1,443
Views
2
CrossRef citations to date
0
Altmetric
Original Articles

International expert group collaboration for developing an adverse outcome pathway for radiation induced leukemia

ORCID Icon, , ORCID Icon, , , , , , & show all
Pages 1802-1815 | Received 30 Mar 2022, Accepted 22 Aug 2022, Published online: 07 Sep 2022

References

  • Alexander BJ, Rasko JE, Morahan G, Cook WD. 1995. Gene deletion explains both in vivo and in vitro generated chromosome 2 aberrations associated with murine myeloid leukemia. Leukemia. 9(12):2009–2015.
  • Allen TE, Goodman JM, Gutsell S, Russell PJ. 2014. Defining molecular initiating events in the adverse outcome pathway framework for risk. Chem Res Toxicol. 27(12):2100–2112.
  • Alloni D, Cutaia C, Mariotti L, Friedland W, Ottolenghi A. 2014. Modeling dose deposition and DNA damage due to low-energy β(-) emitters. Radiat Res. 182(3):322–330.
  • Anglesio MS, Papadopoulos N, Ayhan A, Nazeran TM, Noe M, Horlings HM, Lum A, Jones S, Senz J, Seckin T, et al. 2017. Cancer-associated mutations in endometriosis without cancer. N Engl J Med. 376(19):1835–1848.
  • Babineau J. 2014. Product review: covidence (systematic review software). J Can Health Libr Assoc. 35(2):68–71.
  • Bai J, Wang Y, Wang J, Zhai J, He F, Zhu G. 2020. Irradiation-induced senescence of bone marrow mesenchymal stem cells aggravates osteogenic differentiation dysfunction via paracrine signaling. Am J Physiol Cell Physiol. 318(5):C1005–C1017.
  • Boice JD, Jr., Cohen SS, Mumma MT, Ellis ED. 2022. The Million Person Study, whence it came and why. Int J Radiat Biol. 98(4):537–550.
  • Bouffler SD, Meijne EI, Morris DJ, Papworth D. 1997. Chromosome 2 hypersensitivity and clonal development in murine radiation acute myeloid leukaemia. Int J Radiat Biol. 72(2):181–189.
  • Bouville A, Toohey RE, Boice JD, Jr., Beck HL, Dauer LT, Eckerman KF, Hagemeyer D, Leggett RW, Mumma MT, Napier B, et al. 2015. Dose reconstruction for the million worker study: status and guidelines. Health Phys. 108(2):206–220.
  • Brown NL, Finnon R, Bulman RA, Finnon P, Moody J, Bouffler SD, Badie C. 2011. Sfpi1/PU.1 mutations in mouse radiation-induced acute myeloid leukaemias affect mRNA and protein abundance and associate with disrupted transcription. Leuk Res. 35(1):126–132.
  • Brown N, Finnon R, Manning G, Bouffler S, Badie C. 2015. Influence of radiation quality on mouse chromosome 2 deletions in radiation-induced acute myeloid leukaemia. Mutat Res Genet Toxicol Environ Mutagen. 793:48–54.
  • Bullinger L, Dohner K, Dohner H. 2017. Genomics of acute myeloid leukemia diagnosis and pathways. J Clin Oncol. 35(9):934–946.
  • Camacho V, Kuznetsova V, Welner RS. 2021. Inflammatory cytokines shape an altered immune response during myeloid malignancies. Front Immunol. 12:772408.
  • Chauhan V, Beaton D, Hamada N, Wilkins R, Burtt J, Leblanc J, Cool D, Garnier-Laplace J, Laurier D, Le Y, et al. 2022. Adverse outcome pathway: a path toward better data consolidation and global co-ordination of radiation research. Int J Radiat Biol. 1–10.
  • Chauhan V, Hamada N, Monceau V, Ebrahimian T, Adam N, Wilkins RC, Sebastian S, Patel ZS, Huff JL, Simonetto C, et al. 2021. Expert consultation is vital for adverse outcome pathway development: a case example of cardiovascular effects of ionizing radiation. Int J Radiat Biol. 97(11):1516–1525.
  • Chauhan V, Said Z, Daka J, Sadi B, Bijlani D, Marchetti F, Beaton D, Gaw A, Li C, Burtt J, et al. 2019. Is there a role for the adverse outcome pathway framework to support radiation protection? Int J Radiat Biol. 95(2):225–232.
  • Cheek DM, Naxerova K. 2022. Mapping the long road to cancer. Cell. 185(6):939–940.
  • Christiansen DH, Andersen MK, Pedersen-Bjergaard J. 2001. Mutations with loss of heterozygosity of p53 are common in therapy-related myelodysplasia and acute myeloid leukemia after exposure to alkylating agents and significantly associated with deletion or loss of 5q, a complex karyotype, and a poor prognosis. JCO. 19(5):1405–1413.
  • Cook WD, McCaw BJ, Herring C, John DL, Foote SJ, Nutt SL, Adams JM. 2004. PU.1 is a suppressor of myeloid leukemia, inactivated in mice by gene deletion and mutation of its DNA binding domain. Blood. 104(12):3437–3444.
  • Coombs CC, Zehir A, Devlin SM, Kishtagari A, Syed A, Jonsson P, Hyman DM, Solit DB, Robson ME, Baselga J, et al. 2017. Therapy-related clonal hematopoiesis in patients with non-hematologic cancers is common and associated with adverse clinical outcomes. Cell Stem Cell. 21(3):374–382 e374.
  • Darakhshan F, Badie C, Moody J, Coster M, Finnon R, Finnon P, Edwards AA, Szluinska M, Skidmore CJ, Yoshida K, et al. 2006. Evidence for complex multigenic inheritance of radiation AML susceptibility in mice revealed using a surrogate phenotypic assay. Carcinogenesis. 27(2):311–318.
  • Dekkers F, Bijwaard H, Bouffler S, Ellender M, Huiskamp R, Kowalczuk C, Meijne E, Sutmuller M. 2011. A two-mutation model of radiation-induced acute myeloid leukemia using historical mouse data. Radiat Environ Biophys. 50(1):37–45.
  • Ding L, Ley TJ, Larson DE, Miller CA, Koboldt DC, Welch JS, Ritchey JK, Young MA, Lamprecht T, McLellan MD, et al. 2012. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature. 481(7382):506–510.
  • Dohner H, Weisdorf DJ, Bloomfield CD. 2015. Acute myeloid leukemia. N Engl J Med. 373(12):1136–1152.
  • Finnon R, Brown N, Moody J, Badie C, Olme CH, Huiskamp R, Meijne E, Sutmuller M, Rosemann M, Bouffler SD. 2012. Flt3-ITD mutations in a mouse model of radiation-induced acute myeloid leukaemia. Leukemia. 26(6):1445–1446.
  • Fleenor CJ, Marusyk A, DeGregori J. 2010. Ionizing radiation and hematopoietic malignancies: altering the adaptive landscape. Cell Cycle. 9(15):3005–3011.
  • Folley JH, Borges W, Yamawaki T. 1952. Incidence of leukemia in survivors of the atomic bomb in Hiroshima and Nagasaki, Japan. Am J Med. 13(3):311–321.
  • Gault N, Verbiest T, Badie C, Romeo PH, Bouffler S. 2019. Hematopoietic stem and progenitor cell responses to low radiation doses - implications for leukemia risk. Int J Radiat Biol. 95(7):892–899.
  • Genovese G, Kahler AK, Handsaker RE, Lindberg J, Rose SA, Bakhoum SF, Chambert K, Mick E, Neale BM, Fromer M, et al. 2014. Clonal hematopoiesis and blood-cancer risk inferred from blood DNA sequence. N Engl J Med. 371(26):2477–2487.
  • Gomolka M, Blyth B, Bourguignon M, Badie C, Schmitz A, Talbot C, Hoeschen C, Salomaa S. 2020. Potential screening assays for individual radiation sensitivity and susceptibility and their current validation state. Int J Radiat Biol. 96(3):280–296.
  • Goodhead DT. 1994. Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int J Radiat Biol. 65(1):7–17.
  • Hellmich C, Moore JA, Bowles KM, Rushworth SA. 2020. Bone marrow senescence and the microenvironment of hematological malignancies. Front Oncol. 10:230.
  • Henry CJ, Marusyk A, DeGregori J. 2011. Aging-associated changes in hematopoiesis and leukemogenesis: what’s the connection? Aging (Albany NY). 3(6):643–656.
  • Hepburn M, Doherty I, Briscoe C, Riches A. 1987. Transplantation and morphological studies of primary and passaged murine radiation-induced myeloid leukaemias. Leuk Res. 11(11):1001–1009.
  • Hsu WL, Preston DL, Soda M, Sugiyama H, Funamoto S, Kodama K, Kimura A, Kamada N, Dohy H, Tomonaga M, et al. 2013. The incidence of leukemia, lymphoma and multiple myeloma among atomic bomb survivors: 1950–2001. Radiat Res. 179(3):361–382.
  • Jaiswal S, Fontanillas P, Flannick J, Manning A, Grauman PV, Mar BG, Lindsley RC, Mermel CH, Burtt N, Chavez A, et al. 2014. Age-related clonal hematopoiesis associated with adverse outcomes. N Engl J Med. 371(26):2488–2498.
  • Juliusson G, Lehmann S, Lazarevic V. 2021. Epidemiology and etiology of AML. In: Röllig C, Ossenkoppele GJ, editors. Acute myeloid leukemia. Cham: Springer International Publishing; p. 1–22.
  • Karabulutoglu M, Finnon R, Cruz-Garcia L, Hill MA, Badie C. 2021. Oxidative stress and x-ray exposure levels-dependent survival and metabolic changes in murine HSPCs. Antioxidants (Basel). 11(1):11.
  • Karabulutoglu M, Finnon R, Imaoka T, Friedl AA, Badie C. 2019. Influence of diet and metabolism on hematopoietic stem cells and leukemia development following ionizing radiation exposure. Int J Radiat Biol. 95(4):452–479.
  • Karlic H, Herrmann H, Varga F, Thaler R, Reitermaier R, Spitzer S, Ghanim V, Blatt K, Sperr WR, Valent P, et al. 2014. The role of epigenetics in the regulation of apoptosis in myelodysplastic syndromes and acute myeloid leukemia. Crit Rev Oncol Hematol. 90(1):1–16.
  • Khaldoyanidi S, Nagorsen D, Stein A, Ossenkoppele G, Subklewe M. 2021. Immune biology of acute myeloid leukemia: implications for immunotherapy. J Clin Oncol. 39(5):419–432.
  • Klymenko SV, Bink K, Trott KR, Bebeshko VG, Bazyka DA, Dmytrenko IV, Abramenko IV, Bilous NI, Zitzelsberger H, Misurin AV, et al. 2005. MLL gene alterations in radiation-associated acute myeloid leukemia. Exp Oncol. 27(1):71–75.
  • Klymenko S, Trott K, Atkinson M, Bink K, Bebeshko V, Bazyka D, Dmytrenko I, Abramenko I, Bilous N, Misurin A, et al. 2005. Aml1 gene rearrangements and mutations in radiation-associated acute myeloid leukemia and myelodysplastic syndromes. J Radiat Res. 46(2):249–255.
  • Kozbenko T, Adam N, Lai V, Sandhu S, Kuan J, Flores D, Appleby M, Parker H, Hocking R, Tsaioun K, et al. 2022. Deploying elements of scoping review methods for Adverse Outcome Pathway development: a space travel case example. Int J Radiat Biol. Submitted. 1–12.
  • Larrue C, Heydt Q, Saland E, Boutzen H, Kaoma T, Sarry JE, Joffre C, Recher C. 2019. Oncogenic KIT mutations induce STAT3-dependent autophagy to support cell proliferation in acute myeloid leukemia. Oncogenesis. 8(8):39.
  • Leuraud K, Richardson DB, Cardis E, Daniels RD, Gillies M, O'Hagan JA, Hamra GB, Haylock R, Laurier D, Moissonnier M, et al. 2015. Ionising radiation and risk of death from leukaemia and lymphoma in radiation-monitored workers (INWORKS): an international cohort study. Lancet Haematol. 2(7):e276–e281.
  • Lo Coco F, Pisegna S, Diverio D. 1997. The AML1 gene: a transcription factor involved in the pathogenesis of myeloid and lymphoid leukemias. Haematologica. 82(3):364–370.
  • Loh PR, Genovese G, Handsaker RE, Finucane HK, Reshef YA, Palamara PF, Birmann BM, Talkowski ME, Bakhoum SF, McCarroll SA, et al. 2018. Insights into clonal haematopoiesis from 8,342 mosaic chromosomal alterations. Nature. 559(7714):350–355.
  • Lomax ME, Folkes LK, O'Neill P. 2013. Biological consequences of radiation-induced DNA damage: relevance to radiotherapy. Clin Oncol (R Coll Radiol). 25(10):578–585.
  • Major IR. 1979. Induction of myeloid leukaemia by whole-body single exposure of CBA male mice to x-rays. Br J Cancer. 40(6):903–913.
  • Marusyk A, Casas-Selves M, Henry CJ, Zaberezhnyy V, Klawitter J, Christians U, DeGregori J. 2009. Irradiation alters selection for oncogenic mutations in hematopoietic progenitors. Cancer Res. 69(18):7262–7269.
  • McNerney ME, Godley LA, Le Beau MM. 2017. Therapy-related myeloid neoplasms: when genetics and environment collide. Nat Rev Cancer. 17(9):513–527.
  • Meldrum RA, Mole RH. 1982. Radiation-induced myeloid leukaemia in CBA/H mice: a non-immunogenic malignant disease in syngeneic mice. Br J Cancer. 45(3):403–412.
  • NCRP Report 171. 2012. Uncertainties in the estimation of radiation risks and probability of disease causation. Bethesda (MD): NCRP.
  • NCRP Report 186. 2020. Approaches for integrating information from radiation biology and epidemology to enhance low-dose health risk assessments. Bethesda (MD): NCRP.
  • O'Brien G, Cruz-Garcia L, Zyla J, Brown N, Finnon R, Polanska J, Badie C. 2020. Kras mutations and PU.1 promoter methylation are new pathways in murine radiation-induced AML. Carcinogenesis. 41(8):1104–1112.
  • Olme CH, Brown N, Finnon R, Bouffler SD, Badie C. 2013. Frequency of acute myeloid leukaemia-associated mouse chromosome 2 deletions in X-ray exposed immature haematopoietic progenitors and stem cells. Mutat Res. 756(1–2):119–126.
  • Olme CH, Finnon R, Brown N, Kabacik S, Bouffler SD, Badie C. 2013. Live cell detection of chromosome 2 deletion and Sfpi1/PU1 loss in radiation-induced mouse acute myeloid leukaemia. Leuk Res. 37(10):1374–1382.
  • Patel A, Anderson J, Kraft D, Finnon R, Finnon P, Scudamore CL, Manning G, Bulman R, Brown N, Bouffler S, et al. 2016. The influence of the CTIP polymorphism, Q418P, on homologous recombination and predisposition to radiation-induced tumorigenesis (mainly rAML) in mice. Radiat Res. 186(6):638–649.
  • Pedersen-Bjergaard J, Philip P, Larsen SO, Andersson M, Daugaard G, Ersboll J, Hansen SW, Hou-Jensen K, Nielsen D, Sigsgaard TC. 1993. Therapy-related myelodysplasia and acute myeloid leukemia. Cytogenetic characteristics of 115 consecutive cases and risk in seven cohorts of patients treated intensively for malignant diseases in the Copenhagen series. Leukemia. 7(12):1975–1986.
  • Peng Y, Brown N, Finnon R, Warner CL, Liu X, Genik PC, Callan MA, Ray FA, Borak TB, Badie C, et al. 2009. Radiation leukemogenesis in mice: loss of PU.1 on chromosome 2 in CBA and C57BL/6 mice after irradiation with 1 GeV/nucleon 56Fe ions, X rays or gamma rays. Part I. Experimental observations. Radiat Res. 171(4):474–483.
  • Poluben L, Puligandla M, Neuberg D, Bryke CR, Hsu Y, Shumeiko O, Yuan X, Voznesensky O, Pihan G, Adam M, et al. 2019. Characteristics of myeloproliferative neoplasms in patients exposed to ionizing radiation following the Chernobyl nuclear accident. Am J Hematol. 94(1):62–73.
  • Preston RJ, Ruhm W, Azzam EI, Boice JD, Bouffler S, Held KD, Little MP, Shore RE, Shuryak I, Weil MM. 2021. Adverse outcome pathways, key events, and radiation risk assessment. Int J Radiat Biol. 97(6):804–814.
  • Rassool FV, Gaymes TJ, Omidvar N, Brady N, Beurlet S, Pla M, Reboul M, Lea N, Chomienne C, Thomas NS, et al. 2007. Reactive oxygen species, DNA damage, and error-prone repair: a model for genomic instability with progression in myeloid leukemia? Cancer Research. 67(18):8762–8771.
  • Riley PA. 1994. Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int J Radiat Biol. 65(1):27–33.
  • Rithidech KN, Cronkite EP, Bond VP. 1999. Advantages of the CBA mouse in leukemogenesis research. Blood Cells Mol Dis. 25(1):38–45.
  • Rothkamm K, Kruger I, Thompson LH, Lobrich M. 2003. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol Cell Biol. 23(16):5706–5715.
  • Rubner Y, Wunderlich R, Ruhle PF, Kulzer L, Werthmoller N, Frey B, Weiss EM, Keilholz L, Fietkau R, Gaipl US. 2012. How does ionizing irradiation contribute to the induction of anti-tumor immunity? Front Oncol. 2:75.
  • Sabin RJ, Anderson RM. 2011. Cellular Senescence - its role in cancer and the response to ionizing radiation. Genome Integr. 2(1):7.
  • Schuringa JJ, Bonifer C. 2020. Dissecting clonal heterogeneity in AML. Cancer Cell. 38(6):782–784.
  • Shallis RM, Wang R, Davidoff A, Ma X, Zeidan AM. 2019. Epidemiology of acute myeloid leukemia: recent progress and enduring challenges. Blood Rev. 36:70–87.
  • Siegel RL, Miller KD, Jemal A. 2019. Cancer statistics, 2019. CA A Cancer J Clin. 69(1):7–34.
  • Silver A, Moody J, Dunford R, Clark D, Ganz S, Bulman R, Bouffler S, Finnon P, Meijne E, Huiskamp R, et al. 1999. Molecular mapping of chromosome 2 deletions in murine radiation-induced AML localizes a putative tumor suppressor gene to a 1.0 cM region homologous to human chromosome segment 11p11-12. Genes Chromosom Cancer. 24(2):95–104.
  • Smith SM, Le Beau MM, Huo D, Karrison T, Sobecks RM, Anastasi J, Vardiman JW, Rowley JD, Larson RA. 2003. Clinical-cytogenetic associations in 306 patients with therapy-related myelodysplasia and myeloid leukemia: the University of Chicago series. Blood. 102(1):43–52.
  • Steensma DP. 2018. Clinical consequences of clonal hematopoiesis of indeterminate potential. Blood Adv. 2(22):3404–3410.
  • Stouten S, Verduyn Lunel S, Finnon R, Badie C, Dekkers F. 2021. Modeling low-dose radiation-induced acute myeloid leukemia in male CBA/H mice. Radiat Environ Biophys. 60(1):49–60.
  • Super HJ, McCabe NR, Thirman MJ, Larson RA, Le Beau MM, Pedersen-Bjergaard J, Philip P, Diaz MO, Rowley JD. 1993. Rearrangements of the MLL gene in therapy-related acute myeloid leukemia in patients previously treated with agents targeting DNA-topoisomerase II. Blood. 82(12):3705–3711.
  • Takasugi M, Yoshida Y, Hara E, Ohtani N. 2022. The role of cellular senescence and SASP in tumour microenvironment. Febs J.
  • UNSCEAR 2021. Annex C. Biological mechanisms relevant for the inference of cancer risks from low-dose and low-dose-rate radiation UNSCEAR 2020/2021 report. Vienna: UNSCEAR.
  • Verbiest T, Bouffler S, Nutt SL, Badie C. 2015. PU.1 downregulation in murine radiation-induced acute myeloid leukaemia (AML): from molecular mechanism to human AML. Carcinogenesis. 36(4):413–419.
  • Verbiest T, Finnon R, Brown N, Cruz-Garcia L, Finnon P, O'Brien G, Ross E, Bouffler S, Scudamore CL, Badie C. 2018. Tracking preleukemic cells in vivo to reveal the sequence of molecular events in radiation leukemogenesis. Leukemia. 32(6):1435–1444.
  • Vinken M. 2013. The adverse outcome pathway concept: a pragmatic tool in toxicology. Toxicology. 312:158–165.
  • Wang B, Kohli J, Demaria M. 2020. Senescent cells in cancer therapy: friends or foes? Trends Cancer. 6(10):838–857.
  • Wang Y, Liu L, Zhou D. 2011. Inhibition of p38 MAPK attenuates ionizing radiation-induced hematopoietic cell senescence and residual bone marrow injury. Radiat Res. 176(6):743–752.
  • Wild CP. 2005. Complementing the genome with an “exposome”: the outstanding challenge of environmental exposure measurement in molecular epidemiology. Cancer Epidemiol Biomarkers Prev. 14(8):1847–1850.
  • Wodnar-Filipowicz A, Kalberer CP. 2007. Function of natural killer cells in immune defence against human leukaemia. Swiss Med Wkly. 137 Suppl 155(Suppl 155):25S–30S.
  • Wong TN, Ramsingh G, Young AL, Miller CA, Touma W, Welch JS, Lamprecht TL, Shen D, Hundal J, Fulton RS, et al. 2015. Role of TP53 mutations in the origin and evolution of therapy-related acute myeloid leukaemia. Nature. 518(7540):552–555.
  • Yasinska IM, Goncalves Silva I, Sakhnevych S, Gibbs BF, Raap U, Fasler-Kan E, Sumbayev VV. 2018. Biochemical mechanisms implemented by human acute myeloid leukemia cells to suppress host immune surveillance. Cell Mol Immunol. 15(11):989–991.
  • Zhao Y, Shao Q, Peng G. 2020. Exhaustion and senescence: two crucial dysfunctional states of T cells in the tumor microenvironment. Cell Mol Immunol. 17(1):27–35.