Epigenetic effects of cannabis exposure

Biological Psychiatry

Volumn 79, Issue 7, 2016, Pages 586-594

  Szutorisz, Henrietta ^a   Hurd, Yasmin L ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Addiction; Cannabinoids; CB1 receptor; DNA methylation; Epigenetics; Neurodevelopment

Indexed keywords

ANANDAMIDE; CANNABINOID; CANNABIS; CATECHOL METHYLTRANSFERASE; ENDOCANNABINOID; HISTONE H3; MICRORNA; UNTRANSLATED RNA;

DNA METHYLATION; DNA MODIFICATION; DRUG EXPOSURE; EPIGENETICS; GENE EXPRESSION; GENOTYPE ENVIRONMENT INTERACTION; HISTONE MODIFICATION; HUMAN; LONG TERM CARE; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION INITIATION; ANIMAL; ANIMAL MODEL; BRAIN; DRUG EFFECTS; FEMALE; GENETIC EPIGENESIS; HISTONE CODE; MARIJUANA ABUSE; METABOLISM; MOUSE; RAT;

ANIMALS; BRAIN; CANNABINOIDS; CANNABIS; DNA METHYLATION; ENDOCANNABINOIDS; EPIGENESIS, GENETIC; FEMALE; HISTONE CODE; HUMANS; MARIJUANA ABUSE; MICE; MODELS, ANIMAL; RATS;

EID: 84953244289     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2015.09.014     Document Type: Review

References (80)

1. Alegria AA, Hasin DS, Nunes EV, Liu SM, Davies C, Grant BF, Blanco C (2010): Comorbidity of generalized anxiety disorder and substance use disorders: Results from the National Epidemiologic Survey on Alcohol and Related Conditions. J Clin Psychiatry 71:1187-1195; quiz 1252-1253.
2. Crean RD, Crane NA, Mason BJ (2011): An evidence based review of acute and long-term effects of cannabis use on executive cognitive functions. J Addict Med 5:1-8.
3. Jutras-Aswad D, DiNieri JA, Harkany T, Hurd YL (2009): Neurobiological consequences of maternal cannabis on human fetal development and its neuropsychiatric outcome. Eur Arch Psychiatry Clin Neurosci 259:395-412.
4. Leweke FM, Koethe D (2008): Cannabis and psychiatric disorders: It is not only addiction. Addict Biol 13:264-275.
5. Malone DT, Hill MN, Rubino T (2010): Adolescent cannabis use and psychosis: Epidemiology and neurodevelopmental models. Br J Pharmacol 160:511-522.
6. Mechoulam R, Parker LA (2013): The endocannabinoid system and the brain. Annu Rev Psychol 64:21-47.
7. Morris CV, DiNieri JA, Szutorisz H, Hurd YL (2011): Molecular mechanisms of maternal cannabis and cigarette use on human neurodevelopment. Eur J Neurosci 34:1574-1583.
8. Owen KP, Sutter ME, Albertson TE (2014): Marijuana: Respiratory tract effects. Clin Rev Allergy Immunol 46:65-81.
9. Chadwick B, Miller ML, Hurd YL (2013): Cannabis use during adolescent development: Susceptibility to psychiatric illness. Front Psychiatry 4:129.
10. Bari M, Battista N, Pirazzi V, Maccarrone M (2011): The manifold actions of endocannabinoids on female and male reproductive events. Front Biosci (Landmark Ed) 16:498-516.
11. Szutorisz H, DiNieri JA, Sweet E, Egervari G, Michaelides M, Carter JM, et al. (2014): Parental THC exposure leads to compulsive heroinseeking and altered striatal synaptic plasticity in the subsequent generation. Neuropsychopharmacology 39:1315-1323.
12. Byrnes JJ, Babb JA, Scanlan VF, Byrnes EM (2011): Adolescent opioid exposure in female rats: Transgenerational effects on morphine analgesia and anxiety-like behavior in adult offspring. Behav Brain Res 218:200-205.
13. Byrnes JJ, Johnson NL, Carini LM, Byrnes EM (2013): Multigenerational effects of adolescent morphine exposure on dopamine D2 receptor function. Psychopharmacology (Berl) 227:263-272.
14. Vassoler FM, Johnson NL, Byrnes EM (2013): Female adolescent exposure to cannabinoids causes transgenerational effects on morphine sensitization in female offspring in the absence of in utero exposure. J Psychopharmacol 27:1015-1022.
15. Watson CT, Szutorisz H, Garg P, Martin Q, Landry JA, Sharp AJ, Hurd YL (2015): Genome-wide DNA methylation profiling reveals epigenetic changes in the rat nucleus accumbens associated with crossgenerational effects of adolescent THC exposure [published online ahead of print June 5]. Neuropsychopharmacology.
16. Baedke J (2013): The epigenetic landscape in the course of time: Conrad Hal Waddington's methodological impact on the life sciences. Stud Hist Philos Biol Biomed Sci 44(4 Pt B):756-773.
17. Van Speybroeck L (2002): From epigenesis to epigenetics: The case of C. H. Waddington. Ann N Y Acad Sci 981:61-81.
18. Dambacher S, de Almeida GP, Schotta G (2013): Dynamic changes of the epigenetic landscape during cellular differentiation. Epigenomics 5:701-713.
19. Dillon N (2012): Factor mediated gene priming in pluripotent stem cells sets the stage for lineage specification. Bioessays 34:194-204.
20. Weake VM, Workman JL (2010): Inducible gene expression: Diverse regulatory mechanisms. Nat Rev Genet 11:426-437.
21. Baubec T, Schubeler D (2014): Genomic patterns and context specific interpretation of DNA methylation. Curr Opin Genet Dev 25: 85-92.
22. Kato T, Iwamoto K (2014): Comprehensive DNA methylation and hydroxymethylation analysis in the human brain and its implication in mental disorders. Neuropharmacology 80:133-139.
23. Cheng Y, Bernstein A, Chen D, Jin P (2015): 5-Hydroxymethylcytosine: A new player in brain disorders? Exp Neurol 268:3-9.
24. Feng J, Shao N, Szulwach KE, Vialou V, Huynh J, Zhong C, et al. (2015): Role of Tet1 and 5-hydroxymethylcytosine in cocaine action. Nat Neurosci 18:536-544.
25. Branco MR, Ficz G, Reik W (2012): Uncovering the role of 5- hydroxymethylcytosine in the epigenome. Nat Rev Genet 13:7-13.
26. Szyf M (2013): The genome- and system-wide response of DNA methylation to early life adversity and its implication on mental health. Can J Psychiatry 58:697-704.
27. Szyf M (2015): Nongenetic inheritance and transgenerational epigenetics. Trends Mol Med 21:134-144.
28. Bhaumik SR, Smith E, Shilatifard A (2007): Covalent modifications of histones during development and disease pathogenesis. Nat Struct Mol Biol 14:1008-1016.
29. Cosgrove MS, Boeke JD, Wolberger C (2004): Regulated nucleosome mobility and the histone code. Nat Struct Mol Biol 11:1037-1043.
30. Ciccarelli A, Giustetto M (2014): Role of ERK signaling in activitydependent modifications of histone proteins. Neuropharmacology 80: 34-44.
31. Aguado T, Carracedo A, Julien B, Velasco G, Milman G, Mechoulam R, et al. (2007): Cannabinoids induce glioma stem-like cell differentiation and inhibit gliomagenesis. J Biol Chem 282:6854-6862.
32. DiNieri JA, Wang X, Szutorisz H, Spano SM, Kaur J, Casaccia P, et al. (2011): Maternal cannabis use alters ventral striatal dopamine D2 gene regulation in the offspring. Biol Psychiatry 70:763-769.
33. Tomasiewicz HC, Jacobs MM, Wilkinson MB, Wilson SP, Nestler EJ, Hurd YL (2012): Proenkephalin mediates the enduring effects of adolescent cannabis exposure associated with adult opiate vulnerability. Biol Psychiatry 72:803-810.
34. Yang X, Hegde VL, Rao R, Zhang J, Nagarkatti PS, Nagarkatti M (2014): Histone modifications are associated with Delta9- tetrahydrocannabinol-mediated alterations in antigen-specific T cell responses. J Biol Chem 289:18707-18718.
35. Iyengar BR, Choudhary A, Sarangdhar MA, Venkatesh KV, Gadgil CJ, Pillai B (2014): Non-coding RNA interact to regulate neuronal development and function. Front Cell Neurosci 8:47.
36. Chandra LC, Kumar V, Torben W, Vande Stouwe C, Winsauer P, Amedee A, et al. (2015): Chronic administration of Delta9- tetrahydrocannabinol induces intestinal anti-inflammatory microRNA expression during acute simian immunodeficiency virus infection of rhesus macaques. J Virol 89:1168-1181.
37. Hegde VL, Tomar S, Jackson A, Rao R, Yang X, Singh UP, et al. (2013): Distinct microRNA expression profile and targeted biological pathways in functional myeloid-derived suppressor cells induced by Delta9-tetrahydrocannabinol in vivo: Regulation of CCAAT/enhancerbinding protein alpha by microRNA-690. J Biol Chem 288: 36810-36826.
38. Jackson AR, Nagarkatti P, Nagarkatti M (2014): Anandamide attenuates Th-17 cell-mediated delayed-type hypersensitivity response by triggering IL-10 production and consequent microRNA induction. PLoS One 9:e93954.
39. Molina PE, Amedee A, LeCapitaine NJ, Zabaleta J, Mohan M, Winsauer P, et al. (2011): Cannabinoid neuroimmune modulation of SIV disease. J Neuroimmune Pharmacol 6:516-527.
40. Berghuis P, Rajnicek AM, Morozov YM, Ross RA, Mulder J, Urban GM, et al. (2007): Hardwiring the brain: Endocannabinoids shape neuronal connectivity. Science 316:1212-1216.
41. Tortoriello G, Morris CV, Alpar A, Fuzik J, Shirran SL, Calvigioni D, et al. (2014): Miswiring the brain: Delta9-tetrahydrocannabinol disrupts cortical development by inducing an SCG10/stathmin-2 degradation pathway. EMBO J 33:668-685.
42. Luchicchi A, Pistis M (2012): Anandamide and 2-arachidonoylglycerol: Pharmacological properties, functional features, and emerging specificities of the two major endocannabinoids. Mol Neurobiol 46:374-392.
43. Calvigioni D, Hurd YL, Harkany T, Keimpema E (2014): Neuronal substrates and functional consequences of prenatal cannabis exposure. Eur Child Adolesc Psychiatry 23:931-941.
44. Shirtcliff EA, Dismukes AR, Marceau K, Ruttle PL, Simmons JG, Han G (2015): A dual-axis approach to understanding neuroendocrine development. Dev Psychobiol 57:643-653.
45. Koch M, Varela L, Kim JG, Kim JD, Hernandez-Nuno F, Simonds SE, et al. (2015): Hypothalamic POMC neurons promote cannabinoidinduced feeding. Nature 519:45-50.
46. Cabral GA, Raborn ES, Griffin L, Dennis J, Marciano-Cabral F (2008): CB2 receptors in the brain: Role in central immune function. Br J Pharmacol 153:240-251.
47. Onaivi ES, Ishiguro H, Gong JP, Patel S, Perchuk A, Meozzi PA, et al. (2006): Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain. Ann N Y Acad Sci 1074:514-536.
48. Van Sickle MD, Duncan M, Kingsley PJ, Mouihate A, Urbani P, Mackie K, et al. (2005): Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science 310:329-332.
49. Ignatowska-Jankowska BM, Muldoon PP, Lichtman AH, Damaj MI (2013): The cannabinoid CB2 receptor is necessary for nicotineconditioned place preference, but not other behavioral effects of nicotine in mice. Psychopharmacology (Berl) 229:591-601.
50. Xi ZX, Peng XQ, Li X, Song R, Zhang HY, Liu QR, et al. (2011): Brain cannabinoid CB(2) receptors modulate cocaine's actions in mice. Nat Neurosci, 14:1160-1166.
51. Graham ES, Ashton JC, Glass M (2009): Cannabinoid receptors: A brief history and "what's hot". Front Biosci (Landmark Ed) 14:944-957.
52. D'Addario C, Di Francesco A, Pucci M, Finazzi Agro A, Maccarrone M (2013): Epigenetic mechanisms and endocannabinoid signalling. FEBS J 280:1905-1917.
53. Paradisi A, Pasquariello N, Barcaroli D, Maccarrone M (2008): Anandamide regulates keratinocyte differentiation by inducing DNA methylation in a CB1 receptor-dependent manner. J Biol Chem 283: 6005-6012.
54. Robison AJ, Nestler EJ (2011): Transcriptional and epigenetic mechanisms of addiction. Nat Rev Neurosci 12:623-637.
55. Sweatt JD (2013): The emerging field of neuroepigenetics. Neuron 80: 624-632.
56. Lee KS, Asgar J, Zhang Y, Chung MK, Ro JY (2013): The role of androgen receptor in transcriptional modulation of cannabinoid receptor type 1 gene in rat trigeminal ganglia. Neuroscience 254: 395-403.
57. Mukhopadhyay B, Liu J, Osei-Hyiaman D, Godlewski G, Mukhopadhyay P, Wang L, et al. (2010): Transcriptional regulation of cannabinoid receptor-1 expression in the liver by retinoic acid acting via retinoic acid receptor-gamma. J Biol Chem 285:19002-19011.
58. Nagre NN, Subbanna S, Shivakumar M, Psychoyos D, Basavarajappa BS (2015): CB1-receptor knockout neonatal mice are protected against ethanol-induced impairments of DNMT1, DNMT3A, and DNA methylation. J Neurochem 132:429-442.
59. Liu J, Chen J, Ehrlich S, Walton E, White T, Perrone-Bizzozero N, et al. (2014): Methylation patterns in whole blood correlate with symptoms in schizophrenia patients. Schizophr Bull 40:769-776.
60. Beuten J, Payne TJ, Ma JZ, Li MD (2006): Significant association of catechol-O-methyltransferase (COMT) haplotypes with nicotine dependence in male and female smokers of two ethnic populations. Neuropsychopharmacology 31:675-684.
61. Vandenbergh DJ, Rodriguez LA, Miller IT, Uhl GR, Lachman HM (1997): High-activity catechol-O-methyltransferase allele is more prevalent in polysubstance abusers. Am J Med Genet 74:439-442.
62. Tammimaki AE, Mannisto PT (2010): Are genetic variants of COMT associated with addiction? Pharmacogenet Genomics 20: 717-741.
63. van der Knaap LJ, Schaefer JM, Franken IH, Verhulst FC, van Oort FV, Riese H (2014): Catechol-O-methyltransferase gene methylation and substance use in adolescents: The TRAILS study. Genes Brain Behav 13:618-625.
64. Rubio P, Rodriguez de Fonseca F, Martin-Calderon JL, Del Arco I, Bartolome S, Villanua MA, Navarro M (1998): Maternal exposure to low doses of delta9-tetrahydrocannabinol facilitates morphineinduced place conditioning in adult male offspring. Pharmacol Biochem Behav 61:229-238.
65. Vela G, Martin S, Garcia-Gil L, Crespo JA, Ruiz-Gayo M, Fernandez-Ruiz JJ, et al. (1998): Maternal exposure to delta9-tetrahydrocannabinol facilitates morphine self-administration behavior and changes regional binding to central mu opioid receptors in adult offspring female rats. Brain Res 807:101-109.
66. Campolongo P, Trezza V, Cassano T, Gaetani S, Morgese MG, Ubaldi M, et al. (2007): Perinatal exposure to delta-9-tetrahydrocannabinol causes enduring cognitive deficits associated with alteration of cortical gene expression and neurotransmission in rats. Addict Biol 12:485-495.
67. Singh ME, McGregor IS, Mallet PE (2006): Perinatal exposure to delta (9)-tetrahydrocannabinol alters heroin-induced place conditioning and fos-immunoreactivity. Neuropsychopharmacology 31:58-69.
68. Spano MS, Ellgren M, Wang X, Hurd YL (2007): Prenatal cannabis exposure increases heroin seeking with allostatic changes in limbic enkephalin systems in adulthood. Biol Psychiatry 61:554-563.
69. Everitt BJ, Robbins TW (2013): From the ventral to the dorsal striatum: Devolving views of their roles in drug addiction. Neurosci Biobehav Rev 37:1946-1954.
70. Girault JA (2012): Integrating neurotransmission in striatal medium spiny neurons. Adv Exp Med Biol 970:407-429.
71. Koob GF, Volkow ND (2010): Neurocircuitry of addiction. Neuropsychopharmacology 35:217-238.
72. Khare M, Taylor AH, Konje JC, Bell SC (2006): Delta9- tetrahydrocannabinol inhibits cytotrophoblast cell proliferation and modulates gene transcription. Mol Hum Reprod 12:321-333.
73. Bohacek J, Mansuy IM (2013): Epigenetic inheritance of disease and disease risk. Neuropsychopharmacology 38:220-236.
74. Vassoler FM, Sadri-Vakili G (2014): Mechanisms of transgenerational inheritance of addictive-like behaviors. Neuroscience 264: 198-206.
75. Wang Z, Yan P, Hui T, Zhang J (2014): Epigenetic upregulation of PSD-95 contributes to the rewarding behavior by morphine conditioning. Eur J Pharmacol 732:123-129.
76. Byrnes JJ, Johnson NL, Schenk ME, Byrnes EM (2012): Cannabinoid exposure in adolescent female rats induces transgenerational effects on morphine conditioned place preference in male offspring. J Psychopharmacol 26:1348-1354.
77. Banerjee A, Singh A, Srivastava P, Turner H, Krishna A (2011): Effects of chronic bhang (cannabis) administration on the reproductive system of male mice. Birth Defects Res B Dev Reprod Toxicol 92: 195-205.
78. Chioccarelli T, Cacciola G, Altucci L, Lewis SE, Simon L, Ricci G, et al. (2010): Cannabinoid receptor 1 influences chromatin remodeling in mouse spermatids by affecting content of transition protein 2 mRNA and histone displacement. Endocrinology 151:5017-5029.
79. Klonoff-Cohen HS, Natarajan L, Chen RV (2006): A prospective study of the effects of female and male marijuana use on in vitro fertilization (IVF) and gamete intrafallopian transfer (GIFT) outcomes. Am J Obstet Gynecol 194:369-376.
80. Hollins SL, Zavitsanou K, Walker FR, Cairns MJ (2014): Alteration of imprinted Dlk1-Dio3 miRNA cluster expression in the entorhinal cortex induced by maternal immune activation and adolescent cannabinoid exposure. Transl Psychiatry 4:e452.