Mitochondrial DNA damage in the hair bulb: can it be used as a noninvasive biomarker of local exposure to low LET ionizing radiation?

References

• Ackerman AB, Böer A, Bennin B, Gottlieb GJ. 2005. Histologic diagnosis of inflammatory skin diseases: an algorithmic method based on pattern analysis. 3rd ed. New York: Ardor Scribendi.
   Google Scholar
• Anderson S, Bankier AT, Barrell BG, de Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, et al. 1981. Sequence and organization of the human mitochondrial genome. Nature. 290:457–465.
   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
• Barquinero JF, Beinke C, Borràs M, Buraczewska I, Darroudi F, Gregoire E, Hristova R, Kulka U, Lindholm C, Moreno M, et al. 2017. RENEB biodosimetry intercomparison analyzing translocations by FISH. Int J Radiat Biol. 93:30–35.
   PubMed Web of Science ®Google Scholar
• Bodó E, Tobin DJ, Kamenisch Y, Bíró T, Berneburg M, Funk W, Paus R. 2007. Dissecting the impact of chemotherapy on the human hair follicle: a pragmatic in vitro assay for studying the pathogenesis and potential management of hair follicle dystrophy. Am J Pathol. 171:1153–1167.
   PubMed Web of Science ®Google Scholar
• Castro MDR, Suarez E, Kraiselburd E, Isidro A, Paz J, Ferder L, Ayala-Torres S. 2012. Aging increases mitochondrial DNA damage and oxidative stress in liver of rhesus monkeys. Exp Gerontol. 47:29–37.
   PubMed Web of Science ®Google Scholar
• Chen T, He J, Shen L, Fang H, Nie H, Jin T, Wei X, Xin Y, Jiang Y, Li H, et al. 2011. The mitochondrial DNA 4,977-bp deletion and its implication in copy number alteration in colorectal cancer. BMC Med Genet. 12:8.
   PubMed Web of Science ®Google Scholar
• Chimienti G, Pesce V, Fracasso F, Russo F, de Souza-Pinto NC, Bohr VA, Lezza A. 2019. Deletion of OGG1 results in a differential signature of oxidized purine base damage in mtDNA regions. Int J Mol Sci. 20:3302.
   Web of Science ®Google Scholar
• Chow DC, Rothman S, Lorincz AL, Malkinson F, Sandburg A. 1964. Reduction in rate of growth of hair in mice as an indicator of exposure to chronic low dosage ionizing radiation. Nature. 203:847–848.
   PubMed Web of Science ®Google Scholar
• Cortopassi GA, Shibata D, Soong NW, Arnheim N. 1992. A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proc Natl Acad Sci U S A. 89:7370–7374.
   PubMed Web of Science ®Google Scholar
• Dai JG, Xiao YB, Min JX, Zhang GQ, Yao K, Zhou RJ. 2006. Mitochondrial DNA 4977 bp deletion mutations in lung carcinoma. Indian J Cancer. 43:20–25.
   PubMed Web of Science ®Google Scholar
• Dayal D, Martin SM, Owens KM, Aykin-Burns N, Zhu Y, Boominathan A, Pain D, Limoli CL, Goswami PC, Domann FE, et al. 2009. Mitochondrial complex II dysfunction can contribute significantly to genomic instability after exposure to ionizing radiation. Radiat Res. 172:737–745.
   PubMed Web of Science ®Google Scholar
• Druzhyna NM, Wilson GL, LeDoux SP. 2008. Mitochondrial DNA repair in aging and disease. Mech Ageing Dev. 129:383–390.
   PubMed Web of Science ®Google Scholar
• Du ZD, He L, Tu C, Guo XA, Yu S, Liu K, Gong S. 2019. Mitochondrial DNA 3,860-bp deletion increases with aging in the auditory nervous system of C57BL/6J mice. ORL J Otorhinolaryngol Relat Spec. 81:92–100.
   PubMed Web of Science ®Google Scholar
• Edwards AA. 1997. The use of chromosomal aberrations in human lymphocytes for biological dosimetry. Radiat Res. 148:S39–S44.
   PubMed Web of Science ®Google Scholar
• Edwards JG. 2009. Quantification of mitochondrial DNA (mtDNA) damage and error rates by real-time QPCR. Mitochondrion. 9:31–35.
   PubMed Web of Science ®Google Scholar
• Fischer H, Szabo S, Scherz J, Jaeger K, Rossiter H, Buchberger M, Ghannadan M, Hermann M, Theussl HC, Tobin DJ, et al. 2011. Essential role of the keratinocyte-specific endonuclease DNase1L2 in the removal of nuclear DNA from hair and nails. J Invest Dermatol. 131:1208–1215.
   PubMed Web of Science ®Google Scholar
• Friedland W, Schmitt E, Kundrát P, Baiocco G, Ottolenghi A. 2019. Track-structure simulations of energy deposition patterns to mitochondria and damage to their DNA. Int J Radiat Biol. 95:3–11.
   PubMed Web of Science ®Google Scholar
• Geng L, Potten CS. 1990. Changes after irradiation in the number of mitotic cells and apoptotic fragments in growing mouse hair follicles and in the width of their hairs. Rad Res. 123:75–81.
   PubMed Web of Science ®Google Scholar
• Holt IJ, Harding AE, Morgan-Hughes JA. 1989. Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies: sequence analysis and possible mechanisms. Nucl Acids Res. 17:4465–4469.
   PubMed Web of Science ®Google Scholar
• Hunter SE, Jung D, Di Giulio RT, Meyer JN. 2010. The QPCR assay for analysis of mitochondrial DNA damage, repair, and relative copy number. Methods. 51:444–451.
   PubMed Web of Science ®Google Scholar
• Karachristou I, Karakosta M, Pantelias A, Hatzi VI, Karaiskos P, Dimitriou P, Pantelias G, Terzoudi GI. 2015. Triage biodosimetry using centromeric/telomeric PNA probes and Giemsa staining to score dicentrics or excess fragments in non-stimulated lymphocyte prematurely condensed chromosomes. Mutat Res Genet Toxicol Environ Mutagen. 793:107–114.
   PubMed Web of Science ®Google Scholar
• Kazachkova N, Ramos A, Santos C, Lima M. 2013. Mitochondrial DNA damage patterns and aging: revising the evidences for humans and mice. Aging Dis. 4:337–350.
   PubMed Web of Science ®Google Scholar
• Kligman AM. 1959. The human hair cycle. J Invest Dermatol. 33:307–316.
   PubMed Web of Science ®Google Scholar
• Koch H, Wittern KP, Bergemann J. 2001. In human keratinocytes the common deletion reflects donor variabilities rather than chronologic aging and can be induced by ultraviolet A irradiation. J Invest Dermatol. 117:892–897.
   PubMed Web of Science ®Google Scholar
• Larsen NB, Rasmussen M, Rasmussen LJ. 2005. Nuclear and mitochondrial DNA repair: similar pathways? Mitochondrion. 5:89–108.
   PubMed Web of Science ®Google Scholar
• Lee HC, Pang CY, Hsu HS, Wei YH. 1994. Differential accumulation of 4,977 bp deletion in mitochondrial DNA of various tissues in human ageing. Biochim Biophys Acta. 1226:37–43.
   PubMed Web of Science ®Google Scholar
• Lefkowitz GK, Mukhopadhyay A, Cowing-Zitron C, Benjamin DY. 2011. The post-apoptotic fate of RNAs identified through high-throughput sequencing of human hair. PLoS One. 6:e27603.
   PubMed Web of Science ®Google Scholar
• Lehle S, Hildebrand DG, Merz B, Malak PN, Becker MS, Schmezer P, Essmann F, Schulze-Osthoff K, Rothfuss O. 2014. LORD-Q: a long-run real-time PCR-based DNA-damage quantification method for nuclear and mitochondrial genome analysis. Nucleic Acids Res. 42:e41–e41.
   PubMed Web of Science ®Google Scholar
• Liu CS, Kao SH, Wei YH. 1997. Smoking-associated mitochondrial DNA mutations in human hair follicles. Environ Mol Mutagen. 30:47–55.
   PubMed Web of Science ®Google Scholar
• Liu CS, Ko LY, Lim PS, Kao SH, Wei YH. 2001. Biomarkers of DNA damage in patients with end‐stage renal disease: mitochondrial DNA mutation in hair follicles. Nephrol Dial Transplant. 16:561–565.
   PubMed Web of Science ®Google Scholar
• Lu Z, Fischer TW, Hasse S, Sugawara K, Kamenisch Y, Krengel S, Funk W, Berneburg M, Paus R. 2009. Profiling the response of human hair follicles to ultraviolet radiation. J Invest Dermatol. 129:1790–1804.
   PubMed Web of Science ®Google Scholar
• Malkinson FD, Keane JT. 1981. Radiobiology of the skin: review of some effects on epidermis and hair. J Invest Dermatol. 77:133–138.
   PubMed Web of Science ®Google Scholar
• Mansouri A, Gaou I, de Kerguenec C, Amsellem S, Haouzi D, Berson A, Moreau A, Feldmann G, Lettéron P, Pessayre D, et al. 1999. An alcoholic binge causes massive degradation of hepatic mitochondrial DNA in mice. Gastroenterology. 117:181–190.
   PubMed Web of Science ®Google Scholar
• May A, Bohr VA. 2000. Gene-specific repair of γ-ray-induced DNA strand breaks in colon cancer cells: no coupling to transcription and no removal from the mitochondrial genome. Biochem Biophys Res Commun. 269:433–437.
   PubMed Web of Science ®Google Scholar
• McCall CA, Cohen JJ. 1991. Programmed cell death in terminally differentiating keratinocytes: role of endogenous endonuclease. J Invest Dermatol. 97:111–114.
   PubMed Web of Science ®Google Scholar
• Mita S, Rizzuto R, Moraes CT, Shanske S, Arnaudo E, Fabrizi GM, Koga Y, DiMauro S, Schon EA. 1990. Recombination via flanking direct repeats is a major cause of large-scale deletions of human mitochondrial DNA. Nucl Acids Res. 18:561–567.
   PubMed Web of Science ®Google Scholar
• Müller-Röver S, Handjiski B, van der Veen C, Eichmüller S, Foitzik K, McKay IA, Stenn KS, Paus R. 2001. A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol. 117:3–15.
   PubMed Web of Science ®Google Scholar
• Oestreicher U, Samaga D, Ainsbury E, Antunes AC, Baeyens A, Barrios L, Beinke C, Beukes P, Blakely WF, Cucu A, et al. 2017. RENEB intercomparisons applying the conventional Dicentric Chromosome Assay (DCA). Int J Radiat Biol. 93:20–29.
   PubMed Web of Science ®Google Scholar
• Ozawa T, Tanaka M, Ikebe S, Ohno K, Kondo T, Mizuno Y. 1990. Quantitative determination of deleted mitochondrial DNA relative to normal DNA in parkinsonian striatum by a kinetic PCR analysis. Biochem Biophys Res Commun. 172:483–489.
   PubMed Web of Science ®Google Scholar
• Partridge M A, Huang S X.L, Hernandez-Rosa E, Davidson M M, Hei T K. 2007. Arsenic induced mitochondrial DNA damage and altered mitochondrial oxidative function: implications for genotoxic mechanisms in mammalian cells. Cancer Res. 67:5239–5247.
   PubMed Web of Science ®Google Scholar
• Paus R. 1998. Principles of hair cycle control. J Dermatol. 25:793–802.
   PubMedGoogle Scholar
• Paus R, Cotsarelis G. 1999. The biology of hair follicles. N Engl J Med. 341:491–497.
   PubMed Web of Science ®Google Scholar
• Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45–e45.
   PubMed Web of Science ®Google Scholar
• Poeggeler B, Bodó E, Nadrowitz R, Dunst J, Paus R. 2010. A simple assay for the study of human hair follicle damage induced by ionizing irradiation. Exp Dermatol. 19:e306–e309.
   PubMed Web of Science ®Google Scholar
• Porter RM. 2003. Mouse models for human hair loss disorders. J Anat. 202:125–131.
   PubMed Web of Science ®Google Scholar
• Potten CS. 1985. Cell death (apoptosis) in hair follicles and consequent changes in the width of hairs after irradiation of growing follicles. Int J Radiat Biol. 48:349–360.
   Web of Science ®Google Scholar
• Prithivirajsingh S, Story MD, Bergh SA, Geara FB, Ang KK, Ismail SM, Stevens CW, Buchholz TA, Brock WA. 2004. Accumulation of the common mitochondrial DNA deletion induced by ionizing radiation. FEBS Lett. 571:227–232.
   PubMed Web of Science ®Google Scholar
• Redon CE, Nakamura AJ, Gouliaeva K, Rahman A, Blakely WF, Bonner WM. 2010. The use of gamma-H2AX as a biodosimeter for total-body radiation exposure in non-human primates. PLoS One. 5:e15544.
   PubMed Web of Science ®Google Scholar
• Reisz JA, Bansal N, Qian J, Zhao W, Furdui CM. 2014. Effects of ionizing radiation on biological molecules – mechanisms of damage and emerging methods of detection. Antiox Redox Signal. 21:260–292.
   PubMed Web of Science ®Google Scholar
• Richter C, Park JW, Ames BN. 1988. Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proc Natl Acad Sci U S A. 85:6465–6467.
   PubMed Web of Science ®Google Scholar
• Rogounovitch TI, Saenko VA, Shimizu-Yoshida Y, Abrosimov AY, Lushnikov EF, Roumiantsev PO, Ohtsuru A, Namba H, Tsyb AF, Yamashita S. 2002. Large deletions in mitochondrial DNA in radiation-associated human thyroid tumors. Cancer Res. 62:7031–7041.
   PubMed Web of Science ®Google Scholar
• Rothfuss O, Gasser T, Patenge N. 2010. Analysis of differential DNA damage in the mitochondrial genome employing a semi-long run real-time PCR approach. Nucleic Acids Res. 38:e24.
   PubMed Web of Science ®Google Scholar
• Santos JH, Meyer JN, Mandavilli BS, Van Houten B. 2006. Quantitative PCR-based measurement of nuclear and mitochondrial DNA damage and repair in mammalian cells. Methods Mol Biol. 314:183–199.
   PubMedGoogle Scholar
• Satoh M, Kuroiwa T. 1991. Organization of multiple nucleoids and DNA molecules in mitochondria of a human cell. Exp Cell Res. 196:137–140.
   PubMed Web of Science ®Google Scholar
• Schilling-Tóth B. 2015. Az ionizáló sugárzás indukált molekuláris változások vizsgálata normál fibroblasztokban és tumor sejtekben [Analysis of the ionising radiation-induced molecular changes in normal fibroblasts and tumor cells] [PhD dissertation]. Budapest: Semmelweis University. Hungarian.
   Google Scholar
• Schilling-Tóth B, Sándor N, Kis E, Kadhim M, Sáfrány G, Hegyesi H. 2011. Analysis of the common deletions in the mitochondrial DNA is a sensitive biomarker detecting direct and non-targeted cellular effects of low dose ionizing radiation. Mutat Res. 716:33–39.
   PubMed Web of Science ®Google Scholar
• Schneider MR, Schmidt-Ullrich R, Paus R. 2009. The hair follicle as a dynamic miniorgan. Curr Biol. 19:R132–R142.
   PubMed Web of Science ®Google Scholar
• Schon EA, Rizzuto R, Moraes CT, Nakase H, Zeviani M, DiMauro S. 1989. A direct repeat is a hotspot for large-scale deletion of human mitochondrial DNA. Science. 244:346–349.
   PubMed Web of Science ®Google Scholar
• Seol MA, Jung U, Eom HS, Kim SH, Park HR, Jo SK. 2012. Prolonged expression of senescence markers in mice exposed to gamma-irradiation. J Vet Sci. 13:331–338.
   PubMed Web of Science ®Google Scholar
• Suzuki K, Ojima M, Kodama S, Watanabe M. 2003. Radiation-induced DNA damage and delayed induced genomic instability. Oncogene. 22:6988–6993.
   PubMed Web of Science ®Google Scholar
• Taneja N, Tjalkens R, Philbert MA, Rehemtulla A. 2001. Irradiation of mitochondria initiates apoptosis in a cell free system. Oncogene. 20:167–177.
   PubMed Web of Science ®Google Scholar
• Tanhauser SM, Laipis PJ. 1995. Multiple deletions are detectable in mitochondrial DNA of aging mice. J Biol Chem. 270:24769–24775.
   PubMed Web of Science ®Google Scholar
• Tochio T, Tanaka H, Nakata S, Yoshizato K. 2011. Presence of amplified mRNA in acellular hair shafts: utilization to analyze gene expression profiles of black and white hairs. Int J Dermatol. 50:530–534.
   PubMed Web of Science ®Google Scholar
• Vral A, Fenech M, Thierens H. 2011. The micronucleus assay as a biological dosimeter of in vivo ionising radiation exposure. Mutagenesis. 26:11–17.
   PubMed Web of Science ®Google Scholar
• Wang B, Yang W, McKittrick J, Meyers MA. 2016. Keratin: structure, mechanical properties, occurrence in biological organisms, and efforts at bioinspiration. Prog Mat Sci. 76:229–318.
   Web of Science ®Google Scholar
• Wang L, Kuwahara Y, Li L, Baba T, Shin RW, Ohkubo Y, Ono K, Fukumoto M. 2007. Analysis of Common Deletion (CD) and a novel deletion of mitochondrial DNA induced by ionizing radiation. Int J Radiat Biol. 93:433–442.
   Google Scholar
• Williams AW. 1906. A note on certain appearances of X-rayed hairs. Br J Dermatol. 18:63–65.
   Google Scholar
• Wilson MR, Polanskey D, Butler J, DiZinno JA, Replogle J, Budowle B. 1995. Extraction, PCR amplification and sequencing of mitochondrial DNA from human hair shafts. Biotechniques. 18:662–669.
   PubMed Web of Science ®Google Scholar
• Wojcik A, Oestreicher U, Barrios L, Vral A, Terzoudi G, Ainsbury E, Rothkamm K, Trompier F, Kulka U. 2017. The RENEB operational basis: complement of established biodosimetric assays. Int J Radiat Biol. 93:15–19.
   PubMed Web of Science ®Google Scholar
• Wu L, Sun Y, Hu YJ, Yang Y, Yao LL, Zhou XX, Wang H, Zhang R, Huang X, Kong WJ. 2012. Increased p66Shc in the inner ear of D-galactose-induced aging mice with accumulation of mitochondrial DNA 3873-bp deletion: p66Shc and mtDNA damage in the inner ear during aging. PLoS One. 7:e50483.
   PubMed Web of Science ®Google Scholar
• Zeviani M, Moraes CT, DiMauro S, Nakase H, Bonilla E, Schon EA, Rowland LP. 1988. Deletions of mitochondrial DNA in Kerns-Sayre syndrome. Neurology. 38:1339–1346.
   PubMed Web of Science ®Google Scholar
• Zhang S B, Maguire D, Zhang M, Zhang Z, Zhang A, Yin L, Zhang L, Huang L, Vidyasagar S, Swarts S, et al. 2013. The murine common deletion: mitochondrial DNA 3,860-bp deletion after irradiation. Rad Res. 180:407–413.
   PubMed Web of Science ®Google Scholar
• Zhao XT, Feng JB, Li YW, Luo Q, Yang XC, Lu X, Chen DQ, Liu QJ. 2012. Identification of two novel mitochondrial DNA deletions induced by ionizing radiation. Biomed Environ Sci. 25:533–541.
   PubMed Web of Science ®Google Scholar
• Zheng Y, Luo X, Zhu J, Zhang X, Zhu Y, Cheng H, Xia Z, Su N, Zhang N, Zhou J. 2012. Mitochondrial DNA 4977 bp deletion is a common phenomenon in hair and increases with age. Bosn J Basic Med Sci. 12:187–192.
   PubMed Web of Science ®Google Scholar
• Zhou X, Li N, Wang Y, Wang Y, Zhang X, Zhang H. 2011. Effects of X-irradiation on mitochondrial DNA damage and its supercoiling formation change. Mitochondrion. 11:886–892.
   PubMed Web of Science ®Google Scholar