Low-dose radiation-induced risk in spermatogenesis

Abstract Purpose: To discuss low-dose radiation-induced risks to male fertility focusing on potential mechanisms of low-dose radiation-induced damage on spermatogenesis, epidemiological studies of environmental radiation effects on sperm parameters and transgenerational effects following exposure of spermatogonial stem cells (SSCs). Background: Spermatogenesis produces mature male gametes, spermatozoa, which fertilize their counterpart female gametes, oocytes. The robust maintenance system of spermatogenesis is essential for genomic conservation; however, male fertility can be readily impacted by exposure to environmental, chemical and physical factors including ionizing radiation. The mammalian testes are known to be radiosensitive yet the underlying molecular mechanisms of low-dose radiation-induced risks for spermatogenesis remain unclear. Furthermore, evidence characterizing transgenerational effects following exposure of SSCs remain controversial. Conclusions: Current concerns over the possible effects of low-dose radiation exposure on spermatogenesis requires further elucidation that may be resolved comparing and integrating observed experimental and epidemiological data.

[1]  M. Fukumoto,et al.  Analysis of the Effect of Chronic and Low-Dose Radiation Exposure on Spermatogenic Cells of Male Large Japanese Field Mice (Apodemus speciosus) after the Fukushima Daiichi Nuclear Power Plant Accident , 2017, Radiation Research.

[2]  D. Averill-Bates,et al.  Activation of apoptosis signalling pathways by reactive oxygen species. , 2016, Biochimica et biophysica acta.

[3]  J. T. Smith,et al.  Thirty years after the Chernobyl accident: What lessons have we learnt? , 2016, Journal of environmental radioactivity.

[4]  A. Talebi,et al.  Etiologies of sperm oxidative stress , 2016, International journal of reproductive biomedicine.

[5]  M. Onuma,et al.  Effects of environmental radiation on testes and spermatogenesis in wild large Japanese field mice (Apodemus speciosus) from Fukushima , 2016, Scientific Reports.

[6]  D D Zhou,et al.  Sperm quality and DNA damage in men from Jilin Province, China, who are occupationally exposed to ionizing radiation. , 2016, Genetics and molecular research : GMR.

[7]  E. Azzam,et al.  Is Ionizing Radiation Harmful at any Exposure? An Echo That Continues to Vibrate , 2016, Health physics.

[8]  H. Kimura,et al.  Long-term ex vivo maintenance of testis tissues producing fertile sperm in a microfluidic device , 2016, Scientific Reports.

[9]  R. Brannigan,et al.  Male adolescent fertility preservation. , 2016, Fertility and sterility.

[10]  C. Busby,et al.  Genetic radiation risks: a neglected topic in the low dose debate , 2016, Environmental health and toxicology.

[11]  G. Karsenty,et al.  Review of the Different Treatments and Management for Prostate Cancer and Fertility. , 2015, Urology.

[12]  M. Longobardi,et al.  Transgenerational inheritance of enhanced susceptibility to radiation-induced medulloblastoma in newborn Ptch1+/− mice after paternal irradiation , 2015, Oncotarget.

[13]  Hisanori Fukunaga,et al.  Low-dose radiation risk and individual variation in radiation sensitivity in Fukushima , 2015, Journal of radiation research.

[14]  Hisanori Fukunaga,et al.  Mental Health Crisis in Northeast Fukushima after the 2011 Earthquake, Tsunami and Nuclear Disaster. , 2015, The Tohoku journal of experimental medicine.

[15]  Yasuhiko Kobayashi,et al.  A mathematical model of radiation-induced responses in a cellular population including cell-to-cell communications. , 2015, Radiation protection dosimetry.

[16]  Richard Wakeford,et al.  Long-term effects of radiation exposure on health , 2015, The Lancet.

[17]  C. Rübe,et al.  Persistent DNA Damage in Spermatogonial Stem Cells After Fractionated Low-Dose Irradiation of Testicular Tissue. , 2015, International journal of radiation oncology, biology, physics.

[18]  Takashi Yamamoto,et al.  Genome Editing in Mouse Spermatogonial Stem Cell Lines Using TALEN and Double-Nicking CRISPR/Cas9 , 2015, Stem cell reports.

[19]  Hisanori Fukunaga.  After the earthquake, tsunami and nuclear crisis , 2015, Journal of the Royal Society of Medicine.

[20]  H. Menzel.  International Commission on Radiation Units and Measurements , 2011, Journal of the ICRU.

[21]  M. Tomita,et al.  Mechanisms and biological importance of photon-induced bystander responses: do they have an impact on low-dose radiation responses , 2014, Journal of radiation research.

[22]  N. Ogonuki,et al.  Offspring production with sperm grown in vitro from cryopreserved testis tissues , 2014, Nature Communications.

[23]  S. Murphy,et al.  A paternal environmental legacy: Evidence for epigenetic inheritance through the male germ line , 2014, BioEssays : news and reviews in molecular, cellular and developmental biology.

[24]  M. Meistrich.  Effects of chemotherapy and radiotherapy on spermatogenesis in humans. , 2013, Fertility and sterility.

[25]  K M Prise,et al.  Bystander signalling: exploring clinical relevance through new approaches and new models. , 2013, Clinical oncology (Royal College of Radiologists (Great Britain)).

[26]  H. Krishnamurthy,et al.  Semen Abnormalities, Sperm DNA Damage and Global Hypermethylation in Health Workers Occupationally Exposed to Ionizing Radiation , 2013, PloS one.

[27]  H. Scherthan,et al.  Ku70 and non-homologous end joining protect testicular cells from DNA damage , 2013, Journal of Cell Science.

[28]  Dudley T Goodhead,et al.  Evidence relevant to untargeted and transgenerational effects in the offspring of irradiated parents. , 2013, Mutation research.

[29]  W. J. Bair,et al.  Issues in Low Dose Radiation Biology: The Controversy Continues. A Perspective , 2013, Radiation research.

[30]  M. Little,et al.  Non-targeted effects of ionising radiation--implications for low dose risk. , 2013, Mutation research.

[31]  S. Shibahara,et al.  The Great East-Japan Earthquake and devastating tsunami: an update and lessons from the past Great Earthquakes in Japan since 1923. , 2013, The Tohoku journal of experimental medicine.

[32]  C. de Jager,et al.  What should it take to describe a substance or product as 'sperm-safe'. , 2013, Human reproduction update.

[33]  Edouard I Azzam,et al.  Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury. , 2012, Cancer letters.

[34]  R K Sachs,et al.  Radiation-induced cancer: a modern view. , 2012, The British journal of radiology.

[35]  J. Gosálvez,et al.  Types, Causes, Detection and Repair of DNA Fragmentation in Animal and Human Sperm Cells , 2012, International journal of molecular sciences.

[36]  Conor K McGarry,et al.  A computational model of cellular response to modulated radiation fields. , 2012, International journal of radiation oncology, biology, physics.

[37]  S. Yoshida.  Elucidating the identity and behavior of spermatogenic stem cells in the mouse testis. , 2012, Reproduction.

[38]  A. Rubanovich,et al.  The Dose and Dose-Rate Effects of Paternal Irradiation on Transgenerational Instability in Mice: A Radiotherapy Connection , 2012, PloS one.

[39]  Stephen R. Quake,et al.  Genome-wide Single-Cell Analysis of Recombination Activity and De Novo Mutation Rates in Human Sperm , 2012, Cell.

[40]  Luís Rato,et al.  Metabolic regulation is important for spermatogenesis , 2012, Nature Reviews Urology.

[41]  J. Boice,et al.  Radiation epidemiology: a perspective on Fukushima , 2012, Journal of radiological protection : official journal of the Society for Radiological Protection.

[42]  Takehiko Ogawa,et al.  In vitro production of fertile sperm from murine spermatogonial stem cell lines. , 2011, Nature communications.

[43]  Bryan C Dickinson,et al.  Chemistry and biology of reactive oxygen species in signaling or stress responses. , 2011, Nature chemical biology.

[44]  P. Sykes,et al.  Radiation-Induced Bystander Effects: What Are They, and How Relevant Are They to Human Radiation Exposures? , 2011, Radiation research.

[45]  S. Shibahara.  The 2011 Tohoku earthquake and devastating tsunami. , 2011, The Tohoku journal of experimental medicine.

[46]  Takehiko Ogawa,et al.  In vitro production of functional sperm in cultured neonatal mouse testes , 2011 .

[47]  D. Preston,et al.  Long-term Radiation-Related Health Effects in a Unique Human Population: Lessons Learned from the Atomic Bomb Survivors of Hiroshima and Nagasaki , 2011, Disaster Medicine and Public Health Preparedness.

[48]  Shenmin Zhang,et al.  Protecting the heritable genome: DNA damage response mechanisms in spermatogonial stem cells. , 2011, DNA repair.

[49]  J. Bonde.  Male reproductive organs are at risk from environmental hazards. , 2010, Asian journal of andrology.

[50]  J. Jeruss,et al.  Preservation of fertility in patients with cancer. , 2009, The New England journal of medicine.

[51]  M. Little.  Cancer and non-cancer effects in Japanese atomic bomb survivors , 2009, Journal of radiological protection : official journal of the Society for Radiological Protection.

[52]  Kevin M. Prise,et al.  Radiation-induced bystander signalling in cancer therapy , 2009, Nature Reviews Cancer.

[53]  Andrei Seluanov,et al.  DNA repair by nonhomologous end joining and homologous recombination during cell cycle in human cells , 2008, Cell cycle.

[54]  M. Pimpinella,et al.  Oncogenic bystander radiation effects in Patched heterozygous mouse cerebellum , 2008, Proceedings of the National Academy of Sciences.

[55]  S. Fesenko,et al.  Effects of non-human species irradiation after the Chernobyl NPP accident. , 2008, Environment international.

[56]  S. Amundson,et al.  Mechanism of radiation‐induced bystander effects: a unifying model , 2008, The Journal of pharmacy and pharmacology.

[57]  S. Cordier.  Evidence for a role of paternal exposures in developmental toxicity. , 2008, Basic & clinical pharmacology & toxicology.

[58]  Adrian K. Dixon,et al.  Benefits and costs, an eternal balance , 2007 .

[59]  Kathryn A. Higley,et al.  Environmental consequences of the chernobyl accident and their remediation: twenty years of experience. Report of the chernobyl forum expert group ‘environment’ STI/PUB/1239, 2006, International Atomic Energy Agency, Vienna, Austria ISBN: 92-0-114705-8, 166 pp, 40.00 Euros (softbound) , 2006 .

[60]  D. Averbeck,et al.  Low levels of clustered oxidative DNA damage induced at low and high LET irradiation in mammalian cells , 2006, Radiation and environmental biophysics.

[61]  O. Kovalchuk,et al.  Epigenetic dysregulation underlies radiation-induced transgenerational genome instability in vivo. , 2006, International journal of radiation oncology, biology, physics.

[62]  A. Agarwal,et al.  Oxidative stress, DNA damage and apoptosis in male infertility: a clinical approach , 2005, BJU international.

[63]  J. Schimenti,et al.  Homologous recombinational repair proteins in mouse meiosis , 2004, Cytogenetic and Genome Research.

[64]  S. Izumi,et al.  Cancer incidence in children and young adults did not increase relative to parental exposure to atomic bombs , 2003, British Journal of Cancer.

[65]  K. Prise,et al.  Bystander responses induced by low LET radiation , 2003, Oncogene.

[66]  E. Sheiner,et al.  Effect of occupational exposures on male fertility: literature review. , 2003, Industrial health.

[67]  M. Rahu,et al.  Health effects of the Chernobyl accident: fears, rumours and the truth. , 2003, European journal of cancer.

[68]  P. V. van Buul,et al.  DNA Double-Strand Breaks and γ-H2AX Signaling in the Testis1 , 2003 .

[69]  J. Wickliffe,et al.  Assessing the genotoxicity of chronic environmental irradiation by using mitochondrial dna heteroplasmy in the bank vole (Clethrionomys glareolus) at Chornobyl, Ukraine , 2002, Environmental toxicology and chemistry.

[70]  M. Ohtaki,et al.  Persistent Induction of Somatic Reversions of the Pink-Eyed Unstable Mutation in F1 Mice Born to Fathers Irradiated at the Spermatozoa Stage , 2002, Radiation research.

[71]  K M Prise,et al.  Bystander-induced apoptosis and premature differentiation in primary urothelial explants after charged particle microbeam irradiation. , 2002, Radiation protection dosimetry.

[72]  M. Plumb,et al.  Elevated mutation rates in the germ line of first- and second-generation offspring of irradiated male mice , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[73]  R. Baker,et al.  Consequences of Polluted Environments on Population Structure: The Bank Vole (Clethrionomys Glareolus) at Chornobyl , 2001, Ecotoxicology.

[74]  J. Little,et al.  Unexpected sensitivity to the induction of mutations by very low doses of alpha-particle radiation: evidence for a bystander effect. , 1999, Radiation research.

[75]  K. Boekelheide,et al.  The Fas system is a key regulator of germ cell apoptosis in the testis. , 1998, Endocrinology.

[76]  A. Fischbein,et al.  Ultramorphological sperm characteristics in the risk assessment of health effects after radiation exposure among salvage workers in Chernobyl. , 1997, Environmental health perspectives.

[77]  K. Hiyama,et al.  Lack of effects of atomic bomb radiation on genetic instability of tandem-repetitive elements in human germ cells. , 1995, American journal of human genetics.

[78]  R. Doll,et al.  Hazards of ionising radiation: 100 years of observations on man. , 1995, British Journal of Cancer.

[79]  N. I. Ryabokon,et al.  Dynamics of Cytogenetic Injuries in Natural Populations of Bank Vole in the Republic of Belarus , 1995 .

[80]  Cheburakov IuIu,et al.  [Disorders of spermatogenesis in people working at the clean-up of the Chernobyl nuclear power plant accident]. , 1993 .

[81]  G J Draper,et al.  Cancer in Cumbria and in the vicinity of the Sellafield nuclear installation, 1963-90. , 1993, BMJ.

[82]  Henry I. Kohn,et al.  Health Effects of Exposure to Low Levels of Ionizing Radiation (BEIR V) , 1990 .

[83]  H. Kato,et al.  Malignant tumors during the first 2 decades of life in the offspring of atomic bomb survivors. , 1990, American journal of human genetics.

[84]  A J Hall,et al.  Results of case-control study of leukaemia and lymphoma among young people near Sellafield nuclear plant in West Cumbria. , 1990, BMJ.

[85]  H. Samuel.  Preface to Workshop on Chronic Disease in the Workplace and the Environment , 1984 .

[86]  W. Schull.  Reproductive problems: fertility teratogenesis and mutagenesis. , 1984 .

[87]  W. Bremner,et al.  The effect of testicular x-irradiation on spermatogenesis in man. A comparison with the mouse. , 1983, Journal of andrology.

[88]  N. Suzuki,et al.  Gradual regeneration of mouse testicular stem cells after exposure to ionizing radiation. , 1978, Radiation research.

[89]  M J Rowley,et al.  Effect of graded doses of ionizing radiation on the human testis. , 1974, Radiation research.

[90]  J. Fabia,et al.  Occupation of father at time of birth of children dying of malignant diseases * , 1974, British journal of preventive & social medicine.

[91]  H J Muller,et al.  ARTIFICIAL TRANSMUTATION OF THE GENE. , 1927, Science.

[92]  M. Griswold.  Spermatogenesis: The Commitment to Meiosis. , 2016, Physiological reviews.

[93]  Richard Wakeford,et al.  Further consideration of the incidence of cancers around the nuclear installations at Sellafield and Dounreay , 2016 .

[94]  J. Peñagarícano,et al.  High dose bystander effects in spatially fractionated radiation therapy. , 2015, Cancer letters.

[95]  A. Clark,et al.  Germline stem cells: toward the regeneration of spermatogenesis. , 2014, Fertility and sterility.

[96]  Yu Shyr,et al.  Genetic disease in the children of Danish survivors of childhood and adolescent cancer. , 2012, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[97]  J. Valentin.  The 2007 Recommendations of the International Commission on Radiological Protection. ICRP publication 103. , 2007, Annals of the ICRP.

[98]  F. Egerton,et al.  A History of the Ecological Sciences, Part 19: Leeuwenhoek's Microscopic Natural History , 2006 .

[99]  A. Agarwal,et al.  Role of caspases in male infertility. , 2004, Human reproduction update.

[100]  N. Tarozzi,et al.  Abnormal spermatozoa in the ejaculate: abortive apoptosis and faulty nuclear remodelling during spermatogenesis. , 2003, Reproductive biomedicine online.

[101]  P. V. van Buul,et al.  DNA double-strand breaks and gamma-H2AX signaling in the testis. , 2003, Biology of reproduction.

[102]  Iu Iu Cheburakov,et al.  [Disorders of spermatogenesis in people working at the clean-up of the Chernobyl nuclear power plant accident]. , 1993, Radiatsionnaia biologiia, radioecologiia.

[103]  L. Feinendegen,et al.  A microdosimetric understanding of low-dose radiation effects. , 1988, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[104]  E. G. Ruestow.  Images and ideas: Leeuwenhoek's perception of the spermatozoa , 1983, Journal of the history of biology.

[105]  Icrp.  Recommendations of the International Commission on Radiological Protection, ICRP Publication 26 , 1977 .

[106]  H. Withers,et al.  Radiation survival and regeneration characteristics of spermatogenic stem cells of mouse testis. , 1974, Radiation research.

[107]  Y. Clermont.  Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. , 1972, Physiological reviews.

[108]  W. M. COURT BROWN.  Radiation carcinogenesis. , 1963, The Practitioner.