1988) Spatial and temporal distribution of energy. Health Phys 55:231–240PubMedCrossRefGoogle Scholar
  43. Graidist P, Phongdara A, Fujise K (2004) Antiapoptotic protein partners fortilin and MCL1 independently protect cells from 5-fluorouracil-induced cytotoxicity. J Biol Chem 279:40868–40875PubMedCrossRefGoogle Scholar
  44. Graidist P, Yazawa M, Tonganunt M et al (2007) Fortilin binds Ca2+ and blocks Ca2+-dependent apoptosis in vivo. Biochem J 408:181–191PubMedPubMedCentralCrossRefGoogle Scholar
  45. Hacein-Bey L, Konstas AA, Pile-Spellman J (2014) Natural history, current concepts, classification, factors impacting endovascular therapy, and pathophysiology of cerebral and spinal dural arteriovenous fistulas. Clin Neurol Neurosurg 121:64–75PubMedCrossRefGoogle Scholar
  46. Hall EJ, Giaccia AJ (2006) Radiobiology for the radiologist, 6th edn. Lippincott Williams & Wilkins, Philadelphia, PAGoogle Scholar
  47. Harper JW, Elledge SJ (2007) The DNA damage response: ten years after. Mol Cell 28:739–745PubMedCrossRefGoogle Scholar
  48. Hoeijmakers JH (2009) DNA damage, aging, and cancer. N Engl J Med 361:1475–1485PubMedCrossRefGoogle Scholar
  49. Hsu YC, Chern JJ, Cai Y et al (2007) Drosophila TCTP is essential for growth and proliferation through regulation of dRheb GTPase. Nature 445:785–788PubMedCrossRefGoogle Scholar
  50. Huang L, Snyder AR, Morgan WF (2003) Radiation-induced genomic instability and its implications for radiation carcinogenesis. Oncogene 22:5848–5854PubMedCrossRefGoogle Scholar
  51. Huang Q, Li F, Liu X et al (2011) Caspase 3-mediated stimulation of tumor cell repopulation during cancer radiotherapy. Nat Med 17:860–866PubMedPubMedCentralCrossRefGoogle Scholar
  52. Iliakis G, Wang Y, Guan J et al (2003) DNA damage checkpoint control in cells exposed to ionizing radiation. Oncogene 22:5834–5847PubMedCrossRefGoogle Scholar
  53. Jackson SP, Bartek J (2009) The DNA-damage response in human biology and disease. Nature 461:1071–1078PubMedPubMedCentralCrossRefGoogle Scholar
  54. Jasin M (2015) Accolades for the DNA damage response. N Engl J Med 373:1492–1495PubMedCrossRefGoogle Scholar
  55. Jeggo PA, Pearl LH, Carr AM (2016) DNA repair, genome stability and cancer: a historical perspective. Nat Rev Cancer 16:35–42PubMedCrossRefGoogle Scholar
  56. Johansson H, Svensson F, Runnberg R et al (2010a) Phosphorylated nucleolin interacts with translationally controlled tumor protein during mitosis and with Oct4 during interphase in ES cells. PloS One 5:e13678PubMedPubMedCentralCrossRefGoogle Scholar
  57. Johansson H, Vizlin-Hodzic D, Simonsson T et al (2010b) Translationally controlled tumor protein interacts with nucleophosmin during mitosis in ES cells. Cell Cycle 9:2160–2169PubMedCrossRefGoogle Scholar
  58. Johnson TM, Antrobus R, Johnson LN (2008) Plk1 activation by Ste20-like kinase (Slk) phosphorylation and polo-box phosphopeptide binding assayed with the substrate translationally controlled tumor protein (TCTP). Biochemistry 47:3688–3696PubMedCrossRefGoogle Scholar
  59. Jung J, Kim HY, Kim M et al (2011) Translationally controlled tumor protein induces human breast epithelial cell transformation through the activation of Src. Oncogene 30:2264–2274PubMedCrossRefGoogle Scholar
  60. Kashiwakura JC, Ando T, Matsumoto K et al (2012) Histamine-releasing factor has a proinflammatory role in mouse models of asthma and allergy. J Clin Invest 122:218–228PubMedCrossRefGoogle Scholar
  61. Katschinski DM, Boos K, Schindler SG et al (2000) Pivotal role of reactive oxygen species as intracellular mediators of hyperthermia-induced apoptosis. J Biol Chem 275:21094–21098PubMedCrossRefGoogle Scholar
  62. Koide Y, Kiyota T, Tonganunt M et al (2009) Embryonic lethality of fortilin-null mutant mice by BMP-pathway overactivation. Biochim Biophys Acta 2009:326–338CrossRefGoogle Scholar
  63. Koziol MJ, Garrett N, Gurdon JB (2007) Tpt1 activates transcription of oct4 and nanog in transplanted somatic nuclei. Curr Biol 17:801–807PubMedPubMedCentralCrossRefGoogle Scholar
  64. Larrea AA, Lujan SA, Kunkel TA (2010) SnapShot: DNA mismatch repair. Cell 141:730–e731PubMedCrossRefGoogle Scholar
  65. LaVerne JA, Pimblott SM (1993) Yields of hydroxyl radical and hydrated electron scavenging reactions in aqueous solutions of biological interest. Radiat Res 135:16–23PubMedCrossRefGoogle Scholar
  66. Lazebnik YA, Kaufmann SH, Desnoyers S et al (1994) Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371:346–347PubMedCrossRefGoogle Scholar
  67. Lee JH, Rho SB, Park SY et al (2008) Interaction between fortilin and transforming growth factor-beta stimulated clone-22 (TSC-22) prevents apoptosis via the destabilization of TSC-22. FEBS Lett 582:1210–1218PubMedCrossRefGoogle Scholar
  68. Li F, Zhang D, Fujise K (2001) Characterization of fortilin, a novel antiapoptotic protein. J Biol Chem 276:47542–47549PubMedCrossRefGoogle Scholar
  69. Li M, Gonon G, Buonanno M et al (2014) Health risks of space exploration: targeted and non-targeted oxidative injury by high charge and high energy particles. Antioxid Redox Signal 20:1501–1523PubMedPubMedCentralCrossRefGoogle Scholar
  70. Lieber MR (2008) The mechanism of human nonhomologous DNA end joining. J Biol Chem 283:1–5PubMedCrossRefGoogle Scholar
  71. Lin J, Epel E, Blackburn E (2012) Telomeres and lifestyle factors: roles in cellular aging. Mutat Res 730:85–89PubMedCrossRefGoogle Scholar
  72. Lindahl T (1993) Instability and decay of the primary structure of DNA. Nature 362:709–715PubMedCrossRefGoogle Scholar
  73. Little JB (1968) Delayed initiation of DNA synthesis in irradiated human diploid cells. Nature 218:1064–1065PubMedCrossRefGoogle Scholar
  74. Little JB (2000) Radiation carcinogenesis. Carcinogenesis 21:394–404CrossRefGoogle Scholar
  75. Liu H, Peng HW, Cheng YS et al (2005) Stabilization and enhancement of the antiapoptotic activity of mcl-1 by TCTP. Mol Cell Biol 25:3117–3126PubMedPubMedCentralCrossRefGoogle Scholar
  76. Liu XS, Li H, Song B et al (2010) Polo-like kinase 1 phosphorylation of G2 and S-phase-expressed 1 protein is essential for p53 inactivation during G2 checkpoint recovery. EMBO Rep 11:626–632PubMedPubMedCentralCrossRefGoogle Scholar
  77. Lucibello M, Gambacurta A, Zonfrillo M et al (2011) TCTP is a critical survival factor that protects cancer cells from oxidative stress-induced cell-death. Exp Cell Res 317:2479–2489PubMedCrossRefGoogle Scholar
  78. Macdonald SM (2012) Potential role of histamine releasing factor (HRF) as a therapeutic target for treating asthma and allergy. J Asthma Allergy 5:51–59PubMedPubMedCentralCrossRefGoogle Scholar
  79. MacDonald SM, Rafnar T, Langdon J et al (1995) Molecular identification of an IgE-dependent histamine-releasing factor. Science 269:688–690PubMedCrossRefGoogle Scholar
  80. McKinnon PJ (2009) DNA repair deficiency and neurological disease. Nat Rev Neurosci 10:100–112PubMedPubMedCentralCrossRefGoogle Scholar
  81. Medema RH, Macurek L (2012) Checkpoint control and cancer. Oncogene 31:2601–2613PubMedCrossRefGoogle Scholar
  82. Meesungnoen J, Benrahmoune M, Filali-Mouhim A et al (2001) Monte Carlo calculation of the primary radical and molecular yields of liquid water radiolysis in the linear energy transfer range 0.3–6.5 keV/um: application to 137Cs gamma rays. Radiat Res 155:269–278. Erratum Published in Radiat Res 155 (2001) 2873PubMedCrossRefGoogle Scholar
  83. Moskovitz J (2005) Roles of methionine suldfoxide reductases in antioxidant defense, protein regulation and survival. Curr Pharm Des 11:1451–1457PubMedCrossRefGoogle Scholar
  84. Mothersill C, Seymour CB (2004) Radiation-induced bystander effects--implications for cancer. Nat Rev Cancer 4:158–164PubMedCrossRefGoogle Scholar
  85. Munirathinam G, Ramaswamy K (2012) Sumoylation of human translationally controlled tumor protein is important for its nuclear transport. Biochem Res Int 2012:831940PubMedPubMedCentralCrossRefGoogle Scholar
  86. Muroya Y, Plante I, Azzam EI et al (2006) High-LET ion radiolysis of water: visualization of the formation and evolution of ion tracks and relevance to the radiation-induced bystander effect. Radiat Res 165:485–491PubMedCrossRefGoogle Scholar
  87. Nagano-Ito M, Banba A, Ichikawa S (2009) Functional cloning of genes that suppress oxidative stress-induced cell death: TCTP prevents hydrogen peroxide-induced cell death. FEBS Lett 583:1363–1367PubMedCrossRefGoogle Scholar
  88. Nam EA, Cortez D (2011) ATR signalling: more than meeting at the fork. Biochem J 436:527–536PubMedPubMedCentralCrossRefGoogle Scholar
  89. NCRP (2009) Ionizing radiation exposure of the population of the United States. National Council on Radiation Protection and Measurements, BethesdaGoogle Scholar
  90. Newhauser WD, Durante M (2011) Assessing the risk of second malignancies after modern radiotherapy. Nat Rev Cancer 11:438–448PubMedPubMedCentralCrossRefGoogle Scholar
  91. Nikjoo H, O’Neill P, Wilson WE et al (2001) Computational approach for determining the spectrum of DNA damage induced by ionizing radiation. Radiat Res 156:577–583PubMedCrossRefGoogle Scholar
  92. Oikawa K, Ohbayashi T, Mimura J et al (2002) Dioxin stimulates synthesis and secretion of IgE-dependent histamine-releasing factor. Biochem Biophys Res Commun 290:984–987PubMedCrossRefGoogle Scholar
  93. Okada H, Mak TW (2004) Pathways of apoptotic and non-apoptotic death in tumour cells. Nat Rev Cancer 4:592–603PubMedCrossRefGoogle Scholar
  94. O’Neill P, Wardman P (2009) Radiation chemistry comes before radiation biology. Int J Radiat Biol 85:9–25PubMedCrossRefGoogle Scholar
  95. Panier S, Boulton SJ (2014) Double-strand break repair: 53BP1 comes into focus. Nat Rev 15:7–18CrossRefGoogle Scholar
  96. Petkau A (1987) Role of superoxide dismutase in modification of radiation injury. Br J Cancer Suppl 8:87–95PubMedPubMedCentralGoogle Scholar
  97. Petros AM, Olejniczak ET, Fesik SW (1644) Structural biology of the Bcl-2 family of proteins. Biochim Biophys Acta 2004:83–94Google Scholar
  98. Petruseva IO, Evdokimov AN, Lavrik OI (2014) Molecular mechanism of global genome nucleotide excision repair. Acta Naturae 6:23–34PubMedPubMedCentralGoogle Scholar
  99. Platzman R (1958) The physical and chemical basis of mechanisms in radiation biology. In: Claus W (ed) Radiation biology and medicine. Selected reviews in the life sciences. Addison-Wesley, Reading, MA, pp 15–72Google Scholar
  100. Postel-Vinay S, Vanhecke E, Olaussen KA et al (2012) The potential of exploiting DNA-repair defects for optimizing lung cancer treatment. Nature reviews. Clin Oncol 9:144–155Google Scholar
  101. Prise KM, Schettino G, Folkard M et al (2005) New insights on cell death from radiation exposure. Lancet Oncol 6:520–528PubMedCrossRefGoogle Scholar
  102. Rao CV, Yamada HY, Yao Y et al (2009) Enhanced genomic instabilities caused by deregulated microtubule dynamics and chromosome segregation: a perspective from genetic studies in mice. Carcinogenesis 30:1469–1474PubMedPubMedCentralCrossRefGoogle Scholar
  103. Raynaud CM, Sabatier L, Philipot O et al (2008) Telomere length, telomeric proteins and genomic instability during the multistep carcinogenic process. Crit Rev Oncol Hematol 66:99–117PubMedCrossRefGoogle Scholar
  104. Rho SB, Lee JH, Park MS et al (2011) Anti-apoptotic protein TCTP controls the stability of the tumor suppressor p53. FEBS Lett 585:29–35PubMedCrossRefGoogle Scholar
  105. Rid R, Onder K, Trost A et al (2010) H2O2-dependent translocation of TCTP into the nucleus enables its interaction with VDR in human keratinocytes: TCTP as a further module in calcitriol signalling. J Steroid Biochem Mol Biol 118:29–40PubMedCrossRefGoogle Scholar
  106. Rogakou EP, Pilch DR, Orr AH et al (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273:5858–5868PubMedCrossRefGoogle Scholar
  107. Scolnick DM, Halazonetis TD (2000) Chfr defines a mitotic stress checkpoint that delays entry into metaphase. Nature 406:430–435PubMedCrossRefGoogle Scholar
  108. Sengupta S, Harris CC (2005) p53: traffic cop at the crossroads of DNA repair and recombination. Nat Rev 6:44–55CrossRefGoogle Scholar
  109. Shah NR, Mahmoudi M (2015) The role of DNA damage and repair in atherosclerosis: a review. J Mol Cell Cardiol 86:147–157PubMedCrossRefGoogle Scholar
  110. Shiloh Y (2003) ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 3:155–168PubMedCrossRefGoogle Scholar
  111. Shiloh Y, Ziv Y (2013) The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat Rev 14:197–210CrossRefGoogle Scholar
  112. Sirois I, Raymond MA, Brassard N et al (2011) Caspase-3-dependent export of TCTP: a novel pathway for antiapoptotic intercellular communication. Cell Death Differ 18:549–562PubMedCrossRefGoogle Scholar
  113. Spitz DR, Azzam EI, Li JJ et al (2004) Metabolic oxidation/reduction reactions and cellular responses to ionizing radiation: a unifying concept in stress response biology. Cancer Metastasis Rev 23:311–322PubMedCrossRefGoogle Scholar
  114. Stucki M, Jackson SP (2006) GammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair (Amst) 5:534–543CrossRefGoogle Scholar
  115. Susini L, Besse S, Duflaut D et al (2008) TCTP protects from apoptotic cell death by antagonizing bax function. Cell Death Differ 15:1211–1220PubMedCrossRefGoogle Scholar
  116. Suzuki M, Youle RJ, Tjandra N (2000) Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 103:645–654PubMedCrossRefGoogle Scholar
  117. Syljuasen RG, Krolewski B, Little JB (1999) Loss of normal G1 checkpoint control is an early step in carcinogenesis, independent of p53 status. Cancer Res 59:1008–1014PubMedGoogle Scholar
  118. Symington LS, Gautier J (2011) Double-strand break end resection and repair pathway choice. Annu Rev Genet 45:247–271PubMedCrossRefGoogle Scholar
  119. Thaw P, Baxter NJ, Hounslow AM et al (2001) Structure of TCTP reveals unexpected relationship with guanine nucleotide-free chaperones. Nat Struct Biol 8:701–704PubMedCrossRefGoogle Scholar
  120. Thomas G, Thomas G, Luther H (1981) Transcriptional and translational control of cytoplasmic proteins after serum stimulation of quiescent Swiss 3T3 cells. Proc Natl Acad Sci USA 78:5712–5716PubMedPubMedCentralCrossRefGoogle Scholar
  121. Thompson LH (2012) Recognition, signaling, and repair of DNA double-strand breaks produced by ionizing radiation in mammalian cells: the molecular choreography. Mutat Res 751:158–246PubMedCrossRefGoogle Scholar
  122. Tsarova K, Yarmola EG, Bubb MR (2010) Identification of a cofilin-like actin-binding site on translationally controlled tumor protein (TCTP). FEBS Lett 584:4756–4760PubMedCrossRefGoogle Scholar
  123. Turinetto V, Giachino C (2015) Multiple facets of histone variant H2AX: a DNA double-strand-break marker with several biological functions. Nucleic Acids Res 43:2489–2498PubMedPubMedCentralCrossRefGoogle Scholar
  124. Tuynder M, Susini L, Prieur S et al (2002) Biological models and genes of tumor reversion: cellular reprogramming through tpt1/TCTP and SIAH-1. Proc Natl Acad Sci USA 99:14976–14981PubMedPubMedCentralCrossRefGoogle Scholar
  125. Tuynder M, Fiucci G, Prieur S et al (2004) Translationally controlled tumor protein is a target of tumor reversion. Proc Natl Acad Sci USA 101:15364–15369PubMedPubMedCentralCrossRefGoogle Scholar
  126. Tyldesley S, Boyd C, Schulze K et al (2001) Estimating the need for radiotherapy for lung cancer: an evidence-based, epidemiologic approach. Int J Radiat Oncol Biol Phys 49:973–985PubMedCrossRefGoogle Scholar
  127. van Vugt MA, Gardino AK, Linding R et al (2010) A mitotic phosphorylation feedback network connects Cdk1, Plk1, 53BP1, and Chk2 to inactivate the G(2)/M DNA damage checkpoint. PLoS Biol 8:e1000287PubMedPubMedCentralCrossRefGoogle Scholar
  128. Weichselbaum RR, Nove J, Little JB (1980) X-ray sensitivity of fifty-three human diploid fibroblast cell strains from patients with characterized genetic disorders. Cancer Res 40:920–925PubMedGoogle Scholar
  129. Weinberg RA (2007) The biology of cancer. Garland Science, Taylor & Francis Group, LLC, New YorkGoogle Scholar
  130. Whitesell L, Lindquist SL (2005) HSP90 and the chaperoning of cancer. Nat Rev Cancer 5:761–772PubMedCrossRefGoogle Scholar
  131. Williams ES, Klingler R, Ponnaiya B et al (2009) Telomere dysfunction and DNA-PKcs deficiency: characterization and consequence. Cancer Res 69:2100–2107PubMedPubMedCentralCrossRefGoogle Scholar
  132. Yang Y, Yang F, Xiong Z et al (2005) An N-terminal region of translationally controlled tumor protein is required for its antiapoptotic activity. Oncogene 24:4778–4788PubMedPubMedCentralCrossRefGoogle Scholar
  133. Yarm FR (2002) Plk phosphorylation regulates the microtubule-stabilizing protein TCTP. Mol Cell Biol 22:6209–6221PubMedPubMedCentralCrossRefGoogle Scholar
  134. Yenofsky R, Bergmann I, Brawerman G (1982) Messenger RNA species partially in a repressed state in mouse sarcoma ascites cells. Proc Natl Acad Sci USA 79:5876–5880PubMedPubMedCentralCrossRefGoogle Scholar
  135. Yenofsky R, Cereghini S, Krowczynska A et al (1983) Regulation of mRNA utilization in mouse erythroleukemia cells induced to differentiate by exposure to dimethyl sulfoxide. Mol Cell Biol 3:1197–1203PubMedPubMedCentralCrossRefGoogle Scholar
  136. Yi C, He C (2013) DNA repair by reversal of DNA damage. Cold Spring Harb Perspect Biol 5:a012575PubMedPubMedCentralCrossRefGoogle Scholar
  137. Yu X, Minter-Dykhouse K, Malureanu L et al (2005) Chfr is required for tumor suppression and Aurora A regulation. Nat Genet 37:401–406PubMedCrossRefGoogle Scholar
  138. Yue J, Wang Q, Lu H et al (2009) The cytoskeleton protein filamin-A is required for an efficient recombinational DNA double strand break repair. Cancer Res 69:7978–7985PubMedPubMedCentralCrossRefGoogle Scholar
  139. Zhang D, Li F, Weidner D et al (2002) Physical and functional interaction between myeloid cell leukemia 1 protein (MCL1) and Fortilin. The potential role of MCL1 as a fortilin chaperone. J Biol Chem 277:37430–37438PubMedCrossRefGoogle Scholar
  140. Zhang J, de Toledo SM, Pandey BN et al (2012) Role of the translationally controlled tumor protein in DNA damage sensing and repair. Proc Natl Acad Sci USA 109:E926–E933PubMedPubMedCentralCrossRefGoogle Scholar
  141. Zhou BB, Elledge SJ (2000) The DNA damage response: putting checkpoints in perspective. Nature 408:433–439PubMedCrossRefGoogle Scholar
  142. Zimbrick JD (2002) Radiation chemistry and the Radiation Research Society: a history from the beginning. Radiat Res 158:127–140PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Institute of Preventive Medicine, Fourth Military Medical UniversityXi’an ShannxiPeople’s Republic of China
  2. 2.Department of Radiology, New Jersey Medical School, Cancer CenterRutgers UniversityNewarkUSA

Personalised recommendations