Environmental and Genetic Traffic in the Journey from Sperm to Offspring
Language English Country Switzerland Media electronic
Document type Journal Article, Review
PubMed
38136630
PubMed Central
PMC10741607
DOI
10.3390/biom13121759
PII: biom13121759
Knihovny.cz E-resources
- Keywords
- environmental pollution, epigenetic changes, genetic infertility, semen quality, transgenerational effects,
- MeSH
- Epigenesis, Genetic MeSH
- Phenotype MeSH
- Humans MeSH
- Disease Susceptibility MeSH
- Reproduction genetics MeSH
- Semen * MeSH
- Spermatozoa * MeSH
- Check Tag
- Humans MeSH
- Male MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
Recent advancements in the understanding of how sperm develop into offspring have shown complex interactions between environmental influences and genetic factors. The past decade, marked by a research surge, has not only highlighted the profound impact of paternal contributions on fertility and reproductive outcomes but also revolutionized our comprehension by unveiling how parental factors sculpt traits in successive generations through mechanisms that extend beyond traditional inheritance patterns. Studies have shown that offspring are more susceptible to environmental factors, especially during critical phases of growth. While these factors are broadly detrimental to health, their effects are especially acute during these periods. Moving beyond the immutable nature of the genome, the epigenetic profile of cells emerges as a dynamic architecture. This flexibility renders it susceptible to environmental disruptions. The primary objective of this review is to shed light on the diverse processes through which environmental agents affect male reproductive capacity. Additionally, it explores the consequences of paternal environmental interactions, demonstrating how interactions can reverberate in the offspring. It encompasses direct genetic changes as well as a broad spectrum of epigenetic adaptations. By consolidating current empirically supported research, it offers an exhaustive perspective on the interwoven trajectories of the environment, genetics, and epigenetics in the elaborate transition from sperm to offspring.
Department of Anatomy All India Institute of Medical Sciences New Delhi 110029 India
Department of Life Science and Bioinformatics Assam University Silchar 788011 India
School of Life Sciences Manipal Academy of Higher Education Dubai 345050 United Arab Emirates
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Hart K., Tadros N.N. The role of environmental factors and lifestyle on male reproductive health, the epigenome, and resulting offspring. Panminerva Med. 2019;61:187–195. doi: 10.23736/S0031-0808.18.03531-0. PubMed DOI
Mima M., Greenwald D., Ohlander S. Environmental Toxins and Male Fertility. Curr. Urol. Rep. 2018;19:50. doi: 10.1007/s11934-018-0804-1. PubMed DOI
Rauh V.A., Margolis A.E. Research Review: Environmental exposures, neurodevelopment, and child mental health—New paradigms for the study of brain and behavioral effects. J. Child. Psychol. Psychiatry. 2016;57:775–793. doi: 10.1111/jcpp.12537. PubMed DOI PMC
Jami E.S., Hammerschlag A.R., Bartels M., Middeldorp C.M. Parental characteristics and offspring mental health and related outcomes: A systematic review of genetically informative literature. Transl. Psychiatry. 2021;11:197. doi: 10.1038/s41398-021-01300-2. PubMed DOI PMC
Ralston A., Shaw K. Environment controls gene expression: Sex determination and the onset of genetic disorders. Nat. Educ. 2008;1:203.
Bline A.P., Le Goff A., Allard P. What Is Lost in the Weismann Barrier? J. Dev. Biol. 2020;8:35. doi: 10.3390/jdb8040035. PubMed DOI PMC
Donkin I., Barrès R. Sperm epigenetics and influence of environmental factors. Mol. Metab. 2018;14:1–11. doi: 10.1016/j.molmet.2018.02.006. PubMed DOI PMC
Finelli R., Mottola F., Agarwal A. Impact of Alcohol Consumption on Male Fertility Potential: A Narrative Review. Int. J. Environ. Res. Public Health. 2021;19:328. doi: 10.3390/ijerph19010328. PubMed DOI PMC
Marić T., Fučić A., Aghayanian A. Environmental and occupational exposures associated with male infertility. Arh. Hig. Rada Toksikol. 2021;72:101–113. doi: 10.2478/aiht-2021-72-3510. PubMed DOI PMC
Xavier M.J., Roman S.D., Aitken R.J., Nixon B. Transgenerational inheritance: How impacts to the epigenetic and genetic information of parents affect offspring health. Hum. Reprod. Update. 2019;25:518–540. doi: 10.1093/humupd/dmz017. PubMed DOI
Burton T., Metcalfe N.B. Can environmental conditions experienced in early life influence future generations? Proc. Biol. Sci. 2014;281:20140311. doi: 10.1098/rspb.2014.0311. PubMed DOI PMC
Day J., Savani S., Krempley B.D., Nguyen M., Kitlinska J.B. Influence of paternal preconception exposures on their offspring: Through epigenetics to phenotype. Am. J. Stem Cells. 2016;5:11–18. PubMed PMC
Knudsen M.T., Rezwan F.I., Jiang Y., Karmaus W., Svanes C., Holloway J.W. Transgenerational and intergenerational epigenetic inheritance in allergic diseases. J. Allergy Clin. Immunol. 2018;142:765–772. doi: 10.1016/j.jaci.2018.07.007. PubMed DOI PMC
Branje S., Geeraerts S., de Zeeuw E.L., Oerlemans A.M., Koopman-Verhoeff M.E., Schulz S., Nelemans S., Meeus W., Hartman C.A., Hillegers M.H.J., et al. Intergenerational transmission: Theoretical and methodological issues and an introduction to four Dutch cohorts. Dev. Cogn. Neurosci. 2020;45:100835. doi: 10.1016/j.dcn.2020.100835. PubMed DOI PMC
Magkos F., Yannakoulia M., Chan J.L., Mantzoros C.S. Management of the metabolic syndrome and type 2 diabetes through lifestyle modification. Annu. Rev. Nutr. 2009;29:223–256. doi: 10.1146/annurev-nutr-080508-141200. PubMed DOI PMC
Roberts C.K., Hevener A.L., Barnard R.J. Metabolic syndrome and insulin resistance: Underlying causes and modification by exercise training. Compr. Physiol. 2013;3:1–58. doi: 10.1002/cphy.c110062. PubMed DOI PMC
Jung U.J., Choi M.S. Obesity and its metabolic complications: The role of adipokines and the relationship between obesity, inflammation, insulin resistance, dyslipidemia and nonalcoholic fatty liver disease. Int. J. Mol. Sci. 2014;15:6184–6223. doi: 10.3390/ijms15046184. PubMed DOI PMC
Rando O.J., Simmons R.A. I’m eating for two: Parental dietary effects on offspring metabolism. Cell. 2015;161:93–105. doi: 10.1016/j.cell.2015.02.021. PubMed DOI PMC
Rosenbusch B. To What Extent Are Cryopreserved Sperm and Testicular Biopsy Samples Used in Assisted Reproduction? J. Reprod. Infertil. 2018;19:115–118. PubMed PMC
Sharma R., Agarwal A., Rohra V.K., Assidi M., Abu-Elmagd M., Turki R.F. Effects of increased paternal age on sperm quality, reproductive outcome and associated epigenetic risks to offspring. Reprod. Biol. Endocrinol. 2015;13:35. doi: 10.1186/s12958-015-0028-x. PubMed DOI PMC
Kaltsas A., Moustakli E., Zikopoulos A., Georgiou I., Dimitriadis F., Symeonidis E.N., Markou E., Michaelidis T.M., Tien D.M.B., Giannakis I., et al. Impact of Advanced Paternal Age on Fertility and Risks of Genetic Disorders in Offspring. Genes. 2023;14:486. doi: 10.3390/genes14020486. PubMed DOI PMC
Engeland A., Bjørge T., Daltveit A.K., Skurtveit S., Vangen S., Vollset S.E., Furu K. Effects of preconceptional paternal drug exposure on birth outcomes: Cohort study of 340,000 pregnancies using Norwegian population-based databases. Br. J. Clin. Pharmacol. 2013;75:1134–1141. doi: 10.1111/j.1365-2125.2012.04426.x. PubMed DOI PMC
Vallaster M.P., Kukreja S., Bing X.Y., Ngolab J., Zhao-Shea R., Gardner P.D., Tapper A.R., Rando O.J. Paternal nicotine exposure alters hepatic xenobiotic metabolism in offspring. eLife. 2017;6:e24771. doi: 10.7554/eLife.24771. PubMed DOI PMC
Rutkowska J., Lagisz M., Bonduriansky R., Nakagawa S. Mapping the past, present and future research landscape of paternal effects. BMC Biol. 2020;18:183. doi: 10.1186/s12915-020-00892-3. PubMed DOI PMC
Aitken R.J. Male reproductive ageing: A radical road to ruin. Hum. Reprod. 2023;38:1861–1871. doi: 10.1093/humrep/dead157. PubMed DOI PMC
Fitz-James M.H., Cavalli G. Molecular mechanisms of transgenerational epigenetic inheritance. Nat. Rev. Genet. 2022;23:325–341. doi: 10.1038/s41576-021-00438-5. PubMed DOI
Immler S. The sperm factor: Paternal impact beyond genes. Heredity. 2018;121:239–247. doi: 10.1038/s41437-018-0111-0. PubMed DOI PMC
Maklakov A.A., Immler S. The Expensive Germline and the Evolution of Ageing. Curr. Biol. 2016;26:R577–R586. doi: 10.1016/j.cub.2016.04.012. PubMed DOI
Dhawan V., Kumar M., Dipika D., Malhotra N., Singh N., Dadhwal V., Dada R. Paternal factors and embryonic development: Role in recurrent pregnancy loss. Andrologia. 2019;51:e13171. doi: 10.1111/and.13171. PubMed DOI
Siomi M.C., Sato K., Pezic D., Aravin A.A. Piwi-interacting small RNAs: The vanguard of genome defence. Nat. Rev. Mol. Cell Biol. 2011;12:246–258. doi: 10.1038/nrm3089. PubMed DOI
Ernst C., Odom D.T., Kutter C. The emergence of piRNAs against transposon invasion to preserve mammalian genome integrity. Nat. Commun. 2017;8:1411. doi: 10.1038/s41467-017-01049-7. PubMed DOI PMC
Sharma U. Paternal Contributions to Offspring Health: Role of Sperm Small RNAs in Intergenerational Transmission of Epigenetic Information. Front. Cell Dev. Biol. 2019;7:215. doi: 10.3389/fcell.2019.00215. PubMed DOI PMC
Donelan S.C., Hellmann J.K., Bell A.M., Luttbeg B., Orrock J.L., Sheriff M.J., Sih A. Transgenerational Plasticity in Human-Altered Environments. Trends Ecol. Evol. 2020;35:115–124. doi: 10.1016/j.tree.2019.09.003. PubMed DOI PMC
Hales C.N., Barker D.J. The thrifty phenotype hypothesis. Br. Med. Bull. 2001;60:5–20. doi: 10.1093/bmb/60.1.5. PubMed DOI
Miska E.A., Ferguson-Smith A.C. Transgenerational inheritance: Models and mechanisms of non-DNA sequence-based inheritance. Science. 2016;354:59–63. doi: 10.1126/science.aaf4945. PubMed DOI
Kishimoto S., Uno M., Okabe E., Nono M., Nishida E. Environmental stresses induce transgenerationally inheritable survival advantages via germline-to-soma communication in Caenorhabditis elegans. Nat. Commun. 2017;8:14031. doi: 10.1038/ncomms14031. PubMed DOI PMC
Burgess S.C., Marshall D.J. Adaptive parental effects: The importance of estimating environmental predictability and offspring fitness appropriately. Oikos. 2014;123:769–776. doi: 10.1111/oik.01235. DOI
Marshall D.J., Uller T. When is a maternal effect adaptive? Oikos. 2007;116:1957–1963. doi: 10.1111/j.2007.0030-1299.16203.x. DOI
Xue B., Leibler S. Evolutionary learning of adaptation to varying environments through a transgenerational feedback. Proc. Natl. Acad. Sci. USA. 2016;113:11266–11271. doi: 10.1073/pnas.1608756113. PubMed DOI PMC
Burgess S.C., Marshall D.J. Temperature-induced maternal effects and environmental predictability. J. Exp. Biol. 2011;214:2329–2336. doi: 10.1242/jeb.054718. PubMed DOI
Crean A.J., Dwyer J.M., Marshall D.J. Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance. Ecology. 2013;94:2575–2582. doi: 10.1890/13-0184.1. PubMed DOI
Eisenberg D.T.A. An evolutionary review of human telomere biology: The thrifty telomere hypothesis and notes on potential adaptive paternal effects. Am. J. Hum. Biol. 2011;23:149–167. doi: 10.1002/ajhb.21127. PubMed DOI
Arnqvist G., Rowe L. Sexual Conflict. Princeton University Press; Princeton, NJ, USA: 2005. DOI
Anvar Z., Chakchouk I., Demond H., Sharif M., Kelsey G., Van den Veyver I.B. DNA Methylation Dynamics in the Female Germline and Maternal-Effect Mutations that Disrupt Genomic Imprinting. Genes. 2021;12:1214. doi: 10.3390/genes12081214. PubMed DOI PMC
O’Brien E.K., Wolf J.B. The coadaptation theory for genomic imprinting. Evol. Lett. 2017;1:49–59. doi: 10.1002/evl3.5. PubMed DOI PMC
Haig D. The kinship theory of genomic imprinting. Ann. Rev. Ecol. Syst. 2000;31:9–32. doi: 10.1146/annurev.ecolsys.31.1.9. DOI
Haig D. Genomic imprinting and kinship: How good is the evidence? Ann. Rev. Genet. 2004;38:553–585. doi: 10.1146/annurev.genet.37.110801.142741. PubMed DOI
Day T., Bonduriansky R. Intralocus sexual conflict can drive the evolution of genomic imprinting. Genetics. 2004;167:1537–1546. doi: 10.1534/genetics.103.026211. PubMed DOI PMC
Wolf J.B., Hager R. A maternal-offspring coadaptation theory for the evolution of genomic imprinting. PLoS Biol. 2006;4:2238–2243. doi: 10.1371/journal.pbio.0040380. PubMed DOI PMC
Spencer H.G., Clark A.G. Non-conflict theories for the evolution of genomic imprinting. Heredity. 2014;113:112–118. doi: 10.1038/hdy.2013.129. PubMed DOI PMC
Agren J.A., Clark A.G. Selfish genetic elements. PLoS Genet. 2018;14:e1007700. doi: 10.1371/journal.pgen.1007700. PubMed DOI PMC
Wedell N. Selfish genes and sexual selection: The impact of genomic parasites on host reproduction. J. Zool. 2020;311:1–12. doi: 10.1111/jzo.12780. DOI
Verspoor R.L., Price T.A.R., Wedell N. Selfish genetic elements and male fertility. Phil. Trans. R. Soc. B. 2020;375:20200067. doi: 10.1098/rstb.2020.0067. PubMed DOI PMC
Werren J.H. Selfish genetic elements, genetic conflict, and evolutionary innovation. Proc. Natl. Acad. Sci. USA. 2011;108:10863–10870. doi: 10.1073/pnas.1102343108. PubMed DOI PMC
Wedell N. The effect of non-self genes on the behaviour of hosts. In: Hosken D.J., Hunt J., Wedell N., editors. Genes and Behaviour: Beyond Nature-Nurture. John Wiley & Sons; Chichester, UK: 2019. pp. 157–180.
Zanders S.E., Unckless R.L. Fertility costs of meiotic drivers. Curr. Biol. 2019;29:R512–R520. doi: 10.1016/j.cub.2019.03.046. PubMed DOI PMC
Sutter A., Lindholm A.K. Detrimental effects of an autosomal selfish genetic element on sperm competitiveness in house mice. Proc. Biol. Sci. 2015;282:20150974. doi: 10.1098/rspb.2015.0974. PubMed DOI PMC
Christie J.R., Schaerf T.M., Beekman M. Selection against heteroplasmy explains the evolution of uniparental inheritance of mitochondria. PLoS Genet. 2015;11:e1005112. doi: 10.1371/journal.pgen.1005112. PubMed DOI PMC
Greiner S., Sobanski J., Bock R. Why are most organelle genomes transmitted maternally? Bioessays. 2015;37:80–94. doi: 10.1002/bies.201400110. PubMed DOI PMC
Cordier S. Evidence for a role of paternal exposures in developmental toxicity. Basic Clin. Pharmacol. Toxicol. 2008;102:176–181. doi: 10.1111/j.1742-7843.2007.00162.x. PubMed DOI
Soubry A., Hoyo C., Jirtle R.L., Murphy S.K. A paternal environmental legacy: Evidence for epigenetic inheritance through the male germ line. Bioessays. 2014;36:359–371. doi: 10.1002/bies.201300113. PubMed DOI PMC
Bonde J.P., Tøttenborg S.S., Hougaard K.S. Paternal environmental exposure and offspring health. Curr. Opin. Endocr. Metab. Res. 2019;7:14–20. doi: 10.1016/j.coemr.2019.05.001. DOI
Blay R.M., Pinamang A.D., Sagoe A.E., Owusu E., Koney N.K., Arko-Boham B. Infuence of lifestyle and environmental factors on semen quality in ghanaian men. Int. J. Reprod. Med. 2020;2020:6908458. doi: 10.1155/2020/6908458. PubMed DOI PMC
Nateghian Z., Aliabadi E. Aspects of Environmental Pollutants on Male Fertility and Sperm Parameters. [(accessed on 30 August 2023)];J. Environ. Treat. Tech. 2020 8:299–309. Available online: http://www.jett.dormaj.com.
Selvaraju V., Baskaran S., Agarwal A., Henkel R. Environmental contaminants and male infertility: Effects and mechanisms. Andrologia. 2021;53:e13646. doi: 10.1111/and.13646. PubMed DOI
Wang X., Tian X., Ye B., Zhang Y., Li C., Liao J., Zou Y., Zhang S., Zhu Y., Yang J., et al. Gaseous pollutant exposure affects semen quality in central China: A cross-sectional study. Andrology. 2020;8:117–124. doi: 10.1111/andr.12655. PubMed DOI
Sun S., Zhao J., Cao W., Lu W., Zheng T., Zeng Q. Identifying critical exposure windows for ambient air pollution and semen quality in Chinese men. Environ. Res. 2020;189:109894. doi: 10.1016/j.envres.2020.109894. PubMed DOI
Wdowiak A., Wdowiak E., Bień A., Bojar I., Iwanowicz-Palus G., Raczkiewicz D. Air pollution and semen parameters in men seeking fertility treatment for the first time. Int. J. Occup. Med. Environ. Health. 2019;32:387–399. doi: 10.13075/ijomeh.1896.01355. PubMed DOI
Yang Y., Yang T., Liu S., Cao Z., Zhao Y., Su X., Liao Z., Teng X., Hua J. Concentrated ambient PM2.5 exposure affects mice sperm quality and testosterone biosynthesis. PeerJ. 2019;7:e8109. doi: 10.7717/peerj.8109. PubMed DOI PMC
Dutta S., Sengupta P., Bagchi S., Chhikara B.S., Pavlík A., Sláma P., Roychoudhury S. Reproductive toxicity of combined effects of endocrine disruptors on human reproduction. Front. Cell Dev. Biol. 2023;11:1162015. doi: 10.3389/fcell.2023.1162015. PubMed DOI PMC
Mendiola J., Moreno J.M., Roca M., Vergara-Juárez N., Martínez-García M.J., García-Sánchez A., Elvira-Rendueles B., Moreno-Grau S., LópezEspín J.J., Ten J., et al. Relationships between heavy metal concentrations in three diferent body fuids and male reproductive parameters: A pilot study. Environ. Health. 2011;10:6. doi: 10.1186/1476-069X-10-6. PubMed DOI PMC
Sukhn C., Awwad J., Ghantous A., Zaatari G. Associations of semen quality with non-essential heavy metals in blood and seminal fuid: Data from the Environment and Male Infertility (EMI) study in Lebanon. J. Assist. Reprod. Genet. 2018;35:1691–1701. doi: 10.1007/s10815-018-1236-z. PubMed DOI PMC
Manouchehri A., Shokri S., Pirhadi M., Karimi M., Abbaszadeh S., Mirzaei G., Bahmani M. The Effects of Toxic Heavy Metals Lead, Cadmium and Copper on the Epidemiology of Male and Female Infertility. JBRA Assist. Reprod. 2022;26:627–630. doi: 10.5935/1518-0557.20220013. PubMed DOI PMC
Santonastaso M., Mottola F., Iovine C., Cesaroni F., Colacurci N., Rocco L. In Vitro Effects of Titanium Dioxide Nanoparticles (TiO2NPs) on Cadmium Chloride (CdCl2) Genotoxicity in Human Sperm Cells. Nanomaterials. 2020;10:1118. doi: 10.3390/nano10061118. PubMed DOI PMC
Calogero A.E., Fiore M., Giacone F., Altomare M., Asero P., Ledda C., Romeo G., Mongioì L.M., Copat C., Giuffrida M., et al. Exposure to multiple metals/metalloids and human semen quality: A cross-sectional study. Ecotoxicol. Environ. Saf. 2021;215:112165. doi: 10.1016/j.ecoenv.2021.112165. PubMed DOI
Hardneck F., Israel G., Pool E., Maree L. Quantitative assessment of heavy metal effects on sperm function using computer-aided sperm analysis and cytotoxicity assays. Andrologia. 2018;50:e13141. doi: 10.1111/and.13141. PubMed DOI
Mínguez-Alarcón L., Hauser R., Gaskins A.J. Effects of bisphenol A on male and couple reproductive health: A review. Fertil. Steril. 2016;106:864–870. doi: 10.1016/j.fertnstert.2016.07.1118. PubMed DOI PMC
Cariati F., D’Uonno N., Borrillo F., Iervolino S., Galdiero G., Rb T. Bisphenol a: An emerging threat to male fertility. Reprod. Biol. Endocrinol. 2019;17:6. doi: 10.1186/s12958-018-0447-6. PubMed DOI PMC
Barbonetti A., Castellini C., Di Giammarco N., Santilli G., Francavilla S., Francavilla F. In vitro exposure of human spermatozoa to bisphenol A induces pro-oxidative/apoptotic mitochondrial dysfunction. Reprod. Toxicol. 2016;66:61–67. doi: 10.1016/j.reprotox.2016.09.014. PubMed DOI
Bretveld R., Brouwers M., Ebisch I., Roeleveld N. Infuence of pesticides on male fertility. Scand. J. Work. Environ. Health. 2007;33:13–28. doi: 10.5271/sjweh.1060. PubMed DOI
National Academies of Sciences, Engineering, and Medicine. Division on Earth and Life Studies. Board on Environmental Studies and Toxicology. Committee on Endocrine-Related Low-Dose Toxicity Application of Systematic Review Methods in an Overall Strategy for Evaluating Low-Dose Toxicity from Endocrine Active Chemicals. National Academies Press (US): Washington, DC, USA, 2017; 3, Phthalates and Male Reproductive-Tract Development. [(accessed on 30 August 2023)]; Available online: https://www.ncbi.nlm.nih.gov/books/NBK453249/ PubMed
Hutson J.M. Cryptorchidism and Hypospadias. 14 December 2022. In: Feingold K.R., Anawalt B., Blackman M.R., Boyce A., Chrousos G., Corpas E., de Herder W.W., Dhatariya K., Dungan K., Hofland J., editors. Endotext [Internet] MDText.com, Inc.; South Dartmouth, MA, USA: 2000.
Ding X., Cao L., Zheng Y., Zhou X., He X., Xu S., Ren W. Insights into the Evolution of Spermatogenesis-Related Ubiquitin-Proteasome System Genes in Abdominal Testicular Laurasiatherians. Genes. 2021;12:1780. doi: 10.3390/genes12111780. PubMed DOI PMC
Al-Otaibi S.T. Male infertility among bakers associated with exposure to high environmental temperature at the workplace. J. Taibah Univ. Med. Sci. 2018;13:103–107. doi: 10.1016/j.jtumed.2017.12.003. PubMed DOI PMC
Hamerezaee M., Dehghan S.F., Golbabaei F., Fathi A., Barzegar L., Heidarnejad N. Assessment of semen quality among workers exposed to heat stress: A cross-sectional study in a steel industry. Saf. Health Work. 2018;9:232–235. doi: 10.1016/j.shaw.2017.07.003. PubMed DOI PMC
Kesari K.K., Agarwal A., Henkel R. Radiations and male fertility. Reprod. Biol. Endocrinol. 2018;16:118. doi: 10.1186/s12958-018-0431-1. PubMed DOI PMC
Kim S., Han D., Ryu J., Kim K., Kim Y.H. Effects of mobile phone usage on sperm quality—No time-dependent relationship on usage: A systematic review and updated meta-analysis. Environ. Res. 2021;202:111784. doi: 10.1016/j.envres.2021.111784. PubMed DOI
Aitken R.J. Reactive oxygen species as mediators of sperm capacitation and pathological damage. Mol. Reprod. Dev. 2017;84:1039–1052. doi: 10.1002/mrd.22871. PubMed DOI
Mottola F., Santonastaso M., Ronga V., Finelli R., Rocco L. Polymorphic Rearrangements of Human Chromosome 9 and Male Infertility: New Evidence and Impact on Spermatogenesis. Biomolecules. 2023;13:729. doi: 10.3390/biom13050729. PubMed DOI PMC
Leisegang K., Roychoudhury S., Slama P., Finelli R. The Mechanisms and Management of Age-Related Oxidative Stress in Male Hypogonadism Associated with Non-communicable Chronic Disease. Antioxidants. 2021;10:1834. doi: 10.3390/antiox10111834. PubMed DOI PMC
Durairajanayagam D. Lifestyle causes of male infertility. Arab. J. Urol. 2018;16:10–20. doi: 10.1016/j.aju.2017.12.004. PubMed DOI PMC
Samarasinghe S.V.A.C., Krishnan K., Naidu R., Megharaj M., Miller K., Fraser B., Aitken R.J. Parabens generate reactive oxygen species in human spermatozoa. Andrology. 2018;6:532–541. doi: 10.1111/andr.12499. PubMed DOI
Santonastaso M., Mottola F., Colacurci N., Iovine C., Pacifico S., Cammarota M., Cesaroni F., Rocco L. In vitro genotoxic effects of titanium dioxide nanoparticles (n-TiO2) in human sperm cells. Mol. Reprod. Dev. 2019;86:1369–1377. doi: 10.1002/mrd.23134. PubMed DOI
Jimenez-Villarreal J., Betancourt-Martinex N.D., Carranza-Rosales P., Valdez E.V., Guzman-Delgado N.E., Lopez-Marquez F.C., Moran-Martinez J. Formaldehyde induces DNA strand breaks on spermatozoa and lymphocytes of Wistar rats. Tsitol. Genet. 2017;51:78–80. doi: 10.3103/S0095452717010078. PubMed DOI
Mukherjee A.G., Valsala Gopalakrishnan A. The interplay of arsenic, silymarin, and NF-ĸB pathway in male reproductive toxicity: A review. Ecotoxicol. Environ. Saf. 2023;252:114614. doi: 10.1016/j.ecoenv.2023.114614. PubMed DOI
Khan F., Niaz K., Hassan F.I., Abdollahi M. An evidence-based review of the genotoxic and reproductive effects of sulfur mustard. Arch. Toxicol. 2017;91:1143–1156. doi: 10.1007/s00204-016-1911-8. PubMed DOI
Perrin J., Tassistro V., Mandon M., Grillo J.M., Botta A., Sari-Minodier I. Tobacco consumption and benzo(a)pyrene-diolepoxide-DNA adducts in spermatozoa: In smokers, swim-up procedure selects spermatozoa with decreased DNA damage. Fertil. Steril. 2011;95:2013–2017. doi: 10.1016/j.fertnstert.2011.02.021. PubMed DOI
McQueen D.B., Zhang J., Robins J.C. Sperm DNA fragmentation and recurrent pregnancy loss: A systematic review and meta-analysis. Fertil. Steril. 2019;112:54–60.e3. doi: 10.1016/j.fertnstert.2019.03.003. PubMed DOI
Waber D.P., Bryce C.P., Fitzmaurice G.M., Zichlin M.L., McGaughy J., Girard J.M., Galler J.R. Neuropsychological outcomes at midlife following moderate to severe malnutrition in infancy. Neuropsychology. 2014;28:530–540. doi: 10.1037/neu0000058. PubMed DOI PMC
Soneji S., Beltrán-Sánchez H. Association of Maternal Cigarette Smoking and Smoking Cessation With Preterm Birth. JAMA Netw. Open. 2019;2:e192514. doi: 10.1001/jamanetworkopen.2019.2514. PubMed DOI PMC
Meeker J.D. Exposure to environmental endocrine disruptors and child development. Arch. Pediatr. Adolesc. Med. 2012;166:E1–E7. doi: 10.1001/archpediatrics.2012.241. PubMed DOI PMC
Basak S., Das M.K., Duttaroy A.K. Plastics derived endocrine-disrupting compounds and their effects on early development. Birth Defects Res. 2020;112:1308–1325. doi: 10.1002/bdr2.1741. PubMed DOI
McCanlies E.C., Ma C.C., Gu J.K., Fekedulegn D., Sanderson W.T., Ludeña-Rodriguez Y.J., Hertz-Picciotto I. The CHARGE study: An assessment of parental occupational exposures and autism spectrum disorder. Occup. Environ. Med. 2019;76:644–651. doi: 10.1136/oemed-2018-105395. PubMed DOI
Zhang Y., Shi J., Rassoulzadegan M., Tuorto F., Chen Q. Sperm RNA code programmes the metabolic health of offspring. Nat. Rev. Endocrinol. 2019;15:489–498. doi: 10.1038/s41574-019-0226-2. PubMed DOI PMC
Gapp K., Jawaid A., Sarkies P., Bohacek J., Pelczar P., Prados J., Farinelli L., Miska E., Mansuy I.M. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat. Neurosci. 2014;17:667–669. doi: 10.1038/nn.3695. PubMed DOI PMC
Zumbrun E.E., Sido J.M., Nagarkatti P.S., Nagarkatti M. Epigenetic Regulation of Immunological Alterations Following Prenatal Exposure to Marijuana Cannabinoids and its Long Term Consequences in Offspring. J. Neuroimmune Pharmacol. 2015;10:245–254. doi: 10.1007/s11481-015-9586-0. PubMed DOI PMC
McCarthy D.M., Morgan T.J., Jr., Lowe S.E., Williamson M.J., Spencer T.J., Biederman J., Bhide P.G. Nicotine exposure of male mice produces behavioral impairment in multiple generations of descendants. PLoS Biol. 2018;16:e2006497. doi: 10.1371/journal.pbio.2006497. PubMed DOI PMC
Holloway Z.R., Hawkey A.B., Torres A.K., Evans J., Pippen E., White H., Katragadda V., Kenou B., Wells C., Murphy S.K., et al. Paternal cannabis extract exposure in rats: Preconception timing effects on neurodevelopmental behavior in offspring. Neurotoxicology. 2020;81:180–188. doi: 10.1016/j.neuro.2020.10.007. PubMed DOI
Ueker M.E., Silva V.M., Moi G.P., Pignati W.A., Mattos I.E., Silva A.M.C. Parenteral exposure to pesticides and occurence of congenital malformations: Hospital-based case-control study. BMC Pediatr. 2016;16:125. doi: 10.1186/s12887-016-0667-x. PubMed DOI PMC
Rauh V., Arunajadai S., Horton M., Perera F., Hoepner L., Barr D.B., Whyatt R. Seven-year neurodevelopmental scores and prenatal exposure to chlorpyrifos, a common agricultural pesticide. Environ. Health Perspect. 2011;119:1196–1201. doi: 10.1289/ehp.1003160. PubMed DOI PMC
Shelton J.F., Geraghty E.M., Tancredi D.J., Delwiche L.D., Schmidt R.J., Ritz B., Hansen R.L., Hertz-Picciotto I. Neurodevelopmental disorders and prenatal residential proximity to agricultural pesticides: The CHARGE study. Environ. Health Perspect. 2014;122:1103–1109. doi: 10.1289/ehp.1307044. Erratum in: Environ Health Perspect. 2014, 122, A266. PubMed DOI PMC
Yorifuji T., Tsuda T., Kashima S., Doi H. Mercury and autism: Accelerating evidence? Neuroendocrinol. Lett. 2014;35:221–226.
Ng S.-F., Lin RC Y., Laybutt D.R., Barres R., Owens J.A., Morris M.J. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature. 2010;467:963–966. doi: 10.1038/nature09491. PubMed DOI
Wei Y., Yang C.R., Wei Y.P., Ge Z.J., Zhao Z.A., Zhang X.H. Paternally induced transgenerational inheritance of susceptibility to diabetes in mammals. Proc. Natl. Acad. Sci. USA. 2015;112:5361–5366. doi: 10.1073/pnas.1321195111. PubMed DOI PMC
Wei Y., Yang C.R., Wei Y.P., Zhao Z.A., Hou Y., Schatten H., Sun Q.Y. Paternally induced transgenerational inheritance of susceptibility to cardiac ischemia-reperfusion injury. Front. Biosci. 2014;19:1074–1087.
Janssen B.G., Godderis L., Pieters N., Poels K., Kiciński M., Cuypers A., Fierens F., Penders J., Plusquin M., Gyselaers W., et al. Placental DNA hypomethylation in association with particulate air pollution in early life. Part. Fibre Toxicol. 2017;14:1–14. PubMed PMC
Dolinoy D.C., Weidman J.R., Waterland R.A., Jirtle R.L. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ. Health Perspect. 2007;115:879–885. PubMed PMC
Guerrero-Bosagna C., Covert T.R., Haque M.M., Settles M., Nilsson E.E., Anway M.D., Skinner M.K. Epigenetic transgenerational inheritance of vinclozolin induced mouse adult onset disease and associated sperm epigenome biomarkers. Reprod. Toxicol. 2012;34:694–707. doi: 10.1016/j.reprotox.2012.09.005. PubMed DOI PMC
Bouchard M.F., Bellinger D.C., Wright R.O., Weisskopf M.G. Attention-deficit/hyperactivity disorder and urinary metabolites of organophosphate pesticides. Pediatrics. 2010;125:e1270–e1277. doi: 10.1542/peds.2009-3058. PubMed DOI PMC
Rossides M., Kampitsi C.E., Talbäck M., Mogensen H., Wiebert P., Feychting M., Tettamanti G. Risk of Cancer in Children of Parents Occupationally Exposed to Hydrocarbon Solvents and Engine Exhaust Fumes: A Register-Based Nested Case-Control Study from Sweden (1960–2015) Environ. Health Perspect. 2022;130:77002. doi: 10.1289/EHP11035. PubMed DOI PMC
Short A.K., Fennell K.A., Perreau V.M., Fox A., O’Bryan M.K., Kim J.H., Bredy T.W., Pang T.Y., Hannan A.J. Elevated paternal glucocorticoid exposure alters the small noncoding RNA profile in sperm and modifies anxiety and depressive phenotypes in the offspring. Transl. Psychiatry. 2016;6:e837. doi: 10.1038/tp.2016.109. PubMed DOI PMC
Liu Y., Zhi X. Advances in Genetic Diagnosis of Kallmann Syndrome and Genetic Interruption. Reprod. Sci. 2022;29:1697–1709. doi: 10.1007/s43032-021-00638-8. PubMed DOI PMC
Cox C.M., Thoma M.E., Tchangalova N., Mburu G., Bornstein M.J., Johnson C.L., Kiarie J. Infertility prevalence and the methods of estimation from 1990 to 2021: A systematic review and meta-analysis. Hum. Reprod. Open. 2022;2022:hoac051. doi: 10.1093/hropen/hoac051. PubMed DOI PMC
Mazzilli R., Rucci C., Vaiarelli A., Cimadomo D., Ubaldi F.M., Foresta C., Ferlin A. Male factor infertility and assisted reproductive technologies: Indications, minimum access criteria and outcomes. J. Endocrinol. Investig. 2023;46:1079–1085. doi: 10.1007/s40618-022-02000-4. PubMed DOI PMC
Xie C., Chen X., Liu Y., Wu Z., Ping P. Multicenter study of genetic abnormalities associated with severe oligospermia and non-obstructive azoospermia. J. Int. Med. Res. 2018;46:107–114. doi: 10.1177/0300060517718771. PubMed DOI PMC
Colaco S., Modi D. Genetics of the human Y chromosome and its association with male infertility. Reprod. Biol. Endocrinol. 2018;16:14. doi: 10.1186/s12958-018-0330-5. PubMed DOI PMC
Bardoni B., Zuffardi O., Guioli S., Ballabio A., Simi P., Cavalli P., Grimoldi M.G., Fraccaro M., Camerino G. A deletion map of the human Yq11 region: Implications for the evolution of the Y chromosome and tentative mapping of a locus involved in spermatogenesis. Genomics. 1991;11:443–451. doi: 10.1016/0888-7543(91)90153-6. PubMed DOI
Rabinowitz M.J., Huffman P.J., Haney N.M., Kohn T.P. Y-Chromosome Microdeletions: A Review of Prevalence, Screening, and Clinical Considerations. Appl. Clin. Genet. 2021;14:51–59. doi: 10.2147/TACG.S267421. PubMed DOI PMC
Foresta C., Moro E., Ferlin A. Y chromosome microdeletions and alterations of spermatogenesis. Endocr. Rev. 2001;22:226–239. PubMed
Vogt P.H., Edelmann A., Kirsch S., Henegariu O., Hirschmann P., Kiesewetter F., Kohn F.M., Schill W.B., Farah S., Ramos C., et al. Human Y chromosome azoospermia factors (AZF) mapped to different subregions in Yq11. Hum. Mol. Genet. 1996;5:933–943. doi: 10.1093/hmg/5.7.933. PubMed DOI
SAl-Ouqaili M.T., Al-Ani S.K., Alaany R., Al-Qaisi M.N. Detection of partial and/or complete Y chromosome microdeletions of azoospermia factor a (AZFa) sub-region in infertile Iraqi patients with azoospermia and severe oligozoospermia. J. Clin. Lab. Anal. 2022;36:e24272. doi: 10.1002/jcla.24272. PubMed DOI PMC
Repping S., Skaletsky H., Lange J., Silber S., Van Der Veen F., Oates R.D., Page D.C., Rozen S. Recombination between palindromes P5 and P1 on the human Y chromosome causes massive deletions and spermatogenic failure. Am. J. Hum. Genet. 2002;71:906–922. doi: 10.1086/342928. PubMed DOI PMC
Suganthi R., Vijesh V.V., Vandana N., Fathima Ali Benazir J. Y choromosomal microdeletion screening in the workup of male infertility and its current status in India. Int. J. Fertil. Steril. 2014;7:253–266. PubMed PMC
Navarro-Costa P., Plancha C.E., Goncalves J. Genetic dissection of the AZF regions of the human Y chromosome: Thriller or filler for male (in) fertility? J. Biomed. Biotechnol. 2010;2010:936569. doi: 10.1155/2010/936569. PubMed DOI PMC
Yuen W., Golin A.P., Flannigan R., Schlegel P.N. Histology and sperm retrieval among men with Y chromosome microdeletions. Transl. Androl. Urol. 2021;10:1442–1456. doi: 10.21037/tau.2020.03.35. PubMed DOI PMC
Kuroda-Kawaguchi T., Skaletsky H., Brown L.G., Minx P.J., Cordum H.S., Waterston R.H., Wilson R.K., Silber S., Oates R., Rozen S., et al. The AZFc region of the Y chromosome features massive palindromes and uniform recurrent deletions in infertile men. Nat. Genet. 2001;29:279–286. doi: 10.1038/ng757. PubMed DOI
Vogt P.H., Bender U., Deibel B., Kiesewetter F., Zimmer J., Strowitzki T. Human AZFb deletions cause distinct testicular pathologies depending on their extensions in Yq11 and the Y haplogroup: New cases and review of literature. Cell Biosci. 2021;11:60. doi: 10.1186/s13578-021-00551-2. PubMed DOI PMC
Witherspoon L., Dergham A., Flannigan R. Y-microdeletions: A review of the genetic basis for this common cause of male infertility. Transl. Androl. Urol. 2021;10:1383–1390. doi: 10.21037/tau-19-599. PubMed DOI PMC
Klinefelter H.F., Jr., Reifenstein E.C., Jr., Albright F., Jr. Syndrome characterized by gynecomastia, aspermatogenesis without A-Leydigism, and increased excretion of follicle-stimulating hormone. J. Clin. Endocrinol. 1942;2:615–627. doi: 10.1210/jcem-2-11-615. DOI
Groth K.A., Skakkebæk A., Høst C., Gravholt C.H., Bojesen A. Klinefelter syndrome—A clinical update. J. Clin. Endocrinol. Metab. 2013;98:20–30. doi: 10.1210/jc.2012-2382. PubMed DOI
Rodrigues V.O., Polisseni F., Pannain G.D., Carvalho M.A.G. Genetics in human reproduction. JBRA Assist. Reprod. 2020;24:480–491. doi: 10.5935/1518-0557.20200007. PubMed DOI PMC
Thomas N., Hassold T. Aberrant recombination and the origin of Klinefelter syndrome. Hum. Reprod. Update. 2003;9:309–317. doi: 10.1093/humupd/dmg028. PubMed DOI
Jo D.G., Seo J.T., Lee J.S., Park S.Y., Kim J.W. Klinefelter syndrome diagnosed by prenatal screening tests in high-risk groups. Korean J. Urol. 2013;54:263. doi: 10.4111/kju.2013.54.4.263. PubMed DOI PMC
Bonomi M., Rochira V., Pasquali D., Balercia G., Jannini E., Ferlin A. Klinefelter syndrome (KS): Genetics, clinical phenotype and hypogonadism. J. Endocrinol. Investig. 2017;40:123–134. doi: 10.1007/s40618-016-0541-6. PubMed DOI PMC
Lanfranco F., Kamischke A., Zitzmann M., Nieschlag E. Klinefelter’s syndrome. Lancet. 2004;364:273–283. doi: 10.1016/S0140-6736(04)16678-6. PubMed DOI
Turriff A., Macnamara E., Levy H.P., Biesecker B. The impact of living with Klinefelter syndrome: A qualitative exploration of adolescents and adults. J. Genet. Couns. 2017;26:728–737. doi: 10.1007/s10897-016-0041-z. PubMed DOI PMC
Høst C., Skakkebæk A., Groth K.A., Bojesen A. The role of hypogonadism in Klinefelter syndrome. Asian J. Androl. 2014;16:185–191. doi: 10.4103/1008-682X.122201. PubMed DOI PMC
Liu S., Yuan T., Song S., Chen S., Wang L., Fu Y., Dong Y., Tang Y., Zhao W. Glucose metabolic disorder in Klinefelter syndrome: A retrospective analysis in a single Chinese hospital and literature review. BMC Endocr. Disord. 2021;21:239. doi: 10.1186/s12902-021-00893-5. PubMed DOI PMC
O’Connor M.J., Snyder E.A., Hayes F.J. Klinefelter syndrome and diabetes. Curr. Diabetes Rep. 2019;19:1–6. doi: 10.1007/s11892-019-1197-3. PubMed DOI
Bojesen A., Juul S., Birkebæk N.H., Gravholt C.H. Morbidity in Klinefelter syndrome: A Danish register study based on hospital discharge diagnoses. J. Clin. Endocrinol. Metab. 2006;91:1254–1260. doi: 10.1210/jc.2005-0697. PubMed DOI
Davis S.M., DeKlotz S., Nadeau K.J., Kelsey M.M., Zeitler P.S., Tartaglia N.R. High prevalence of cardiometabolic risk features in adolescents with 47,XXY/Klinefelter syndrome. Am. J. Med. Genet. C Semin. Med. Genet. 2020;184:327–333. doi: 10.1002/ajmg.c.31784. PubMed DOI PMC
Agarwal S., Dekam M. Multiple cardiac anomalies in an elderly man with Klinefelter’s syndrome. Singap. Med. J. 2011;52:e15–e17. PubMed
Jørgensen I.N., Skakkebaek A., Andersen N.H., Pedersen L.N., Hougaard D.M., Bojesen A., Trolle C., Gravholt C.H. Short QTc interval in males with klinefelter syndrome—Influence of CAG repeat length, body composition, and testosterone replacement therapy. Pacing Clin. Electrophysiol. 2015;38:472–482. doi: 10.1111/pace.12580. PubMed DOI
Zitzmann M., Bongers R., Werler S., Bogdanova N., Wistuba J., Kliesch S., Gromoll J., Tüttelmann F. Gene expression patterns in relation to the clinical phenotype in Klinefelter syndrome. J. Clin. Endocrinol. Metab. 2015;100:E518–E523. doi: 10.1210/jc.2014-2780. PubMed DOI
Fricke G., Mattern H., Schweikert H., Schwanitz G. Klinefelter’s syndrome and mitral valve prolapse. An echocardiographic study in twenty-two patients. Biomed. Pharmacother. 1984;38:88–97. PubMed
Pasquali D., Arcopinto M., Renzullo A., Rotondi M., Accardo G., Salzano A., Esposito D., Saldamarco L., Isidori A.M., Marra A.M., et al. Cardiovascular abnormalities in Klinefelter syndrome. Int. J. Cardiol. 2013;168:754–759. doi: 10.1016/j.ijcard.2012.09.215. PubMed DOI
Shiraishi K., Matsuyama H. Klinefelter syndrome: From pediatrics to geriatrics. Reprod. Med. Biol. 2019;18:140–150. doi: 10.1002/rmb2.12261. PubMed DOI PMC
Turriff A., Levy H.P., Biesecker B. Prevalence and psychosocial correlates of depressive symptoms among adolescents and adults with Klinefelter syndrome. Genet. Med. 2011;13:966–972. doi: 10.1097/GIM.0b013e3182227576. PubMed DOI PMC
Sasco A.J., Lowenfels A.B., Jong P.P.D. epidemiology of male breast cancer. A meta-analysis of published case-control studies and discussion of selected aetiological factors. Int. J. Cancer. 1993;53:538–549. doi: 10.1002/ijc.2910530403. PubMed DOI
Völkl T.M., Langer T., Aigner T., Greess H., Beck J.D., Rauch A.M., Dörr H.G. Klinefelter syndrome and mediastinal germ cell tumors. Am. J. Med. Genet. Part A. 2006;140:471–481. doi: 10.1002/ajmg.a.31103. PubMed DOI
Gómez-Raposo C., Tévar F.Z., Moyano M.S., Gómez M.L., Casado E. Male breast cancer. Cancer Treat. Rev. 2010;36:451–457. doi: 10.1016/j.ctrv.2010.02.002. PubMed DOI
Brinton L.A. Breast cancer risk among patients with Klinefelter syndrome. Acta Paediatr. 2011;100:814–818. doi: 10.1111/j.1651-2227.2010.02131.x. PubMed DOI PMC
De Sanctis V., Fiscina B., Soliman A., Giovannini M., Yassin M. Klinefelter syndrome and cancer: From childhood to adulthood. Pediatr. Endocrinol. Rev. 2013;11:44–50. PubMed
Ji J., Zöller B., Sundquist J., Sundquist K. Risk of solid tumors and hematological malignancy in persons with Turner and Klinefelter syndromes: A national cohort study. Int. J. Cancer. 2016;139:754–758. doi: 10.1002/ijc.30126. PubMed DOI
Lazúrová I., Rovenský J., Imrich R., Blažíčková S., Lazúrová Z., Payer J. Autoimmune rheumatic diseases and Klinefelter syndrome Autoimunitné reumatické choroby a Klinefelterov syndróm. Eur. Pharm. J. 2016;63:18–22. doi: 10.1515/afpuc-2016-0017. DOI
Dode C., Hardelin J.P. Kallmann syndrome. Eur. J. Hum. Genet. 2009;17:139–146. doi: 10.1038/ejhg.2008.206. PubMed DOI PMC
Shima H., Tokuhiro E., Okamoto S., Nagamori M., Ogata T., Narumi S., Nakamura A., Izumi Y., Jinno T., Suzuki E., et al. SOX10 Mutation Screening for 117 Patients with Kallmann Syndrome. J. Endocr. Soc. 2021;5:bvab056. doi: 10.1210/jendso/bvab056. PubMed DOI PMC
Marhari H., Chahdi Ouazzani F.Z., Ouahabi H.E., Bouguenouch L. Le syndrome de Kallmann-de Morsier: À propos de trois cas [Kallmann-de Morsier syndrome: About 3 cases] Pan Afr. Med. J. 2019;33:221. doi: 10.11604/pamj.2019.33.221.11678. PubMed DOI PMC
Maestre de San Juan A. Teratolagia: Falta total de los nervios olfactorios con anosmia en un individuo en quien existia una atrofifia congenita de los testiculos y miembro viril. El Siglo Me’dico. 1856;3:211–221.
Kallmann F.J., Schoenfeld W.A., Barrera S.E. The genetic aspects of primary eunuchoidism. Am. J. Ment. Defificiency. 1944;158:203–236.
Stamou M.I., Georgopoulos N.A. Kallmann syndrome: Phenotype and genotype of hypogonadotropic hypogonadism. Metabolism. 2018;86:124–134. doi: 10.1016/j.metabol.2017.10.012. PubMed DOI PMC
Hu Y., Tanriverdi F., MacColl G.S., Bouloux P.M. Kallmann syndrome: Molecular pathogenesis. Int. J. Biochem. Cell. Biol. 2003;35:1157–1162. doi: 10.1016/S1357-2725(02)00395-3. PubMed DOI
Dode C., Teixetra L., Levillers Fouveaut C., Bouchard P., Kottler M.L., Lespinasse J., Lienhardt-Roussie A., Mathieu M., Moerman A., Morgan G. Kallmann syndrome: Mutations in the genes encoding prokineticin-2 and prokineticin receptor-2. PLoS Genet. 2006;2:1648–1652. doi: 10.1371/journal.pgen.0020175. PubMed DOI PMC
Ogata T., Fujiwara I., Ogawa E., Sato N., Udaka T., Kosaki K. Kallman syndrome phenotype in a female patient with CHARGE syndrome and CHD7 mutation. Endocr J. 2006;53:741–743. doi: 10.1507/endocrj.K06-099. PubMed DOI
Young J., Xu C., Papadakis G.E., Acierno J.S., Maione L., Hietamäki J., Raivio T., Pitteloud N. Clinical Management of Congenital Hypogonadotropic Hypogonadism. Endocr. Rev. 2019;40:669–710. doi: 10.1210/er.2018-00116. PubMed DOI
Gu W.J., Zhang Q., Wang Y.Q., Yang G.Q., Hong T.P., Zhu D.L., Yang J.K., Ning G., Jin N., Chen K., et al. Mutation analyses in pedigrees and sporadic cases of ethnic Han Chinese Kallmann syndrome patients. Exp. Biol. Med. 2015;240:1480–1489. doi: 10.1177/1535370215587531. PubMed DOI PMC
Soussi-Yanicostas N., Faivre-Sarrailh C., Hardelin J.P., Levilliers J., Rougon G., Petit C. Anosmin-1 underlying the X chromosomelinked Kallmann syndrome is an adhesion molecule that can modulate neurite growth in a cell-type specifific manner. J. Cell Sci. 1998;111:2953–2965. doi: 10.1242/jcs.19.111.2953. PubMed DOI
Soussi-Yanicostas N., de Castro F., Julliard A.K., Perfettini I., Chedotal A., Petit C. Anosmin1, defective in the X-linked form of Kallmann syndrome, promotes axonal branch formation from olfactory bulb output neurons. Cell. 2002;109:217–228. doi: 10.1016/S0092-8674(02)00713-4. PubMed DOI
Gonzalez-Martinez D., Kim S.H., Hu Y., Guimond S., Schofifield J., Winyard P., Vannelli G.B., Turnbull J., Bouloux P.M. Anosmin-1 modulates fifibroblast growth factor receptor 1 signaling in human gonadotropinreleasing hormone olfactory neuroblasts through a heparan sulfatedependent mechanism. J. Neurosci. 2004;24:10384–10392. doi: 10.1523/JNEUROSCI.3400-04.2004. PubMed DOI PMC
Hardelin J.P., Levilliers J., Blanchard S., Carel J.C., Leutenegger M., Pinard-ertelletto J.P., Bouloux P., Petit C. Heterogeneity in the mutations responsible for X chromosome-linked Kallmann syndrome. Hum. Mol. Genet. 1993;2:373–377. doi: 10.1093/hmg/2.4.373. PubMed DOI
Quinton R., Duke V.M., de Zoysa P.A.R., Platts A.D., Valentine A., Kendall B., Pickman S., Kirk J.M., Besser G.M., Jacobs H.S., et al. The neuroradiology of Kallmann’s syndrome: A genotypic and phenotypic analysis. J. Clin. Endocrinol. Metab. 1996;81:3010–3017. doi: 10.1210/jcem.81.8.8768867. PubMed DOI
Albuisson J., Pecheux C., Carel J.C., Lacombe D., Leheup B., Lapuzina P., Bouchard P., Legius E., Matthijs G., Wasniewska M., et al. Kallmann syndrome: 14 novel mutations in KAL1 and FGFR1 (KAL2) Hum. Mutat. 2005;25:98–99. doi: 10.1002/humu.9298. PubMed DOI
Dode C., Levilliers J., Dupont J.M., De Paepe A., Le Du N., SoussiYanicostas N., Coimbra R.S., Delmaghani S., Compain-Nouaille S., Baverel F., et al. Loss of function mutations in FGFR1 cause autosomal dominant Kallmann syndrome. Nat. Genet. 2003;33:463–465. doi: 10.1038/ng1122. PubMed DOI
Sato N., Katsumata N., Kagami M., Hasegawa T., Hori X., Kawakita S., Minowada S., Shimotsuka A., Shishiba Y., Yokozawa M., et al. Clinical assessment and mutation analysis of Kallmann syndrome 1 (KAL1) and fifibroblast growth factor receptor 1 (FGFR1, or KAL2) in five families and 18 sporadic patients. J. Clin. Endocrinol. Metab. 2004;89:1079–1088. doi: 10.1210/jc.2003-030476. PubMed DOI
Stamou M.I., Cox K.H., Crowley W.F., Jr. Discovering genes essential to the hypothalamic regulation of human reproduction using a human disease model: Adjusting to life in the “-omics” era. Endocr. Rev. 2015;36:603–621. doi: 10.1210/er.2015-1045. PubMed DOI PMC
Topaloglu A.K., Kotan L.D. Genetics of hypogonadotropic hypogonadism. Endocr. Dev. 2016;29:36–49. PubMed
Cariboni A., Balasubramanian R. Kallmann syndrome and idiopathic hypogonadotropic hypogonadism: The role of semaphorin signaling on GnRH neurons. Handb. Clin. Neurol. 2021;182:307–315. PubMed PMC
Lacal I., Ventura R. Epigenetic Inheritance: Concepts, Mechanisms and Perspectives. Front. Mol. Neurosci. 2018;11:292. doi: 10.3389/fnmol.2018.00292. PubMed DOI PMC
Nilsson E.E., Ben Maamar M., Skinner M.K. Role of epigenetic transgenerational inheritance in generational toxicology. Environ. Epigenet. 2022;8:dvac001. doi: 10.1093/eep/dvac001. PubMed DOI PMC
Zheng X., Li Z., Wang G., Wang H., Zhou Y., Zhao X., Cheng C.Y., Qiao Y., Sun F. Sperm epigenetic alterations contribute to inter- and transgenerational effects of paternal exposure to long-term psychological stress via evading offspring embryonic reprogramming. Cell Discov. 2021;7:101. doi: 10.1038/s41421-021-00343-5. PubMed DOI PMC
Allegrucci C., Thurston A., Lucas E., Young L. Epigenetics and the germline. Reproduction. 2005;129:137–149. doi: 10.1530/rep.1.00360. PubMed DOI
Kiselev I.S., Kulakova O.G., Boyko A.N., Favorova O.O. DNA Methylation As an Epigenetic Mechanism in the Development of Multiple Sclerosis. Acta Naturae. 2021;13:45–57. doi: 10.32607/actanaturae.11043. PubMed DOI PMC
Shanthikumar S., Neeland M.R., Maksimovic J., Ranganathan S.C., Saffery R. DNA methylation biomarkers of future health outcomes in children. Mol. Cell Pediatr. 2020;7:7. doi: 10.1186/s40348-020-00099-0. PubMed DOI PMC
Luján S., Caroppo E., Niederberger C., Arce J.-C., Sadler-Riggleman I., Beck D., Nilsson E., Skinner M.K. Sperm DNA methylation epimutation biomarkers for male infertility and FSH therapeutic responsiveness. Sci. Rep. 2019;9:16786. doi: 10.1038/s41598-019-52903-1. PubMed DOI PMC
Ichiyanagi T., Ichiyanagi K., Miyake M., Sasaki H. Accumulation and loss of asymmetric non-CpG methylation during male germ-cell development. Nucleic Acids Res. 2013;41:738–745. doi: 10.1093/nar/gks1117. PubMed DOI PMC
Gkountela S., Zhang K.X., Shafiq T.A., Liao W.-W., Hargan-Calvopiña J., Chen P.-Y., Clark A.T. DNA demethylation dynamics in the human prenatal germline. Cell. 2015;161:1425–1436. doi: 10.1016/j.cell.2015.05.012. PubMed DOI PMC
Tang W.W., Dietmann S., Irie N., Leitch H.G., Floros V.I., Bradshaw C.R., Hackett J.A., Chinnery P.F., Surani M.A. A unique gene regulatory network resets the human germline epigenome for development. Cell. 2015;161:1453–1467. doi: 10.1016/j.cell.2015.04.053. PubMed DOI PMC
Rousseaux S., Khochbin S. Histone acylation beyond acetylation: Terra incognita in chromatin biology. Cell J. 2015;17:1. PubMed PMC
Henikoff S., Smith M.M. Histone variants and epigenetics. Cold Spring Harb. Perspect. Biol. 2015;7:a019364. doi: 10.1101/cshperspect.a019364. PubMed DOI PMC
Gaucher J., Reynoird N., Montellier E., Boussouar F., Rousseaux S., Khochbin S. From meiosis to postmeiotic events: The secrets of histone disappearance. FEBS J. 2010;277:599–604. doi: 10.1111/j.1742-4658.2009.07504.x. PubMed DOI
Goudarzi A., Zhang D., Huang H., Barral S., Kwon O.K., Qi S., Tang Z., Buchou T., Vitte A.-L., He T., et al. Dynamic competing histone H4 K5K8 acetylation and butyrylation are hallmarks of highly active gene promoters. Mol. Cell. 2016;62:169–180. doi: 10.1016/j.molcel.2016.03.014. PubMed DOI PMC
Barral S., Morozumi Y., Tanaka H., Montellier E., Govin J., de Dieuleveult M., Charbonnier G., Coute Y., Puthier D., Buchou T., et al. Histone variant H2A. L. 2 guides transition protein-dependent protamine assembly in male germ cells. Mol. Cell. 2017;66:89–101.e8. doi: 10.1016/j.molcel.2017.02.025. PubMed DOI
Skinner M.K., Maamar M.B., Sadler-Riggleman I., Beck D., Nilsson E., McBirney M., Klukovich R., Xie Y., Tang C., Yan W. Alterations in sperm DNA methylation, non-coding RNA and histone retention associate with DDT-induced epigenetic transgenerational inheritance of disease. Epigenetics Chromatin. 2018;11:1–24. doi: 10.1186/s13072-018-0178-0. PubMed DOI PMC
Carrell D.T., Emery B.R., Hammoud S. The aetiology of sperm protamine abnormalities and their potential impact on the sperm epigenome. Int. J. Androl. 2008;31:537–545. doi: 10.1111/j.1365-2605.2008.00872.x. PubMed DOI
Maamar M.B., Beck D., Nilsson E., McCarrey J.R., Skinner M.K. Developmental origins of transgenerational sperm histone retention following ancestral exposures. Dev. Biol. 2020;465:31–45. doi: 10.1016/j.ydbio.2020.06.008. PubMed DOI PMC
Hammoud S.S., Nix D.A., Hammoud A.O., Gibson M., Cairns B.R., Carrell D.T. Genome-wide analysis identifies changes in histone retention and epigenetic modifications at developmental and imprinted gene loci in the sperm of infertile men. Hum. Reprod. 2011;26:2558–2569. doi: 10.1093/humrep/der192. PubMed DOI PMC
Ihara M., Meyer-Ficca M.L., Leu N.A., Rao S., Li F., Gregory B.D., Zalenskaya I.A., Schultz R.M., Meyer R.G. Paternal poly (ADP-ribose) metabolism modulates retention of inheritable sperm histones and early embryonic gene expression. PLoS Genet. 2014;10:e1004317. doi: 10.1371/journal.pgen.1004317. PubMed DOI PMC
Luense L.J., Wang X., Schon S.B., Weller A.H., Shiao E.L., Bryant J.M., Bartolomei M.S., Coutifaris C., Garcia B.A., Berger S.L. Comprehensive analysis of histone post-translational modifications in mouse and human male germ cells. Epigenetics Chromatin. 2016;9:24. doi: 10.1186/s13072-016-0072-6. PubMed DOI PMC
Van der Heijden G.W., Ramos L., Baart E.B., van den Berg I.M., Derijck A.A., van der Vlag J., Martini E., de Boer P. Sperm-derived histones contribute to zygotic chromatin in humans. BMC Dev. Biol. 2008;8:34. doi: 10.1186/1471-213X-8-34. PubMed DOI PMC
Carone B.R., Hung J.-H., Hainer S.J., Chou M.-T., Carone D.M., Weng Z., Fazzio T.G., Rando O.J. High-resolution mapping of chromatin packaging in mouse embryonic stem cells and sperm. Dev. Cell. 2014;30:11–22. doi: 10.1016/j.devcel.2014.05.024. PubMed DOI PMC
Samans B., Yang Y., Krebs S., Sarode G.V., Blum H., Reichenbach M., Wolf E., Steger K., Dansranjavin T., Schagdarsurengin U. Uniformity of nucleosome preservation pattern in Mammalian sperm and its connection to repetitive DNA elements. Dev. Cell. 2014;30:23–35. doi: 10.1016/j.devcel.2014.05.023. PubMed DOI
Kurimoto K., Saitou M., editors. Cold Spring Harbor Symposia on Quantitative Biology. Cold Spring Harbor Laboratory Press; New York, NY, USA: 2015. Mechanism and reconstitution in vitro of germ cell development in mammals. PubMed
Teperek M., Simeone A., Gaggioli V., Miyamoto K., Allen G.E., Erkek S., Kwon T., Marcotte E.M., Zegerman P., Bradshaw C.R., et al. Sperm is epigenetically programmed to regulate gene transcription in embryos. Genome Res. 2016;26:1034–1046. doi: 10.1101/gr.201541.115. PubMed DOI PMC
Bao J., Bedford M.T. Epigenetic regulation of the histone-to-protamine transition during spermiogenesis. Reproduction. 2016;151:R55. doi: 10.1530/REP-15-0562. PubMed DOI PMC
Miller D., Brinkworth M., Iles D. Paternal DNA packaging in spermatozoa: More than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction. 2010;139:287–301. doi: 10.1530/REP-09-0281. PubMed DOI
Rivera C., Gurard-Levin Z.A., Almouzni G., Loyola A. Histone lysine methylation and chromatin replication. Biochim. Biophys. Acta-Gene Regul. Mech. 2014;1839:1433–1439. doi: 10.1016/j.bbagrm.2014.03.009. PubMed DOI
Verma A., Rajput S., Kumar S., De S., Chakravarty A.K., Kumar R., Datta T.K. Differential histone modification status of spermatozoa in relation to fertility of buffalo bulls. J. Cell. Biochem. 2015;116:743–753. doi: 10.1002/jcb.25029. PubMed DOI
Kutchy N., Menezes E., Chiappetta A., Tan W., Wills R.W., Kaya A., Topper E., Moura A.A., Perkins A.D., Memili E. Acetylation and methylation of sperm histone 3 lysine 27 (H3K27ac and H3K27me3) are associated with bull fertility. Andrologia. 2018;50:e12915. doi: 10.1111/and.12915. PubMed DOI
Barratt C.L., Aitken R.J., Björndahl L., Carrell D.T., de Boer P., Kvist U., Lewis S.E., Perreault S.D., Perry M.J., Ramos L., et al. Sperm DNA: Organization, protection and vulnerability: From basic science to clinical applications—A position report. Hum. Reprod. 2010;25:824–838. doi: 10.1093/humrep/dep465. PubMed DOI
Yamauchi Y., Shaman J.A., Boaz S.M., Ward W.S. Paternal pronuclear DNA degradation is functionally linked to DNA replication in mouse oocytes. Biol. Reprod. 2007;77:407–415. doi: 10.1095/biolreprod.107.061473. PubMed DOI
Shaman J.A., Yamauchi Y., Steven Ward W. Function of the sperm nuclear matrix. Arch. Androl. 2007;53:135–140. doi: 10.1080/01485010701329378. PubMed DOI
Barbu M.G., Thompson D.C., Suciu N., Voinea S.C., Cretoiu D., Predescu D.V. The Roles of MicroRNAs in Male Infertility. Int. J. Mol. Sci. 2021;22:2910. doi: 10.3390/ijms22062910. PubMed DOI PMC
Cecere G. Small RNAs in epigenetic inheritance: From mechanisms to trait transmission. FEBS Lett. 2021;595:2953–2977. doi: 10.1002/1873-3468.14210. PubMed DOI PMC
Suh N., Blelloch R. Small RNAs in early mammalian development: From gametes to gastrulation. Development. 2011;138:1653–1661. doi: 10.1242/dev.056234. PubMed DOI PMC
Du W., Yang W., Xuan J., Gupta S., Krylov S.N., Ma X., Yang Q., Yang B.Z. Reciprocal regulation of miRNAs and piRNAs in embryonic development. Cell Death Differ. 2016;23:1458–1470. doi: 10.1038/cdd.2016.27. PubMed DOI PMC
Yuan S., Schuster A., Tang C., Yu T., Ortogero N., Bao J., Zheng H., Yan W. Sperm-borne miRNAs and endo-siRNAs are important for fertilization and preimplantation embryonic development. Dev. Camb. Engl. 2016;143:635e47. doi: 10.1242/dev.131755. PubMed DOI PMC
Champroux A., Cocquet J., Henry-Berger J., Drevet J.R., Kocer A. A decade of exploring the mammalian sperm epigenome: Paternal epigenetic and transgenerational inheritance. Front. Cell Dev. Biol. 2018;6:50. doi: 10.3389/fcell.2018.00050. PubMed DOI PMC
Sharma U., Conine C.C., Shea J.M., Boskovic A., Derr A.G., Bing X.Y., Belleannee C., Kucukural A., Serra R.W., Sun F., et al. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science. 2016;351:391–396. doi: 10.1126/science.aad6780. PubMed DOI PMC
Grandjean V., Fourré S., De Abreu D.A., Derieppe M.A., Remy J.J., Rassoulzadegan M. RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders. Sci. Rep. 2015;5:18193. doi: 10.1038/srep18193. PubMed DOI PMC
Chen Q., Yan M., Cao Z., Li X., Zhang Y., Shi J., Feng G.H., Peng H., Zhang X., Zhang Y., et al. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science. 2016;351:397–400. doi: 10.1126/science.aad7977. PubMed DOI
Yuan S., Schuster A., Tang C., Yu T., Ortogero N., Bao J., Zheng H., Yan W., Wang Z. Sperm-borne small RNA profiling reveals piRNAs in human seminal plasma. Oncotarget. 2020;11:55–70.
Sendler E., Johnson G.D., Mao S., Goodrich R.D., Diamond M.P., Hauser R., Krawetz S.A. The effect of smoking on the small non-coding RNAome in human sperm. Hum. Reprod. 2016;31:2525–2537.
Rodgers A.B., Morgan C.P., Leu N.A., Bale T.L. Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc. Natl. Acad. Sci. USA. 2015;112:13699–13704. doi: 10.1073/pnas.1508347112. PubMed DOI PMC
Fullston T., Ohlsson Teague E.M., Palmer N.O., DeBlasio M.J., Mitchell M., Corbett M., Print C.G., Owens J.A., Lane M. Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J. 2013;27:4226–4243. doi: 10.1096/fj.12-224048. PubMed DOI
Benchaib M., Braun V., Ressnikof D., Lornage J., Durand P., Niveleau A. Influence of global sperm DNA methylation on IVF results. Hum. Reprod. 2010;25:2158–2168. doi: 10.1093/humrep/deh684. PubMed DOI
Skakkebæk A., Viuff M., Nielsen M.M., Gravholt C.H., editors. American Journal of Medical Genetics Part C: Seminars in Medical Genetics. Wiley Online Library; Hoboken, NJ, USA: 2020. Epigenetics and genomics in Klinefelter syndrome. PubMed
Passerini V., Ozeri-Galai E., De Pagter M.S., Donnelly N., Schmalbrock S., Kloosterman W.P., Kerem B., Storchová Z. The presence of extra chromosomes leads to genomic instability. Nat. Commun. 2016;7:10754. doi: 10.1038/ncomms10754. PubMed DOI PMC
Jowhar Z., Shachar S., Gudla P.R., Wangsa D., Torres E., Russ J.L., Pegoraro G., Ried T., Raznahan A., Misteli T. Effects of human sex chromosome dosage on spatial chromosome organization. Mol. Biol. Cell. 2018;29:2458–2469. doi: 10.1091/mbc.E18-06-0359. PubMed DOI PMC
Migicovsky Z., Kovalchuk I. Epigenetic memory in mammals. Front. Genet. 2011;2:28. doi: 10.3389/fgene.2011.00028. PubMed DOI PMC
Tiffon C. The Impact of Nutrition and Environmental Epigenetics on Human Health and Disease. Int. J. Mol. Sci. 2018;19:3425. doi: 10.3390/ijms19113425. PubMed DOI PMC
Castillo J., Estanyol J.M., Ballescá J.L., Oliva R. Human sperm chromatin epigenetic potential: Genomics, proteomics, and male infertility. Asian J. Androl. 2015;17:601–609. doi: 10.4103/1008-682X.153302. PubMed DOI PMC
Barrachina F., Battistone M.A., Castillo J., Mallofré C., Jodar M., Breton S., Oliva R. Sperm acquire epididymis-derived proteins through epididymosomes. Hum. Reprod. 2022;37:651–668. doi: 10.1093/humrep/deac015. PubMed DOI PMC