Significance of the Wnt canonical pathway in radiotoxicity via oxidative stress of electron beam radiation and its molecular control in mice

References

• Aebi H. 1974. Catalase. In: HU Berger methods of enzymatic analysis. Vol. 3. Weinhein: Verlag Chemie; p. 273–286.
   Google Scholar
• Akyol MU, Yalçiner EG, Doğan AI. 2001. Pyogenic granuloma (lobular capillary hemangioma) of the tongue. Int J Pediatr Otorhinolaryngol. 58(3):239–241.
   PubMed Web of Science ®Google Scholar
• Andersen JK. 2004. Oxidative stress in neurodegeneration: cause or consequences? Nat Med. 10(S7):S18–S25.
   PubMed Web of Science ®Google Scholar
• Arnon J, Meirow D, Lewis-Roness H, Ornoy A. 2001. Genetic and teratogenic effects of cancer treatments on gametes and embryos. Hum Reprod Update. 7(4):394–403.
   PubMed Web of Science ®Google Scholar
• Bhanja P, Saha S, Kabarriti R, Liu L, Roy-Chowdhury N, Roy-Chowdhury J, Sellers RS, Alfieri AA, Guha C. 2009. Protective role of R-spondin1, an intestinal stem cell growth factor, against radiation-induced gastrointestinal syndrome in mice. PLoS One. 4(11):e8014.
   PubMed Web of Science ®Google Scholar
• Bhatia AL, Manda K. 2004. Study on pre-treatment of melatonin against radiation-induced oxidative stress in mice. Environ Toxicol Pharmacol. 18(1):13–20.
   PubMed Web of Science ®Google Scholar
• Bonner JA, Harari PM, Giralt J, Azarnia N, Shin DM, Cohen RB, Jones CU, Sur R, Raben D, Jassem J, et al. 2006. Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N Engl J Med. 354(6):567–578.
   PubMed Web of Science ®Google Scholar
• Boudaïffa B, Cloutier P, Hunting D, Huels MA, Sanche L. 2000. Resonant formation of DNA strand breaks by low-energy (3 to 20 eV) electrons. Science. 287(5458):1658–1660.
   PubMed Web of Science ®Google Scholar
• Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. 2005. Migrating cancer stem cells—an integrated concept of malignant tumour progression. Nat Rev Cancer. 5(9):744–749.
   PubMed Web of Science ®Google Scholar
• Bristow RG, Ozcelik H, Jalali F, Chan N, Vesprini D. 2007. Homologous recombination and prostate cancer: a model for novel DNA repair targets and therapies. Radiother Oncol. 83(3):220–230.
   PubMed Web of Science ®Google Scholar
• Budinger GS, Tso M, McClintock DS, Dean DA, Sznajder JI, Chandel NS. 2002. Hyperoxia-induced apoptosis does not require mitochondrial reactive oxygen species and is regulated by Bcl-2 proteins. J Biol Chem. 277(18):15654–15660.
   PubMed Web of Science ®Google Scholar
• Chang YF, Lee-Chang JS, Panneerdoss S, MacLean JA II, Rao MK. 2011. Isolation of Sertoli, Leydig, and spermatogenic cells from the mouse testis. Biotechniques. 51(5):341–344.
   PubMed Web of Science ®Google Scholar
• Chen MS, Woodward WA, Behbod F, Peddibhotla S, Alfaro MP, Buchholz TA, Rosen JM. 2007. Wnt/β-Catenin mediates radiation resistance of Sca1+ progenitors in an immortalized mammary gland cell line. J Cell Sci. 120(Pt 3):468–477.
   PubMed Web of Science ®Google Scholar
• Chen S, Guttridge DC, You Z, Zhang Z, Fribley A, Mayo MW, Kitajewski J, Wang CY. 2001. Wnt-1 signaling inhibits apoptosis by activating β-Catenin/T cell factor-mediated transcription. J Cell Biol. 152(1):87–96.
   PubMed Web of Science ®Google Scholar
• Chipuk JE, Green DR. 2008. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol. 18(4):157–164.
   PubMed Web of Science ®Google Scholar
• Choi J, Southworth LK, Sarin KY, Venteicher AS, Ma W, Chang W, Cheung P, Jun S, Artandi MK, Shah N, et al. 2008. TERT promotes epithelial proliferation through transcriptional control of a Myc- and Wnt-related developmental program. PLOS Genet. 4(1):e10.
   PubMed Web of Science ®Google Scholar
• Choi YS, Zhang Y, Xu M, Yang Y, Ito M, Peng T, Cui Z, Nagy A, Hadjantonakis A-K, Lang RA, et al. 2013. Distinct functions for Wnt/β-Catenin in hair follicle stem cell proliferation and survival and interfollicular epidermal homeostasis. Cell Stem Cell. 13(6):720–733.
   PubMed Web of Science ®Google Scholar
• Cross CE, Halliwell B, Borish ET, Pryor WA, Ames BN, Saul RL, McCord JM, Harman D. 1987. Oxygen radicals and human disease. Ann Intern Med. 107(4):526–545.
   PubMed Web of Science ®Google Scholar
• Cselenyi CS, Jernigan KK, Tahinci E, Thorne CA, Lee LA, Lee E. 2008. LRP6 transduces a canonical Wnt signal independently of Axin degradation by inhibiting GSK3's phosphorylation of β-Catenin. Proc Natl Acad Sci USA. 105(23):8032–8037.
   PubMed Web of Science ®Google Scholar
• Damalas A, Ben-Ze'ev A, Simcha I, Shtutman M, Leal JF, Zhurinsky J, Geiger B, Oren M. 1999. Excess beta-Catenin promotes accumulation of transcriptionally active p53. EMBO J. 18(11):3054–3063.
   PubMed Web of Science ®Google Scholar
• Das K, Samanta L, Chainy GBN. 2000. A modified spectrophotometric assay of superoxide dismutase using nitrite formation by superoxide radicals.
   Google Scholar
• Davis AJ, Chen DJ. 2013. DNA double-strand break repair via non-homologous end-joining. Transl Cancer Res. 2(3):130–143.
   PubMed Web of Science ®Google Scholar
• Dym M, Clermont Y. 1970. Role of spermatogonia in the repair of the seminiferous epithelium following X‐irradiation of the rat testis. Dev Dyn. 128(3):265–281.
   Google Scholar
• Fevr T, Robine S, Louvard D, Huelsken J. 2007. Wnt/betaCatenin is essential for intestinal homeostasis and maintenance of intestinal stem cells. Mol Cell Biol. 27(21):7551–7559.
   PubMed Web of Science ®Google Scholar
• Garg H, Suri P, Gupta JC, Talwar GP, Dubey S. 2016. Survivin: a unique target for tumor therapy. Cancer Cell Int. 16(1):49.
   PubMedGoogle Scholar
• Good JS, Harrington KJ. 2013. The hallmarks of cancer and the radiation oncologist: updating the 5Rs of radiobiology. Clin Oncol. 25(10):569–577.
   Web of Science ®Google Scholar
• Hai B, Yang Z, Shangguan L, Zhao Y, Boyer A, Liu F. 2012. Concurrent transient activation of Wnt/β-Catenin pathway prevents radiation damage to salivary glands. Int J Radiat Oncol Biol Phys. 83(1):e109–e116.
   PubMed Web of Science ®Google Scholar
• He B, Reguart N, You L, Mazieres J, Xu Z, Lee AY, Mikami I, McCormick F, Jablons DM. 2005. Blockade of Wnt-1 signaling induces apoptosis in human colorectal cancer cells containing downstream mutations. Oncogene. 24(18):3054–3058.
   PubMed Web of Science ®Google Scholar
• Her J, Bunting SF. 2018. How cells ensure correct repair of DNA double-strand breaks. J Biol Chem. 293(27):10502–10511.
   PubMed Web of Science ®Google Scholar
• Huang GJ, Sheu MJ, Chen HJ, Chang YS, Lin YH. 2007. Inhibition of reactive nitrogen species in vitro and ex vivo by trypsin inhibitor from sweet potato ‘Tainong 57’ storage roots. J Agric Food Chem. 55(15):6000–6006.
   PubMed Web of Science ®Google Scholar
• Jackson SP, Bartek J. 2009. The DNA-damage response in human biology and disease. Nature. 461(7267):1071–1078.
   PubMed Web of Science ®Google Scholar
• Jagetia GC, Baliga MS. 2004. The evaluation of nitric oxide scavenging activity of certain Indian medicinal plants in vitro: a preliminary study. J Med Food. 7(3):343–348.
   PubMed Web of Science ®Google Scholar
• Jamieson CH, Weissman IL, Passegué E. 2004. Chronic versus acute myelogenous leukemia: a question of self-renewal. Cancer Cell. 6(6):531–533.
   PubMed Web of Science ®Google Scholar
• Jin Y, Nie D, Li J, Du X, Lu Y, Li Y, Liu C, Zhou J, Pan J. 2017. Gas6/AXL signaling regulates self-renewal of chronic myelogenous leukemia stem cells by stabilizing β-Catenin. Clin Cancer Res. 23(11):2842–2855.
   PubMed Web of Science ®Google Scholar
• Johansson J, Naszai M, Hodder MC, Pickering KA, Miller BW, Ridgway RA, Yu Y, Peschard P, Brachmann S, Campbell AD, et al. 2019. RAL GTPases drive intestinal stem cell function and regeneration through internalization of Wnt signalosomes. Cell Stem Cell. 24(4):592–607.e7.
   PubMed Web of Science ®Google Scholar
• Kalita B, Ranjan R, Gupta ML. 2019. Combination treatment of podophyllotoxin and rutin promotes mouse Lgr5(+ve) intestinal stem cells survival against lethal radiation injury through Wnt signaling. Apoptosis. 24(3–4):326–340.
   PubMed Web of Science ®Google Scholar
• Kangasniemi M, Huhtaniemi I, Meistrich ML. 1996. Failure of spermatogenesis to recover despite the presence of aspermatogonia in the irradiated LBNF1 rat. Biol Reprod. 54(6):1200–1208.
   PubMed Web of Science ®Google Scholar
• Kramer GF, Norman HA, Krizek DT, Mirecki RM. 1991. Influence of UV-B radiation on polyamines, lipid peroxidation and membrane lipids in cucumber. Phytochemistry. 30(7):2101–2108.
   Web of Science ®Google Scholar
• Lento W, Ito T, Zhao C, Harris JR, Huang W, Jiang C, Owzar K, Piryani S, Racioppi L, Chao N, et al. 2014. Loss of beta-Catenin triggers oxidative stress and impairs hematopoietic regeneration. Genes Dev. 28(9):995–1004.
   PubMed Web of Science ®Google Scholar
• Liu J, Doty T, Gibson B, Heyer WD. 2010. Human BRCA2 protein promotes RAD51 filament formation on RPA-covered single-stranded DNA. Nat Struct Mol Biol. 17(10):1260–1262.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2 − ΔΔCT method. methods. 25(4):402–408.
   PubMed Web of Science ®Google Scholar
• Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. J Biol Chem. 193(1):265–275.
   PubMed Web of Science ®Google Scholar
• Lundin A, Driscoll B. 2013. Lung cancer stem cells: progress and prospects. Cancer Lett. 338(1):89–93.
   PubMed Web of Science ®Google Scholar
• Meneghini R. 1997. Iron homeostasis, oxidative stress, and DNA damage. Free Radic Biol Med. 23(5):783–792.
   PubMed Web of Science ®Google Scholar
• Metcalfe C, Kljavin NM, Ybarra R, de Sauvage FJ. 2014. Lgr5+ stem cells are indispensable for radiation-induced intestinal regeneration. Cell Stem Cell. 14(2):149–159.
   PubMed Web of Science ®Google Scholar
• Miao C-G, Yang Y-Y, He X, Huang C, Huang Y, Qin D, Du C-L, Li J. 2014. MicroRNA-152 modulates the canonical Wnt pathway activation by targeting DNA methyltransferase 1 in arthritic rat model. Biochimie. 106:149–156.
   PubMed Web of Science ®Google Scholar
• Mishra L, Shetty K, Tang Y, Stuart A, Byers SW. 2005. The role of TGF-β and Wnt signaling in gastrointestinal stem cells and cancer. Oncogene. 24(37):5775–5789.
   PubMed Web of Science ®Google Scholar
• Molinolo AA, Amornphimoltham P, Squarize CH, Castilho RM, Patel V, Gutkind JS. 2009. Dysregulated molecular networks in head and neck carcinogenesis. Oral Oncol. 45(4–5):324–334.
   PubMed Web of Science ®Google Scholar
• Mügge A. 1998. The role of reactive oxygen species in atherosclerosis. Z Kardiol. 87(11):851–864.
   PubMedGoogle Scholar
• Ohkawa H, Ohishi N, Yagi K. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 95(2):351–358.
   PubMed Web of Science ®Google Scholar
• Paravicini TM, Touyz RM. 2006. Redox signaling in hypertension. Cardiovasc Res. 71(2):247–258.
   PubMed Web of Science ®Google Scholar
• Rattis FM, Voermans C, Reya T. 2004. Wnt signaling in the stem cell niche. Curr Opin Hematol. 11(2):88–94.
   PubMed Web of Science ®Google Scholar
• Regoli F, Winston GW. 1998. Applications of a new method for measuring the total oxyradical scavenging capacity in marine invertebrates. Mar Environ Res. 46(1–5):439–442.
   Web of Science ®Google Scholar
• Reya T, Clevers H. 2005. Wnt signalling in stem cells and cancer. Nature. 434(7035):843–850.
   PubMed Web of Science ®Google Scholar
• Riley PA. 1994. Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int J Radiat Biol. 65(1):27–33.
   PubMed Web of Science ®Google Scholar
• Rosen JM, Chen MS. 2006. Beta-catenin: a potential survival marker of breast cancer stem cells. Houston (TX): Baylor College of Medicine.
   Google Scholar
• Sanchez-Moreno C. 2002. Methods used to evaluate the free radical scavenging activity in foods and biological systems. Food Sci Technol Int. 8(3):121–137.
   Web of Science ®Google Scholar
• Sebastian-Leon P, Vidal E, Minguez P, Conesa A, Tarazona S, Amadoz A, Armero C, Salavert F, Vidal-Puig A, Montaner D, et al. 2014. Understanding disease mechanisms with models of signaling pathway activities. BMC Syst Biol. 8(1):1–19.
   PubMedGoogle Scholar
• Simms D, Cizdziel PE, Chomczynski P. 1993. TRIzol: A new reagent for optimal single-step isolation of RNA. Focus. 15(4):532–535.
   Google Scholar
• Steinhusen U, Badock V, Bauer A, Behrens J, Wittman-Liebold B, Dörken B, Bommert K. 2000. Apoptosis-induced cleavage of β-Catenin by caspase-3 results in proteolytic fragments with reduced transactivation potential. J Biol Chem. 275(21):16345–16353.
   PubMed Web of Science ®Google Scholar
• Thornalley PJ, Vašák M. 1985. Possible role for metallothionein in protection against radiation-induced oxidative stress. Kinetics and mechanism of its reaction with superoxide and hydroxyl radicals. Biochim Biophys Acta. 827(1):36–44.
   PubMed Web of Science ®Google Scholar
• Thotala DK, Geng L, Dickey AK, Hallahan DE, Yazlovitskaya EM. 2010. A new class of molecular targeted radioprotectors: GSK-3β inhibitors. Int J Radiat Oncol Biol Phys. 76(2):557–565.
   PubMed Web of Science ®Google Scholar
• van der Meer Y, Huiskamp R, Davids JAG, van der Tweel I, de Rooij DG, Huiskamp R. 1992. The sensitivity to X rays of mouse spermatogonia that are committed to differentiate and of differentiating spermatogonia. Radiat Res. 130(3):296–302.
   PubMed Web of Science ®Google Scholar
• Wang J, Wynshaw-Boris A. 2004. The canonical Wnt pathway in early mammalian embryogenesis and stem cell maintenance/differentiation. Curr Opin Genet Dev. 14(5):533–539.
   PubMed Web of Science ®Google Scholar
• Weydert CJ, Cullen JJ. 2010. Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nat Protoc. 5(1):51–66.
   PubMed Web of Science ®Google Scholar
• Xu M, Yu Q, Subrahmanyam R, Difilippantonio MJ, Ried T, Sen JM. 2008. Beta-Catenin expression results in p53-independent DNA damage and oncogene-induced senescence in prelymphomagenicthymocytes in vivo. Mol Cell Biol. 28(5):1713–1723.
   PubMed Web of Science ®Google Scholar
• Zhang P, Wei Y, Wang L, Debeb BG, Yuan Y, Zhang J, Yuan J, Wang M, Chen D, Sun Y, et al. 2014. ATM-mediated stabilization of ZEB1 promotes DNA.
   Google Scholar
• Zhang DY, Wang HJ, Tan YZ. 2011. Wnt/beta-Catenin signaling induces the aging of mesenchymal stem cells through the DNA damage response and the p53/p21 pathway. PLOS One. 6(6):e21397.
   PubMed Web of Science ®Google Scholar
• Zhang L, Zhou F, Li Y, Drabsch Y, Zhang J, van Dam H, ten Dijke P. 2012. Fas-associated factor 1 is a scaffold protein that promotes β-transducin repeat-containing protein (β-TCP)-mediated β-Catenin ubiquitination and degradation. J Biol Chem. 287(36):30701–30710.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Tao L, Yi J, Song H, Chen L. 2018. The role of canonical Wnt signaling in regulating radioresistance. Cell Physiol Biochem. 48(2):419–432.
   PubMedGoogle Scholar