24,149
Views
47
CrossRef citations to date
0
Altmetric
Research Paper

Cannabis use is associated with potentially heritable widespread changes in autism candidate gene DLGAP2 DNA methylation in sperm

, , , , , , , & ORCID Icon show all
Pages 161-173 | Received 14 Mar 2019, Accepted 08 Aug 2019, Published online: 26 Aug 2019

References

  • Gunn JK, Rosales CB, Center KE, et al. Prenatal exposure to cannabis and maternal and child health outcomes: a systematic review and meta-analysis. BMJ Open. 2016 Apr 5;6(4):e009986.
  • Smart R, Caulkins JP, Kilmer B, et al. Variation in cannabis potency and prices in a newly legal market: evidence from 30 million cannabis sales in Washington state. Addiction. 2017 Dec;112(12):2167–2177.
  • Berke J, Gould S. Illinois just became the first state to legalize marijuana sales through the legislature – here are all the states where marijuana is legal. 2018 cited 2019 Jun 25. Available from: https://www.businessinsider.com/legal-marijuana-states-2018-1.
  • Elsohly MA, Slade D. Chemical constituents of marijuana: the complex mixture of natural cannabinoids. Life Sci. 2005 Dec 22;78(5):539–548.
  • ElSohly MA, Mehmedic Z, Foster S, et al. Changes in cannabis potency over the last 2 decades (1995-2014): Analysis of current data in the United States. Biol Psychiatry. 2016 Apr 1;79(7):613–619.
  • Hasin DS. US epidemiology of cannabis use and associated problems. Neuropsychopharmacology. 2018 Jan;43(1):195–212.
  • Budney AJ, Roffman R, Stephens RS, et al. Marijuana dependence and its treatment. Addict Sci Clin Pract. 2007 Dec;4(1):4–16.
  • Lloyd D. JRAM, O’Malley PM, Bachman JG, et al. Monitoring the future. National survey results on drug use: The University of Michigan Institute for Social Research. 2017 cited 2018 Oct 29. Available from: http://www.monitoringthefuture.org/pubs/monographs/mtf-overview2017.pdf.
  • Azofeifa A, Mattson ME, Schauer G, et al. National estimates of marijuana use and related indicators — National survey on drug use and health. 2016 [cited 2018 oct]. Available from: https://www.cdc.gov/mmwr/volumes/65/ss/ss6511a1.htm.
  • Yahoo News/Marist Poll. Weed and the American family. 2017 cited 2018 Oct 29. Available from: http://maristpoll.marist.edu/wp-content/misc/Yahoo%20News/20170417_Banners%20of%20Americans_Yahoo%20News-Marist%20Poll_Weed%20and%20The%20American%20Family.pdf.
  • Illum LRH, Bak ST, Lund S, et al. DNA methylation in epigenetic inheritance of metabolic diseases through the male germ line. J Mol Endocrinol. 2018 Feb;60(2):R39–R56.
  • Dong C, Chen J, Harrington A, et al. Cannabinoid exposure during pregnancy and its impact on immune function. Cell Mol Life Sci. 2019;76(4):729–743.
  • Szutorisz H, DiNieri JA, Sweet E, et al. Parental THC exposure leads to compulsive heroin-seeking and altered striatal synaptic plasticity in the subsequent generation. Neuropsychopharmacology. 2014 May;39(6):1315–1323.
  • Szutorisz H, Hurd YL. Epigenetic effects of cannabis exposure. Biol Psychiatry. 2016 Apr 1;79(7):586–594.
  • Watson CT, Szutorisz H, Garg P, et al. Genome-Wide DNA methylation profiling reveals epigenetic changes in the rat nucleus accumbens associated with cross-generational effects of adolescent THC exposure. Neuropsychopharmacology. 2015 Dec;40(13):2993–3005.
  • Ibn Lahmar Andaloussi Z, Taghzouti K, Abboussi O. Behavioural and epigenetic effects of paternal exposure to cannabinoids during adolescence on offspring vulnerability to stress. Int J Dev Neurosci. 2019 Feb;72:48–54.
  • Heijmans BT, Tobi EW, Lumey LH, et al. The epigenome: archive of the prenatal environment. Epigenetics. 2009 Nov 16;4(8):526–531.
  • Wu H, Hauser R, Krawetz SA, et al. Environmental susceptibility of the sperm epigenome during windows of male germ cell development. Curr Environ Health Rep. 2015 Dec;2(4):356–366.
  • Day J, Savani S, Krempley BD, et al. Influence of paternal preconception exposures on their offspring: through epigenetics to phenotype. Am J Stem Cells. 2016;5(1):11–18.
  • Soubry A, Murphy SK, Wang F, et al. Newborns of obese parents have altered DNA methylation patterns at imprinted genes. Int J Obes (Lond). 2015 Apr;39(4):650–657.
  • Abbasi J. The paternal epigenome makes its mark. JAMA. 2017 May 23;317(20):2049–2051.
  • Donkin I, Barres R. Sperm epigenetics and influence of environmental factors. Mol Metab. 2018 Feb 27;14:1–11.
  • Schuster A, Skinner MK, Yan W. Ancestral vinclozolin exposure alters the epigenetic transgenerational inheritance of sperm small noncoding RNAs. Environ Epigenet. 2016;2:1.
  • Leter G, Consales C, Eleuteri P, et al. Exposure to perfluoroalkyl substances and sperm DNA global methylation in Arctic and European populations. Environ Mol Mutagen. 2014 Aug;55(7):591–600.
  • Murphy SK, Itchon-Ramos N, Visco Z, et al. Cannabinoid exposure and altered DNA methylation in rat and human sperm. Epigenetics. 2018;13(12):1208–1221.
  • Rasmussen AH, Rasmussen HB, Silahtaroglu A. The DLGAP family: neuronal expression, function and role in brain disorders. Mol Brain. 2017 Sep 4;10(1):43.
  • Nardone S, Sams DS, Reuveni E, et al. DNA methylation analysis of the autistic brain reveals multiple dysregulated biological pathways. Transl Psychiatry. 2014 Sep;2(4):e433.
  • Soler J, Fananas L, Parellada M, et al. Genetic variability in scaffolding proteins and risk for schizophrenia and autism-spectrum disorders: a systematic review. J Psychiatry Neurosci. 2018 Jul;43(4):223–244.
  • Lee SE, Kim JA, Chang S. nArgBP2-SAPAP-SHANK, the core postsynaptic triad associated with psychiatric disorders. Exp Mol Med. 2018 Apr 9;50(4):2.
  • Luedi PP, Dietrich FS, Weidman JR, et al. Computational and experimental identification of novel human imprinted genes. Genome Res. 2007 Dec;17(12):1723–1730.
  • Murphy SK, Adigun A, Huang Z, et al. Gender-specific methylation differences in relation to prenatal exposure to cigarette smoke. Gene. 2012 Feb 15;494(1):36–43.
  • Dosemeci A, Weinberg RJ, Reese TS, et al. The postsynaptic density: There is more than meets the eye. Front Synaptic Neurosci. 2016;8:23.
  • Chien WH, Gau SS, Liao HM, et al. Deep exon resequencing of DLGAP2 as a candidate gene of autism spectrum disorders. Mol Autism. 2013 Aug 1;4(1):26.
  • Xing J, Kimura H, Wang C, et al. Resequencing and association analysis of six PSD-95-related genes as possible susceptibility genes for schizophrenia and autism spectrum disorders. Sci Rep. 2016 Jun 7;6:27491.
  • Chertkow-Deutsher Y, Cohen H, Klein E, et al. DNA methylation in vulnerability to post-traumatic stress in rats: evidence for the role of the post-synaptic density protein Dlgap2. Int J Neuropsychopharmacol. 2010 Apr;13(3):347–359.
  • Jiang-Xie LF, Liao HM, Chen CH, et al. Autism-associated gene Dlgap2 mutant mice demonstrate exacerbated aggressive behaviors and orbitofrontal cortex deficits. Mol Autism. 2014;5:32.
  • Rey JM, Tennant CC. Cannabis and mental health. BMJ. 2002 Nov 23;325(7374):1183–1184.
  • David A, AJS G, Richard H. Cannabis use and disorder: epidemiology, comorbidity, health consequences, and medico-legal status. 2016 cited 2018 Nov 28. Available from: https://www.uptodate.com/contents/cannabis-use-and-disorder-epidemiology-comorbidity-health-consequences-and-medico-legal-status.
  • Szutorisz H, Hurd YL. High times for cannabis: Epigenetic imprint and its legacy on brain and behavior. Neurosci Biobehav Rev. 2018 Feb;85:93–101.
  • Reece AS, Hulse GK. Effect of cannabis legalization on US autism incidence and medium term projections. Clin Pediatr Open Access. 2019;4(2):17.
  • Centers of Disease Control and Prevention. Autism Spectrum Disorder (ASD) Data & Statistics. 2014 cited 2018 Oct 30. Available from: https://www.cdc.gov/ncbddd/autism/data.html.
  • Werling DM, Geschwind DH. Sex differences in autism spectrum disorders. Curr Opin Neurol. 2013 Apr;26(2):146–153.
  • Ly L, Chan D, Trasler JM. Developmental windows of susceptibility for epigenetic inheritance through the male germline. Semin Cell Dev Biol. 2015 Jul;43:96–105.
  • Murphy SK, Huang Z, Hoyo C. Differentially methylated regions of imprinted genes in prenatal, perinatal and postnatal human tissues. PLoS One. 2012;7(7):e40924.
  • Bartolomei MS, Tilghman SM. Genomic imprinting in mammals. Annu Rev Genet. 1997;31:493–525.
  • Gkountela S, Zhang KX, Shafiq TA, et al. DNA demethylation dynamics in the human prenatal germline. Cell. 2015 Jun 4;161(6):1425–1436.
  • Tang WW, Dietmann S, Irie N, et al. A unique gene regulatory network resets the human germline epigenome for development. Cell. 2015 Jun 4;161(6):1453–1467.
  • Shin SM, Zhang N, Hansen J, et al. GKAP orchestrates activity-dependent postsynaptic protein remodeling and homeostatic scaling. Nat Neurosci. 2012 Dec;15(12):1655–1666.
  • Roloff AM, Anderson GR, Martemyanov KA, et al. Homer 1a gates the induction mechanism for endocannabinoid-mediated synaptic plasticity. J Neurosci. 2010 Feb 24;30(8):3072–3081.
  • Howlett AC, Barth F, Bonner TI, et al. International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev. 2002 Jun;54(2):161–202.
  • Chen M, Wan Y, Ade K, et al. Sapap3 deletion anomalously activates short-term endocannabinoid-mediated synaptic plasticity. J Neurosci. 2011 Jun 29;31(26):9563–9573.
  • Rey RA, Grinspon RP. Normal male sexual differentiation and aetiology of disorders of sex development. Best Pract Res Clin Endocrinol Metab. 2011 Apr;25(2):221–238.
  • Bassil CF, Huang Z, Murphy SK. Bisulfite pyrosequencing. Methods Mol Biol. 2013;1049:95–107.