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Effect of heat stress on DNA damage: a systematic literature review

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Abstract

Thermal stress has a direct effect on various types of DNA damage, which depends on the stage of the cell cycle when the cell is exposed to different climate conditions. A literature review was conducted to systematically investigate and assess the overall effect of heat stress and DNA damage following heat exposure. In this study, electronic databases including PubMed, Scopus, and Web of Science were searched to find relevant literature on DNA damage in different ambient temperatures. Outcomes included (1) measurement of DNA damage in heat exposure, (2) three different quantification methods (comet assay, 8-hydroxy-2-deoxyguanosine (8-OHdG), and γ-H2AX), and (3) protocols used for moderate (31) and high temperatures (42). The evidence shows that long exposure and very high temperature can induce an increase in DNA damage through aggregate in natural proteins, ROS generation, cell death, and reproductive damage in hot-humid and hot-dry climate conditions. A substantial increase in DNA damage occurs following acute heat stress exposure, especially in tropical and subtropical climate conditions. The results of this systematic literature review showed a positive association between thermal stress exposure and inhibition of repair of DNA damage.

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References

  • Alekseenko LL, Zemelko VI, Zenin VV, Pugovkina NA, Kozhukharova IV, Kovaleva ZV, ..., Nikolsky NN (2012a) Heat shock induces apoptosis in human embryonic stem cells but a premature senescence phenotype in their differentiated progeny. Cell Cycle 11(17):3260-3269.https://doi.org/10.4161/cc.21595

  • Beachy SH, Repasky EA (2011) Toward establishment of temperature thresholds for immunological impact of heat exposure in humans. Int J Hyperth 27(4):344–352

    Article  Google Scholar 

  • Bettaieb A, Averill-Bates DA (2015) Thermotolerance induced at a mild temperature of 40°C alleviates heat shock-induced ER stress and apoptosis in HeLa cells. Biochimica Et Biophysica Acta - Molecular Cell Research 1853(1):52–62. https://doi.org/10.1016/j.bbamcr.2014.09.016

    Article  CAS  Google Scholar 

  • Bierkens JG (2000) Applications and pitfalls of stress-proteins in biomonitoring. Toxicology 153(1–3):61–72

    Article  CAS  Google Scholar 

  • Dubrez L, Causse S, Borges Bonan N, Dumetier B, Garrido C (2020) Heat-shock proteins: chaperoning DNA repair. Oncogene 39(3):516–529. https://doi.org/10.1038/s41388-019-1016-y

    Article  CAS  Google Scholar 

  • Evans MD, Dizdaroglu M, Cooke MS (2004) Oxidative DNA damage and disease: induction, repair and significance. Mutation Research/reviews in Mutation Research 567(1):1–61

    Article  CAS  Google Scholar 

  • Feng H, Sun L, Li Y, Yang B (1998) Study on induced mutagenesis interaction of the high temperature and/or cigarette smoke. Wei sheng yan jiu= Journal of hygiene research, 27(6):379–381

  • Golbabaei F, Heydari A, Moradi G, Dehghan H, Moradi A, Habibi P (2020) The effect of cooling vests on physiological and perceptual responses: a systematic review. International J Occup Saf Ergon(just-accepted) 1–36.

  • Habibi P, Momeni R, Dehghan H (2015) Relationship of environmental, physiological, and perceptual heat stress indices in Iranian Men. International Journal of Preventive Medicine 6

  • Habibi, P., Moradi, G., Moradi, A., & Golbabaei, F. (2021a). A review on advanced functional photonic fabric for enhanced thermoregulating performance. Environmental Nanotechnology, Monitoring & Management, 100504.

  • Habibi P, Moradi G, Moradi A, Heydari A (2021b) The impacts of climate change on occupational heat strain in outdoor workers: a systematic review. Urban Climate 36:100770

    Article  Google Scholar 

  • Harrouk W, Codrington A, Vinson R, Robaire B, Hales BF (2000) Paternal exposure to cyclophosphamide induces DNA damage and alters the expression of DNA repair genes in the rat preimplantation embryo. Mutation Research/DNA Repair 461(3):229–241

    Article  CAS  Google Scholar 

  • Houston BJ, Nixon B, Martin JH, De Iuliis GN, Trigg NA, Bromfield EG, ..., Aitken RJ (2018) Heat exposure induces oxidative stress and DNA damage in the male germ line. Biol Reprod 98(4):593-606

  • Hunt CR, Pandita RK, Laszlo A, Higashikubo R, Agarwal M, Kitamura T, ..., Pandita TK (2007) Hyperthermia activates a subset of ataxia-telangiectasia mutated effectors independent of DNA strand breaks and heat shock protein 70 status. Cancer Res 67(7):3010-3017. https://doi.org/10.1158/0008-5472.can-06-4328

  • Kampinga HH, Laszlo A, Takahashi A, Mori E, Ohnishi T (2005) DNA double strand breaks do not play a role in heat-induced cell killing [1] (multiple letters). Can Res 65(22):10632–10633. https://doi.org/10.1158/0008-5472.CAN-05-0006

    Article  CAS  Google Scholar 

  • Kantidze OL, Velichko AK, Luzhin AV, Razin SV (2016) Heat Stress-Induced DNA Damage Acta Naturae 8(2):75–78. https://doi.org/10.32607/20758251-2016-8-2-75-78

    Article  CAS  Google Scholar 

  • Kjellstrom T, Lemke B, Hyatt O, Otto M (2014) Climate change and occupational health: a South African perspective. Samj South Afr Med J 104(8), 586-+. https://doi.org/10.7196/samj.8646

  • Laszlo A, Fleischer I (2009) The heat-induced-H2AX response does not play a role in hyperthermic cell killing. Int J Hyperth 25(3):199–209. https://doi.org/10.1080/02656730802631775

    Article  CAS  Google Scholar 

  • Lepock JR, Borrelli MJ (2005) How do cells respond to their thermal environment? Int J Hyperth 21(8):681–687. https://doi.org/10.1080/02656730500307298

    Article  CAS  Google Scholar 

  • Liu FW, Liu FC, Wang YR, Tsai HI, Yu HP (2015) Aloin protects skin fibroblasts from heat stress-induced oxidative stress damage by regulating the oxidative defense system. PloS one 10(12). https://doi.org/10.1371/journal.pone.0143528

  • MacLachlan TK, Sang N, Giordano A (1995) Cyclins, cyclin-dependent kinases and cdk inhibitors: implications in cell cycle control and cancer. Critical Reviews™ in Eukaryotic Gene Expression 5(2)

  • Maghsudlu M, Yazd EF (2017) Heat-induced inflammation and its role in esophageal cancer. J Dig Dis 18(8):431–444. https://doi.org/10.1111/1751-2980.12511

    Article  CAS  Google Scholar 

  • Mah L, El-Osta A, Karagiannis T (2010) γH2AX: a sensitive molecular marker of DNA damage and repair. Leukemia 24(4):679–686

    Article  CAS  Google Scholar 

  • Maroni P, Bendinelli P, Tiberio L, Rovetta F, Piccoletti R, Schiaffonati L (2003) In vivo heat-shock response in the brain: signalling pathway and transcription factor activation. Brain Res Mol Brain Res 119(1):90–99. https://doi.org/10.1016/j.molbrainres.2003.08.018

    Article  CAS  Google Scholar 

  • Milani V, Horsman M (2008) Cellular and vascular effects of hyperthermia. Int J Hyperth 24(1):1–2. https://doi.org/10.1080/02656730701858313

    Article  Google Scholar 

  • Miyagawa R, Mizuno R, Watanabe K, Ijiri K (2012) Formation of tRNA granules in the nucleus of heat-induced human cells. Biochem Biophys Res Commun 418(1):149–155. https://doi.org/10.1016/j.bbrc.2011.12.150

    Article  CAS  Google Scholar 

  • Mohammadi B, Safaiyan A, Habibi P, Moradi G (2021) Evaluation of the acoustic performance of polyurethane foams embedded with rock wool fibers at low-frequency range; design and construction. Appl Acoust 182:108223

    Article  Google Scholar 

  • Nam JW, Kim SY, Yoon T, Lee YJ, Kil YS, Lee YS, Seo EK (2013) Heat shock factor 1 inducers from the bark of Eucommia ulmoides as cytoprotective agents. Chem Biodivers 10(7):1322–1327. https://doi.org/10.1002/cbdv.201200401

    Article  CAS  Google Scholar 

  • Nasr MA, Dovbeshko GI, Bearne SL, El-Badri N, Matta CF (2019) Heat shock proteins in the “hot” mitochondrion: identity and putative roles. Bioessays 41(9). https://doi.org/10.1002/bies.201900055

  • Nezhad FS, Lavvaf A, Karimi S (2013) Influence of heat stress on DNA damage on sheep’s Sertoli cells. International Research Journal of Applied and Basic Sciences 6(10):1396–1400

    Google Scholar 

  • Paul C, Murray AA, Spears N, Saunders PT (2008) A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice. Reproduction 136(1):73–84. https://doi.org/10.1530/rep-08-0036

    Article  CAS  Google Scholar 

  • Paul C, Teng S, Saunders PT (2009) A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod 80(5):913–919. https://doi.org/10.1095/biolreprod.108.071779

    Article  CAS  Google Scholar 

  • Penã ST, Gummow B, Parker AJ, Paris DBBP (2017) Revisiting summer infertility in the pig: could heat stress-induced sperm DNA damage negatively affect early embryo development? Animal Production Science 57(10):1975–1983. https://doi.org/10.1071/AN16079

    Article  Google Scholar 

  • Peña ST, Stone F, Gummow B, Parker AJ, Paris DBBP (2019) Tropical summer induces DNA fragmentation in boar spermatozoa: implications for evaluating seasonal infertility. Reprod Fertil Dev 31(3):590–601. https://doi.org/10.1071/RD18159

    Article  CAS  Google Scholar 

  • Petrova NV, Velichko AK, Razin SV, Kantidze OL (2016) Early S-phase cell hypersensitivity to heat stress. Cell Cycle 15(3):337–344. https://doi.org/10.1080/15384101.2015.1127477

    Article  CAS  Google Scholar 

  • Prandini MN, Neves A, Lapa AJ, Stavale JN (2005) Mild hypothermia reduces polymorphonuclear leukocytes infiltration in induced brain inflammation. Arq Neuropsiquiatr 63(3B):779–784. https://doi.org/10.1590/s0004-282x2005000500012

    Article  Google Scholar 

  • Raaphorst GP, LeBlanc JM, Li LF, Yang DP (2005) Hyperthermia responses in cell lines with normal and deficient DNA repairs systems. J Therm Biol 30(6):478–484. https://doi.org/10.1016/j.jtherbio.2005.05.010

    Article  CAS  Google Scholar 

  • Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Mol Cell 40(2):253–266

    Article  CAS  Google Scholar 

  • Rockett JC, Mapp FL, Garges JB, Luft JC, Mori C, Dix DJ (2001) Effects of hyperthermia on spermatogenesis, apoptosis, gene expression, and fertility in adult male mice. Biol Reprod 65(1):229–239

    Article  CAS  Google Scholar 

  • Roti Roti JL, Pandita RK, Mueller JD, Novak P, Moros EG, Laszlo A (2010) Severe, short-duration (0–3 min) heat shocks (50–52°C) inhibit the repair of DNA damage. Int J Hyperth 26(1):67–78. https://doi.org/10.3109/02656730903417947

    Article  CAS  Google Scholar 

  • Ryabchenko NM, Rodionova NK, Sychevska IS, Muzalev II, Mykhailenko VM, Druzhina MO (2013) Genotoxic effects of radiation and hyperthermia in linear mice with different radiation sensitivity. Cytol Genet 47(1):39–43. https://doi.org/10.3103/s0095452713010088

    Article  Google Scholar 

  • Shamseer LMD, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. Bmj 2:7647

    Article  Google Scholar 

  • Sirriyeh R, Lawton R, Gardner P, Armitage G (2012) Reviewing studies with diverse designs: the development and evaluation of a new tool. J Eval Clin Pract 18(4):746–752

    Article  Google Scholar 

  • Stocker AJ, Madalena CR, Gorab E (2006) The effects of temperature shock on transcription and replication in Rhynchosciara americana (Diptera: Sciaridae). Genetica 126(3):277–290. https://doi.org/10.1007/s10709-005-7407-8

    Article  Google Scholar 

  • Tabuchi Y, Furusawa Y, Kariya A, Wada S, Ohtsuka K, Kondo T (2013) Common gene expression patterns responsive to mild temperature hyperthermia in normal human fibroblastic cells. Int J Hyperth 29(1):38–50. https://doi.org/10.3109/02656736.2012.753163

    Article  CAS  Google Scholar 

  • Tang-Chun W, Han-Zhen H, Tanguay RM, Yang W, Dai-Gen X, Currie RW, ..., Guo-gao Z (1995) The combined effects of high temperature and carbon monoxide on heat stress response. J Tongji Med Univ 15(3):178-183

  • Tramontano F, Malanga M, Farina B, Jones R, Quesada P (2000) Heat stress reduces poly (ADPR) polymerase expression in rat testis. Mol Hum Reprod 6(7):575–581

    Article  CAS  Google Scholar 

  • Van’t Veer LJ, Dai H, Van De Vijver MJ, He YD, Hart AA, Mao M, . . ., Witteveen AT (2002) Gene expression profiling predicts clinical outcome of breast cancer. Nature 415(6871): 530–536.

  • Vanos J, Vecellio DJ, Kjellstrom T (2019) Workplace heat exposure, health protection, and economic impacts: a case study in Canada. Am J Ind Med 62(12):1024–1037. https://doi.org/10.1002/ajim.22966

    Article  Google Scholar 

  • Velichko AK, Petrova NV, Kantidze OL, Razin SV (2012) Dual effect of heat shock on DNA replication and genome integrity. Mol Biol Cell 23(17):3450–3460. https://doi.org/10.1091/mbc.E11-12-1009

    Article  CAS  Google Scholar 

  • Velichko AK, Petrova NV, Razin SV, Kantidze OL (2015) Mechanism of heat stress-induced cellular senescence elucidates the exclusive vulnerability of early S-phase cells to mild genotoxic stress. Nucleic Acids Res 43(13):6309–6320. https://doi.org/10.1093/nar/gkv573

    Article  CAS  Google Scholar 

  • Venugopal V, Krishnamoorthy M, Venkatesan V, Jaganathan V, Paul S (2018) Occupational heat stress, DNA damage and heat shock protein—a review. Medical Research Archives 6(1)

  • Venugopal V, Krishnamoorthy M, Venkatesan V, Jaganathan V, Shanmugam R, Kanagaraj K, Paul SF (2019) Association between occupational heat stress and DNA damage in lymphocytes of workers exposed to hot working environments in a steel industry in Southern India. Temperature 6(4):346–359

    Article  Google Scholar 

  • Wu T, Chen S, Xiao C, Wang C, Pan Q, Wang Z, ..., Tanguay RM (2001) Presence of antibody against the inducible Hsp71 in patients with acute heat-induced illness. Cell Stress Chaperones 6(2):113

  • Xiang JJ, Bi P, Pisaniello D, Hansen A (2014) Health impacts of workplace heat exposure: an epidemiological review. Ind Health 52(2):91–101. https://doi.org/10.2486/indhealth.2012-0145

    Article  Google Scholar 

  • Yaeram J, Setchell B, Maddocks S (2006) Effect of heat stress on the fertility of male mice in vivo and in vitro. Reprod Fertil Dev 18(6):647–653

    Article  CAS  Google Scholar 

  • Yan Y-E, Zhao Y-Q, Wang H, Fan M (2006) Pathophysiological factors underlying heatstroke. Med Hypotheses 67(3):609–617

    Article  CAS  Google Scholar 

  • Yang X, Yuan J, Sun J, Wang H, Liang H, Bai Y, ..., Wang J (2008) Association between heat-shock protein 70 gene polymorphisms and DNA damage in peripheral blood lymphocytes among coke-oven workers. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 649(1-2):221-229

  • Yili X, Tangchun W, Yongxing Z, Tanguay R, Nicole L, Ye Y, Guogao Z (1997) Preliminary studies on the relationship between autoantibodies to heat stress proteins and heat injury of pilots during acute heat stress. J Tongji Med Univ 17(2):83–85

    Article  Google Scholar 

  • Zhu B-K, Setchell BP (2004) Effects of paternal heat stress on the in vivo development of preimplantation embryos in the mouse. Reprod Nutr Dev 44(6):617–629

    Article  Google Scholar 

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Acknowledgements

The researchers express their gratitude to the School of Public Health Research Council of Tehran University of Medical Sciences, Tehran, Iran, for their advices and support.

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PH and AH participated in the study design and data collection. SNO, SA, and ARF participated in data analysis, manuscript writing, revising, and editing. Study was done under the supervision of FG and MRM. All authors read, revised, and approved the final manuscript.

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Correspondence to Farideh Golbabaei.

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Habibi, P., Ostad, S.N., Heydari, A. et al. Effect of heat stress on DNA damage: a systematic literature review. Int J Biometeorol 66, 2147–2158 (2022). https://doi.org/10.1007/s00484-022-02351-w

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