114
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Observational methods for human studies of transgenerational effects

, , , , , & show all
Article: 2366065 | Received 02 Feb 2024, Accepted 05 Jun 2024, Published online: 13 Jun 2024

References

  • Kaati G, Bygren LO, Edvinsson S. Cardiovascular and diabetes mortality determined by nutrition during parents’ and grandparents’ slow growth period. Eur J Hum Genet. 2002;10(11):682–18. doi: 10.1038/sj.ejhg.5200859
  • Jablonka E, Noble D. Systemic integration of different inheritance systems. Curr Opin Syst Biol. 2019;13:52–58. doi: 10.1016/j.coisb.2018.10.002
  • Nilsson EE, Sadler-Riggleman I, Skinner MK, et al. Environmentally induced epigenetic transgenerational inheritance of disease. Environ Epigenet. 2018;4(2):dvy016. doi: 10.1093/eep/dvy016
  • Nilsson EE, Ben Maamar M, Skinner MK. Role of epigenetic transgenerational inheritance in generational toxicology. Environ Epigenet. 2022;8(1):dvac001. doi: 10.1093/eep/dvac001
  • Skinner MK, Manikkam M, Guerrero-Bosagna C. Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab. 2010;21(4):214–222. doi: 10.1016/j.tem.2009.12.007
  • van den Berg GJ, Pinger PR. Transgenerational effects of childhood conditions on third generation health and education outcomes. Econ Hum Biol. 2016;23:103–120. doi: 10.1016/j.ehb.2016.07.001
  • Rahman MF, McGowan PO. Cell-type-specific epigenetic effects of early life stress on the brain. Transl Psychiatry. 2022;12(1):326. doi: 10.1038/s41398-022-02076-9
  • Shi Y, Lan F, Matson C, et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell. 2004;119(7):941–953. doi: 10.1016/j.cell.2004.12.012
  • Tsukada YI, Fang J, Erdjument-Bromage H, et al. Histone demethylation by a family of JmjC domain-containing proteins. Nature. 2006;439(7078):811–816. doi: 10.1038/nature04433
  • Holliday R, Pugh JE. DNA modification mechanisms and gene activity during development: developmental clocks may depend on the enzymic modification of specific bases in repeated DNA sequences. Science. 1975;187(4173):226–232. doi: 10.1126/science.187.4173.226
  • Breton CV, Landon R, Kahn LG, et al. Exploring the evidence for epigenetic regulation of environmental influences on child health across generations. Commun Biol. 2021;4(1):769. doi: 10.1038/s42003-021-02316-6
  • Felsenfeld G. The evolution of epigenetics. Perspect Biol Med. 2014;57(1):132–148. doi: 10.1353/pbm.2014.0004
  • Pembrey M, Saffery R, Bygren LO. Human transgenerational responses to early-life experience: potential impact on development, health and biomedical research. J Med Genet. 2014;51(9):563–572. doi: 10.1136/jmedgenet-2014-102577
  • Skinner MK. What is an epigenetic transgenerational phenotype?: F3 or F2. Reprod Toxicol. 2008;25(1):2–6. doi: 10.1016/j.reprotox.2007.09.001
  • Skinner MK. Environmental stress and epigenetic transgenerational inheritance. BMC Med. 2014;12(1):1–5. doi: 10.1186/s12916-014-0153-y
  • Nava-Rivera LE, Betancourt-Martínez ND, Lozoya-Martinez R, et al. Transgenerational effects in DNA methylation, genotoxicity and reproductive phenotype by chronic arsenic exposure. Sci Rep. 2021;11(1):8276. doi: 10.1038/s41598-021-87677-y
  • Franzago M, Santurbano D, Vitacolonna E, et al. Genes and diet in the prevention of chronic diseases in future generations. Int J Mol Sci. 2020;21(7):2633. doi: 10.3390/ijms21072633
  • Kovalchuk I. Transgenerational epigenetic inheritance in animals. Front Genet. 2012;3:76. doi: 10.3389/fgene.2012.00076
  • Lettieri G, Marra F, Moriello C, et al. Molecular alterations in spermatozoa of a family case living in the land of fires—a first look at possible transgenerational effects of pollutants. Int J Mol Sci. 2020;21(18):6710. doi: 10.3390/ijms21186710
  • Wolstenholme JT, Edwards M, Shetty SR, et al. Gestational exposure to bisphenol a produces transgenerational changes in behaviors and gene expression. Endocrinology. 2012;153(8):3828–3838. doi: 10.1210/en.2012-1195
  • Clark J, Rager JE. Epigenetics: an overview of CpG methylation, chromatin remodeling, and regulatory/noncoding RNAs. Environ Epigenetin Toxicol Public Health. 2020;22:3–32.
  • Daxinger L, Whitelaw E. Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat Rev Genet. 2012;13(3):153–162. doi: 10.1038/nrg3188
  • Stener-Victorin E, Deng Q. Epigenetic inheritance of polycystic ovary syndrome—challenges and opportunities for treatment. Nat Rev Endocrinol. 2021;17(9):521–533. doi: 10.1038/s41574-021-00517-x
  • Chen Q, Yan W, Duan E. Epigenetic inheritance of acquired traits through sperm RNAs and sperm RNA modifications. Nat Rev Genet. 2016;17(12):733–743. doi: 10.1038/nrg.2016.106
  • Martos SN, Tang WY, Wang Z. Elusive inheritance: transgenerational effects and epigenetic inheritance in human environmental disease. Prog Biophys Mol Biol. 2015;118(1–2):44–54. doi: 10.1016/j.pbiomolbio.2015.02.011
  • Roseboom TJ, Watson ED. The next generation of disease risk: are the effects of prenatal nutrition transmitted across generations? Evidence from animal and human studies. Placenta. 2012;33:e40–e44. doi: 10.1016/j.placenta.2012.07.018
  • Pang TY, Short AK, Bredy TW, et al. Transgenerational paternal transmission of acquired traits: stress-induced modification of the sperm regulatory transcriptome and offspring phenotypes. Curr Opin Behav Sci. 2017;14:140–147. doi: 10.1016/j.cobeha.2017.02.007
  • Skinner MK, Nilsson EE. Role of environmentally induced epigenetic transgenerational inheritance in evolutionary biology: unified evolution theory. Environ Epigenet. 2021;7(1):dvab012. doi: 10.1093/eep/dvab012
  • Knudsen TM, Rezwan FI, Jiang Y, et al. Transgenerational and intergenerational epigenetic inheritance in allergic diseases. J Allergy Clin Immunol. 2018;142(3):765–772. doi: 10.1016/j.jaci.2018.07.007
  • Raherison C, Pénard-Morand C, Moreau D, et al. In utero and childhood exposure to parental tobacco smoke, and allergies in schoolchildren. Respir med. 2007;101(1):107–117. doi: 10.1016/j.rmed.2006.04.010
  • Sasco AJ, Vainio H. From in utero and childhood exposure to parental smoking to childhood cancer: a possible link and the need for action. Hum Exp Toxicol. 1999;18(4):192–201.
  • Dolinoy DC, Das R, Weidman JR, et al. Metastable epialleles, imprinting, and the fetal origins of adult diseases. Pediat Res. 2007;61(7):30–37. doi: 10.1203/pdr.0b013e31804575f7
  • Shukla A, Bunkar N, Kumar R, et al. Air pollution associated epigenetic modifications: transgenerational inheritance and underlying molecular mechanisms. Sci Total Environ. 2019;656:760–777. doi: 10.1016/j.scitotenv.2018.11.381
  • Whitelaw NC, Whitelaw E. Transgenerational epigenetic inheritance in health and disease. Curr Opin Genet Dev. 2008;18(3):273–279. doi: 10.1016/j.gde.2008.07.001
  • Mitchell M. Fitting issues: the visual representation of time in family tree diagrams. Σημειωτκή-Sign Syst Stud. 2014;42(2–3):241–280. doi: 10.12697/SSS.2014.42.2-3.05
  • Richards Steed R, Bakian AV, Smith KR, et al. Evidence of transgenerational effects on autism spectrum disorder using multigenerational space-time cluster detection. Int J Health Geogr. 2022;21(1):13. doi: 10.1186/s12942-022-00313-4
  • Anway MD, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors. Endocrinology. 2006;147(6):s43–s49. doi: 10.1210/en.2005-1058
  • Kubsad D, Nilsson EE, King SE, et al. Assessment of glyphosate induced epigenetic transgenerational inheritance of pathologies and sperm epimutations: generational toxicology. Sci Rep. 2019;9(1):6372. doi: 10.1038/s41598-019-42860-0
  • Rahman MS, Pang WK, Ryu DY, et al. Multigenerational and transgenerational impact of paternal bisphenol a exposure on male fertility in a mouse model. Hum Reprod. 2020;35(8):1740–1752.
  • Skinner MK, Nilsson E, Sadler-Riggleman I, et al. Transgenerational sperm DNA methylation epimutation developmental origins following ancestral vinclozolin exposure. Epigenetics. 2019;14(7):721–739.
  • Wolstenholme JT, Goldsby JA, Rissman EF Transgenerational effects of prenatal bisphenol a on social recognition. Horm Behav. 2013;64(5):833–839.
  • Nilsson EE, McBirney M, De Santos S, et al. Multiple generation distinct toxicant exposures induce epigenetic transgenerational inheritance of enhanced pathology and obesity. Environ Epigenet. 2023;9(1):dvad006. doi: 10.1093/eep/dvad006
  • US EPA. US environmental protection clean air act. 2024 [cited 2024 Jan 28]. Available from: https://www.epa.gov/clean-air-act-overview/clean-air-act-requirements-and-history
  • Bygren LO, Tinghög P, Carstensen J, et al. Change in paternal grandmothers´ early food supply influenced cardiovascular mortality of the female grandchildren. BMC Genet. 2014;15(1):1–6. doi: 10.1186/1471-2156-15-12
  • Pembrey ME, Bygren LO, Kaati G, et al. Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet. 2006;14(2):159–166. doi: 10.1038/sj.ejhg.5201538
  • Kaati G, Bygren LO, Pembrey M, et al. Transgenerational response to nutrition, early life circumstances and longevity. Eur J Hum Genet. 2007;15(7):784–790. doi: 10.1038/sj.ejhg.5201832
  • Laubenthal J, Zlobinskaya O, Poterlowicz K, et al. Cigarette smoke‐induced transgenerational alterations in genome stability in cord blood of human F1 offspring. FASEB J. 2012;26(10):3946–3956. doi: 10.1096/fj.11-201194
  • Golding J, Gregory S, Northstone K, et al. Human transgenerational observations of regular smoking before puberty on fat mass in grandchildren and great-grandchildren. Sci Rep. 2022;12(1):1139. doi: 10.1038/s41598-021-04504-0
  • Knox G. Epidemiology of childhood leukaemia in Northumberland and Durham. Br J Preventive Soc Medi. 1964;18(1):17. doi: 10.1136/jech.18.1.17
  • Hossain MM, Lawson AB, Cai B, et al. Space-time stick-breaking processes for small area disease cluster estimation. Environ Ecol Stat. 2013;20(1):91–107. doi: 10.1007/s10651-012-0209-0
  • Moore DA, Carpenter TE. Spatial analytical methods and geographic information systems: use in health research and epidemiology. Epidemiol Rev. 1999;21(2):143–161. doi: 10.1093/oxfordjournals.epirev.a017993
  • Selevan SG, Kimmel CA, Mendola P. Identifying critical windows of exposure for children’s health. Environ Health Perspect. 2000;108(suppl 3):451–455. doi: 10.1289/ehp.00108s3451
  • Constantino JN, Daniels J, Durkin MS, et al. “Prevalence and characteristics of autism spectrum disorder among children aged 4 years-early autism and developmental disabilities monitoring network, 7 sites, United States, 2010, 2012m 2014. 2019.
  • Croen LA, Najjar DV, Fireman B, et al. Maternal and paternal age and risk of autism spectrum disorders. Arch Pediatr Adolesc Med. 2007;161(4):334–340. doi: 10.1001/archpedi.161.4.334
  • Apa APA. Diagnostic and statistical manual of mental disorders. Am Psychiatric Assoc. 2013;5.
  • Gamsiz ED, Viscidi, EW, Frederick, AM, et al. Intellectual disability is associated with increased runs of homozygosity in simplex autism. Am J Hum Genet. 2013;93(1):103–109.
  • Lauritsen MB, Astrup A, Pedersen CB, et al. Urbanicity and autism spectrum disorders. J Autism Dev Disord. 2014;44(2):394–404.
  • Ozonoff S, Young GS, Carter A, et al. Recurrence risk for autism spectrum disorders: a baby siblings research consortium study. Pediatrics. 2011;128(3):e488–e495.
  • Sandin S, Hultman CM, Kolevzon A, et al. Advancing maternal age is associated with increasing risk for autism: a review and meta-analysis. J Am Acad Child Adolesc Psychiatry. 2012;51(5):477–486. doi: 10.1016/j.jaac.2012.02.018
  • Taylor MJ, Rosenqvist MA, Larsson H, et al. Etiology of autism spectrum disorders and autistic traits over time. JAMA Psychiatry. 2020;77(9):936–943. doi: 10.1001/jamapsychiatry.2020.0680
  • Bai D, Marrus N, Yip BHK, et al. Inherited risk for autism through maternal and paternal lineage. Biol Psychiatry. 2020;88(6):480–487.
  • Brandler WM, Antaki D, Gujral M, et al. Paternally inherited cis-regulatory structural variants are associated with autism. Science. 2018;360(6386):327–331. doi: 10.1126/science.aan2261
  • LaSalle JM. Epigenomic signatures reveal mechanistic clues and predictive markers for autism spectrum disorder. Mol Psychiatry. 2023;28(5):1890–1901. doi: 10.1038/s41380-022-01917-9
  • Dickerson AS, Rahbar MH, Han I, et al. Autism spectrum disorder prevalence and proximity to industrial facilities releasing arsenic, lead or mercury. Sci Total Environ. 2015;536:245–251.
  • Dickerson AS, Rahbar MH, Bakian AV, et al. Autism spectrum disorder prevalence and associations with air concentrations of lead, mercury, and arsenic. Environ Monit Assess. 2016;188(7):1–15.
  • Gong T, Dalman C, Wicks S, et al. Perinatal exposure to traffic-related air pollution and autism spectrum disorders. Environ Health Perspect. 2017;125(1):119.
  • Grindler N, Vanderlinden L, Karthikraj R, et al. Exposure to phthalate, an endocrine disrupting chemical, alters the first trimester placental methylome and transcriptome in women. Sci Rep. 2018;8(1):1–9.
  • Volk HE, Lurmann F, Penfold B, et al. Traffic-related air pollution, particulate matter, and autism. JAMA Psychiatry. 2013;70(1):71–77. doi: 10.1001/jamapsychiatry.2013.266
  • Windham GC, Zhang L, Gunier R, et al. Autism spectrum disorders in relation to distribution of hazardous air pollutants in the San Francisco Bay area. Environ Health Perspect. 2006;114(9):1438–1444.
  • Utah Registry for Autism and Developmental Disabilities, URADD. Available from: https://medicine.utah.edu/psychiatry/research/labs/uradd – Not an online resource.
  • Utah Population Database, UPDB. Available from: https://uofuhealth.utah.edu/huntsman/utah-population-database – Not an online resource.
  • SaTScan. Available from: https://maps.cancer.gov/overview/DCCPSGrants/abstract.jsp?applId=8635986&term=CA165057
  • Kulldorff M, Huang L, Pickle L, et al. An elliptic spatial scan statistic. Stat Med. 2006;25(22):3929–3943. doi: 10.1002/sim.2490
  • Nordsborg RB, Meliker JR, Ersbøll AK, et al. Space-time clusters of breast cancer using residential histories: a Danish case–control study. BMC Cancer. 2014;14(1):1–12. doi: 10.1186/1471-2407-14-255
  • Sloan C, Chandrasekhar R, Mitchel E, et al. Spatial and temporal clustering of patients hospitalized with laboratory-confirmed influenza in the United States. Epidemics. 2020;31:100387. doi: 10.1016/j.epidem.2020.100387
  • Ahmed AAM, Jui SJJ, Sharma E, et al. An advanced deep learning predictive model for air quality index forecasting with remote satellite-derived hydro-climatological variables. Sci Total Environ. 2024;906:167234. doi: 10.1016/j.scitotenv.2023.167234
  • VanDerslice J, Taddie MC, Curtin K, et al. Early life exposures associated with risk of small intestinal neuroendocrine tumors. PLOS ONE. 2020;15(4):e0231991. doi: 10.1371/journal.pone.0231991
  • Martinez-Zamudio R, Ha HC. Environmental epigenetics in metal exposure. Epigenetics. 2011;6(7):820–827. doi: 10.4161/epi.6.7.16250
  • Ke T, Tinkov AA, Skalny AV, et al. Epigenetics and methylmercury-induced neurotoxicity, evidence from experimental studies. Toxics. 2023;11(1):72. doi: 10.3390/toxics11010072
  • Ding M, Shi S, Qie S, et al. Association between heavy metals exposure (cadmium, lead, arsenic, mercury) and child autistic disorder: a systematic review and meta-analysis. Front Pediatr. 2023;11:11. doi: 10.3389/fped.2023.1169733
  • Ijomone OM, Olung NF, Akingbade GT, et al. Environmental influence on neurodevelopmental disorders: potential association of heavy metal exposure and autism. J Trace Elem Med Biol. 2020;62:126638. doi: 10.1016/j.jtemb.2020.126638
  • Long KR, DeYoung JH, Ludington SD. Database of significant deposits of gold, silver, copper, lead and zinc in the United States: part A: database description and analysis. US Geol Surv Open File Rep. 1998;95(3):629–644.
  • Martin A. Gold, Silver, Copper, Lead, and Zinc. Miner Yearb. 1947;1947:1504–1507.
  • Arai Y, Hayakawa K, Arai D, et al. Putative epimutagens in maternal peripheral and cord blood samples identified using human induced pluripotent stem cells. Biomed Res Int. 2015;2015:1–13. doi: 10.1155/2015/876047
  • Mitchell LE, Zajchowski CA. The history of air quality in Utah: a narrative review. Sustainability. 2022;14(15):9653. doi: 10.3390/su14159653
  • Kartchner AD. Air pollution control and abatement proceedings of a symposium. 1968.
  • Dye JA, Lehmann JR, McGee JK, et al. Acute pulmonary toxicity of particulate matter filter extracts in rats: coherence with epidemiologic studies in Utah Valley residents. Environ Health Perspect. 2001;109(suppl 3):395–403. doi: 10.1289/ehp.01109s3395
  • Sobolewski M, Abston K, Conrad K, et al. Lineage-and sex-dependent behavioral and biochemical transgenerational consequences of developmental exposure to lead, prenatal stress, and combined lead and prenatal stress in mice. Environ Health Perspect. 2020;128(2):027001. doi: 10.1289/EHP4977
  • Maccani JZ, Koestler DC, Houseman EA, et al. DNA methylation changes in the placenta are associated with fetal manganese exposure. Reprod Toxicol. 2015;57:43–49. doi: 10.1016/j.reprotox.2015.05.002
  • Wang L, Shiraki A, Itahashi M, et al. Aberration in epigenetic gene regulation in hippocampal neurogenesis by developmental exposure to manganese chloride in mice. Toxicol Sci. 2013;136(1):154–165. doi: 10.1093/toxsci/kft183
  • Gaspari L, Soyer-Gobillard MO, Rincheval N, et al. Birth outcomes in DES children and grandchildren: a multigenerational national cohort study on informative families. Int J Environ Res Public Health. 2023;20(3):2542. doi: 10.3390/ijerph20032542
  • Yim G, Roberts A, Ascherio A, et al. Smoking during pregnancy and risk of attention-deficit/hyperactivity disorder in the third generation. Epidemiology. 2022;33(3):431–440. doi: 10.1097/EDE.0000000000001467
  • US EPA. Environmental protection agency air quality system data mart [internet database] available via. 2024 [cited 2024 Jan 28]. Available from: https://www.epa.gov/outdoor-air-quality-data
  • McGee G, Perkins NJ, Mumford SL, et al. Methodological issues in population-based studies of multigenerational associations. Am J Epidemiol. 2020;189(12):1600–1609. doi: 10.1093/aje/kwaa125
  • Shafran-Nathan R, Levy I, Levin N, et al. Ecological bias in environmental health studies: the problem of aggregation of multiple data sources. Air Qual Atmos Health. 2017;10(4):411–420. doi: 10.1007/s11869-016-0436-x