Prenatal cannabis exposure - The “first hit” to the endocannabinoid system

Neurotoxicology and Teratology

Volumn 58, Issue , 2016, Pages 5-14

  Richardson, Kimberlei A ^a   Hester, Allison K ^a   McLemore, Gabrielle L ^b  

^a HOWARD UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b MORGAN STATE UNIVERSITY   (United States)

Author keywords

Double hit hypothesis; Epigenetics; Fetal malprogramming; Fetal neurodevelopment; Marijuana; Maternal cannabis exposure; Neurodevelopment; Prenatal cannabis exposure

Indexed keywords

CANNABIS; DRONABINOL; ENDOCANNABINOID;

BRAIN FUNCTION; CANNABIS USE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR PROCEDURE; CEREBELLUM; COGNITION; EPIGENETICS; FRONTAL GYRUS; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INCIDENCE; LONGITUDINAL STUDY; MALPRESENTATION; MATERNAL SMOKING; MATERNAL STRESS; MENTAL DISEASE; PHENOTYPE; PREFRONTAL CORTEX; PREIMPLANTATION EMBRYO; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PROSPECTIVE STUDY; REVIEW; SOCIAL STATUS; CANNABIS SMOKING; FEMALE; PATHOPHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE;

CANNABIS; ENDOCANNABINOIDS; FEMALE; HUMANS; MARIJUANA SMOKING; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84995450851     PISSN: 08920362     EISSN: 18729738     Source Type: Journal    
DOI: 10.1016/j.ntt.2016.08.003     Document Type: Review

References (155)

1. Ahmed, S.A., et al. Cannabinoid ester constituents from high-potency Cannabis sativa. J. Nat. Prod. 71:4 (2008), 536–542.
2. Ahmed, S.A., et al. Structure determination and absolute configuration of cannabichromanone derivatives from high potency Cannabis sativa. Tetrahedron Lett. 49:42 (2008), 6050–6053.
3. Alwasel, S.H., Barker, D.J., Ashton, N., Prenatal programming of renal salt wasting resets postnatal salt appetite, which drives food intake in the rat. Clin. Sci. (Lond.) 122:6 (2012), 281–288.
4. Anon, Results From the 2013 National Survey on Drug Use and Health: Summary of National Findings. 2014.
5. Bada, H.S., et al. Low birth weight and preterm births: etiologic fraction attributable to prenatal drug exposure. J. Perinatol. 25:10 (2005), 631–637.
6. Barker, D.J., In utero programming of chronic disease. Clin. Sci. (Lond.) 95:2 (1998), 115–128.
7. Batkai, S., Pacher, P., Endocannabinoids and cardiac contractile function: pathophysiological implications. Pharmacol. Res. 60:2 (2009), 99–106.
8. Bell, S.H., et al. The remarkably high prevalence of epilepsy and seizure history in fetal alcohol spectrum disorders. Alcohol. Clin. Exp. Res. 34:6 (2010), 1084–1089.
9. Berghuis, P., et al. Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 316:5828 (2007), 1212–1216.
10. Bird, A., Perceptions of epigenetics. Nature 447:7143 (2007), 396–398.
11. Bohacek, J., Mansuy, I.M., Epigenetic inheritance of disease and disease risk. Neuropsychopharmacology 38:1 (2013), 220–236.
12. Breivogel, C.S., Selley, D.E., Childers, S.R., Cannabinoid receptor agonist efficacy for stimulating [35S]GTPgammaS binding to rat cerebellar membranes correlates with agonist-induced decreases in GDP affinity. J. Biol. Chem. 273:27 (1998), 16865–16873.
13. Burns, J.K., Pathways from cannabis to psychosis: a review of the evidence. Front. Psychol., 4, 2013, 128.
14. Calvigioni, D., et al. Neuronal substrates and functional consequences of prenatal cannabis exposure. Eur. Child Adolesc. Psychiatry 23:10 (2014), 931–941.
15. Campolongo, P., et al. Developmental exposure to cannabinoids causes subtle and enduring neurofunctional alterations. Int. Rev. Neurobiol. 85 (2009), 117–133.
16. Campolongo, P., et al. Developmental consequences of perinatal cannabis exposure: behavioral and neuroendocrine effects in adult rodents. Psychopharmacology 214:1 (2011), 5–15.
17. Centers for Disease, C. and Prevention, Trends in ischemic heart disease death rates for blacks and whites—United States, 1981–1995. MMWR. Morb. Mortal. Wkly Rep. 47:44 (1998), 945–949.
18. Coyle, I., Wayner, M.J., Singer, G., Behavioral teratogenesis: a critical evaluation. Pharmacol. Biochem. Behav. 4:2 (1976), 191–200.
19. Day, N.L., Richardson, G.A., Prenatal marijuana use: epidemiology, methodologic issues, and infant outcome. Clin. Perinatol. 18:1 (1991), 77–91.
20. Defer, N., et al. The cannabinoid receptor type 2 promotes cardiac myocyte and fibroblast survival and protects against ischemia/reperfusion-induced cardiomyopathy. FASEB J. 23:7 (2009), 2120–2130.
21. Devane, W.A., et al. Determination and characterization of a cannabinoid receptor in rat brain. Mol. Pharmacol. 34:5 (1988), 605–613.
22. Devane, W.A., et al. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258:5090 (1992), 1946–1949.
23. Di Marzo, V., The endocannabinoid system: its general strategy of action, tools for its pharmacological manipulation and potential therapeutic exploitation. Pharmacol. Res. 60:2 (2009), 77–84.
24. Di Marzo, V., De Petrocellis, L., Why do cannabinoid receptors have more than one endogenous ligand?. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 367:1607 (2012), 3216–3228.
25. Diaz-Alonso, J., et al. The CB(1) cannabinoid receptor drives corticospinal motor neuron differentiation through the Ctip2/Satb2 transcriptional regulation axis. J. Neurosci. 32:47 (2012), 16651–16665.
26. Dinieri, J.A., Hurd, Y.L., Rat models of prenatal and adolescent cannabis exposure. Methods Mol. Biol. 829 (2012), 231–242.
27. Dinieri, J.A., et al. Maternal cannabis use alters ventral striatal dopamine D2 gene regulation in the offspring. Biol. Psychiatry, 70(8), 2011, 7.
28. DiPatrizio, N.V., Piomelli, D., The thrifty lipids: endocannabinoids and the neural control of energy conservation. Trends Neurosci. 35:7 (2012), 403–411.
29. Dipietro, J.A., Maternal stress in pregnancy: considerations for fetal development. J. Adolesc. Health 51:2 Suppl. (2012), S3–S8.
30. Driscoll, C.D., Streissguth, A.P., Riley, E.P., Prenatal alcohol exposure: comparability of effects in humans and animal models. Neurotoxicol. Teratol. 12:3 (1990), 231–237.
31. Ebrahim, S.H., Gfroerer, J., Pregnancy-related substance use in the United States during 1996–1998. Obstet. Gynecol. 101:2 (2003), 374–379.
32. Elsohly, M.A., Slade, D., Chemical constituents of marijuana: the complex mixture of natural cannabinoids. Life Sci. 78:5 (2005), 539–548.
33. Ewing, C.K., Loffredo, C.A., Beaty, T.H., Paternal risk factors for isolated membranous ventricular septal defects. Am. J. Med. Genet. 71:1 (1997), 42–46.
34. Fergusson, D.M., et al. Maternal use of cannabis and pregnancy outcome. BJOG 109:1 (2002), 21–27.
35. Fernandez-Ruiz, J., et al. The endogenous cannabinoid system and brain development. Trends Neurosci. 23:1 (2000), 14–20.
36. Ferraro, L., et al. Short- and long-term consequences of prenatal exposure to the cannabinoid agonist WIN55,212-2 on rat glutamate transmission and cognitive functions. J. Neural Transm. (Vienna) 116:8 (2009), 1017–1027.
37. Fowler, C.J., Anandamide uptake explained?. Trends Pharmacol. Sci. 33:4 (2012), 181–185.
38. Fride, E., et al. The endocannabinoid system during development: emphasis on perinatal events and delayed effects. Vitam. Horm. 81 (2009), 139–158.
39. Fried, P.A., Marihuana use by pregnant women: neurobehavioral effects in neonates. Drug Alcohol Depend. 6:6 (1980), 415–424.
40. Fried, P.A., Conceptual issues in behavioral teratology and their application in determining long-term sequelae of prenatal marihuana exposure. J. Child Psychol. Psychiatry 43:1 (2002), 81–102.
41. Fried, P.A., O'Connell, C.M., A comparison of the effects of prenatal exposure to tobacco, alcohol, cannabis and caffeine on birth size and subsequent growth. Neurotoxicol. Teratol. 9:2 (1987), 79–85.
42. Fried, P.A., Smith, A.M., A literature review of the consequences of prenatal marihuana exposure. An emerging theme of a deficiency in aspects of executive function. Neurotoxicol. Teratol. 23:1 (2001), 1–11.
43. Fried, P.A., O'Connell, C.M., Watkinson, B., 60- and 72-month follow-up of children prenatally exposed to marijuana, cigarettes, and alcohol: cognitive and language assessment. J. Dev. Behav. Pediatr. 13:6 (1992), 383–391.
44. Fried, P.A., Watkinson, B., Gray, R., Differential effects on cognitive functioning in 9- to 12-year olds prenatally exposed to cigarettes and marihuana. Neurotoxicol. Teratol. 20:3 (1998), 293–306.
45. Gaffuri, A.L., Ladarre, D., Lenkei, Z., Type-1 cannabinoid receptor signaling in neuronal development. Pharmacology 90:1–2 (2012), 19–39.
46. Galve-Roperh, I., et al. Cannabinoid receptor signaling in progenitor/stem cell proliferation and differentiation. Prog. Lipid Res. 52:4 (2013), 633–650.
47. Gaoni, Y., Mechoulam, R., Isolation, structure and partial synthesis of an active constituent of hashish. J. Am. Chem. Soc. 86 (1964), 1646–1647.
48. Goldschmidt, L., Day, N.L., Richardson, G.A., Effects of prenatal marijuana exposure on child behavior problems at age 10. Neurotoxicol. Teratol. 22:3 (2000), 325–336.
49. Goldschmidt, L., et al. Prenatal marijuana and alcohol exposure and academic achievement at age 10. Neurotoxicol. Teratol. 26:4 (2004), 521–532.
50. Goncalves, M.B., et al. A diacylglycerol lipase-CB2 cannabinoid pathway regulates adult subventricular zone neurogenesis in an age-dependent manner. Mol. Cell. Neurosci. 38:4 (2008), 526–536.
51. Gong, J.P., et al. Cannabinoid CB2 receptors: immunohistochemical localization in rat brain. Brain Res. 1071:1 (2006), 10–23.
52. Gorelick, D.A., et al. The cannabinoid CB1 receptor antagonist rimonabant attenuates the hypotensive effect of smoked marijuana in male smokers. Am. Heart J. 151:3 (2006), 754e1–754e5.
53. Gross, C., Hen, R., The developmental origins of anxiety. Nat. Rev. Neurosci. 5:7 (2004), 545–552.
54. Grotenhermen, F., Pharmacokinetics and pharmacodynamics of cannabinoids. Clin. Pharmacokinet. 42:4 (2003), 327–360.
55. Hackett, J.A., et al. Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 339:6118 (2013), 448–452.
56. Hanus, L., et al. N-acyl amino acids and their impact on biological processes. Biofactors 40:4 (2014), 381–388.
57. Hayatbakhsh, M.R., et al. Birth outcomes associated with cannabis use before and during pregnancy. Pediatr. Res. 71:2 (2012), 215–219.
58. Hedden, S.L., Kennet, J., Lipari, R., Medley, G., Tice, P., Behavioral Health Trends in the United States: Results from the 2014 National Survey on Drug Use and Health. 2015.
59. Hoffman, J.I., Kaplan, S., The incidence of congenital heart disease. J. Am. Coll. Cardiol. 39:12 (2002), 1890–1900.
60. Hofman, A., et al. Growth, development and health from early fetal life until young adulthood: the generation R study. Paediatr. Perinat. Epidemiol. 18:1 (2004), 61–72.
61. Howlett, A.C., Fleming, R.M., Cannabinoid inhibition of adenylate cyclase. Pharmacology of the response in neuroblastoma cell membranes. Mol. Pharmacol. 26:3 (1984), 532–538.
62. Huizink, A.C., Prenatal cannabis exposure and infant outcomes: overview of studies. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 52 (2014), 45–52.
63. Huizink, A.C., Mulder, E.J., Maternal smoking, drinking or cannabis use during pregnancy and neurobehavioral and cognitive functioning in human offspring. Neurosci. Biobehav. Rev. 30:1 (2006), 24–41.
64. Hurd, Y.L., et al. Marijuana impairs growth in mid-gestation fetuses. Neurotoxicol. Teratol. 27:2 (2005), 221–229.
65. Hutchings, D.E., et al. The effects of prenatal exposure to delta-9-tetrahydrocannabinol on the rest-activity cycle of the preweanling rat. Neurotoxicol. Teratol. 11:4 (1989), 353–356.
66. Jakubovic, A., McGeer, P.L., Biochemical changes in rat testicular cells in vitro produced by cannabinoids and alcohol: metabolism and incorporation of labeled glucose, amino acids, and nucleic acid precursors. Toxicol. Appl. Pharmacol. 41:3 (1977), 473–486.
67. Jiang, W., et al. Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic- and antidepressant-like effects. J. Clin. Invest. 115:11 (2005), 3104–3116.
68. Jirtle, R.L., Skinner, M.K., Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 8:4 (2007), 253–262.
69. Johnston, L.D., P.O.M., Miech, R.A., Bachman, J.G., Schulenberg, J.E., Monitoring the Future National Survey Results on Drug Use: 1975–2014: Overview, Key Findings on Adolescent Drug Use. 2015.
70. Jouanjus, E., et al. Cannabis-related hospitalizations: unexpected serious events identified through hospital databases. Br. J. Clin. Pharmacol. 71:5 (2011), 758–765.
71. Jouanjus, E., et al. Cannabis use: signal of increasing risk of serious cardiovascular disorders. J. Am. Heart Assoc., 3(2), 2014, e000638.
72. Joyeux, M., et al. Endocannabinoids are implicated in the infarct size-reducing effect conferred by heat stress preconditioning in isolated rat hearts. Cardiovasc. Res. 55:3 (2002), 619–625.
73. Jutras-Aswad, D., et al. Neurobiological consequences of maternal cannabis on human fetal development and its neuropsychiatric outcome. Eur. Arch. Psychiatry Clin. Neurosci. 259:7 (2009), 395–412.
74. Kano, M., et al. Endocannabinoid-mediated control of synaptic transmission. Physiol. Rev. 89:1 (2009), 309–380.
75. Ko, J.Y., et al. Prevalence and patterns of marijuana use among pregnant and nonpregnant women of reproductive age. Am. J. Obstet. Gynecol. 213:2 (2015), 201e1–201e10.
76. Korantzopoulos, P., et al. Atrial fibrillation and marijuana smoking. Int. J. Clin. Pract. 62:2 (2008), 308–313.
77. Lamarine, R.J., Marijuana: modern medical chimaera. J. Drug Educ. 42:1 (2012), 1–11.
78. Leterrier, C., et al. Constitutive activation drives compartment-selective endocytosis and axonal targeting of type 1 cannabinoid receptors. J. Neurosci. 26:12 (2006), 3141–3153.
79. Leung, L., Cannabis and its derivatives: review of medical use. J. Am. Board Fam. Med. 24:4 (2011), 452–462.
80. Li, L., et al. Endocannabinoid signaling is required for development and critical period plasticity of the whisker map in somatosensory cortex. Neuron 64:4 (2009), 537–549.
81. Lurie, I.W., Ferencz, C., VACTERL-hydrocephaly, DK-phocomelia, and cerebro-cardio-radio-reno-rectal community. Am. J. Med. Genet. 70:2 (1997), 144–149.
82. Lyon, M., et al. Fetal neural development and schizophrenia. Schizophr. Bull. 15:1 (1989), 149–161.
83. Maccarrone, M., et al. Programming of neural cells by (endo)cannabinoids: from physiological rules to emerging therapies. Nat. Rev. Neurosci. 15:12 (2014), 786–801.
84. Maccarrone, M., et al. Endocannabinoid signaling at the periphery: 50 years after THC. Trends Pharmacol. Sci. 36:5 (2015), 277–296.
85. Manna, T., et al. Stathmin family protein SCG10 differentially regulates the plus and minus end dynamics of microtubules at steady state in vitro: implications for its role in neurite outgrowth. Biochemistry 46 (2007), 3543–3552.
86. Marijuana, Is There a Link Between Marijuana Use and Mental Illness?. 2015.
87. Mark, K., Desai, A., Terplan, M., Marijuana use and pregnancy: prevalence, associated characteristics, and birth outcomes. Arch. Womens Ment. Health 19:1 (2016), 105–111.
88. Martinez, G., Daniels, K., Chandra, A., Fertility of men and women aged 15–44 years in the United States: National Survey of family growth, 2006–2010. Natl. Health Stat. Rep. 51 (2012), 1–28.
89. Matias, I., Di Marzo, V., Endocannabinoids and the control of energy balance. Trends Endocrinol. Metab. 18:1 (2007), 27–37.
90. Matsuda, L.A., et al. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346:6284 (1990), 561–564.
91. McCabe, J.E., Arndt, S., Demographic and substance abuse trends among pregnant and non-pregnant women: eleven years of treatment admission data. Matern. Child Health J. 16:8 (2012), 1696–1702.
92. McLemore, G.L., Richardson, K.A., Data from three prospective longitudinal human cohorts of prenatal marijuana exposure and offspring outcomes from the fetal period through young adulthood. Neurotoxicology and Teratology Data in Brief, 2016 (submitted for publication).
93. McLemore, G.L., et al. Cannabinoid receptor expression in peripheral arterial chemoreceptors during postnatal development. J. Appl. Physiol. (1985) 97:4 (2004), 1486–1495.
94. McTiernan, M.J., et al. Carboxy- and oxyhemoglobin in pregnant ewe and fetus after inhalation of marijuana, marijuana placebo and tobacco cigarette smoke. Life Sci. 43:24 (1988), 2043–2047.
95. Mechoulam, R., et al. Enantiomeric cannabinoids: stereospecificity of psychotropic activity. Experientia 44:9 (1988), 762–764.
96. Mechoulam, R., et al. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmacol. 50:1 (1995), 83–90.
97. Mehmedic, Z., et al. Potency trends of Delta9-THC and other cannabinoids in confiscated cannabis preparations from 1993 to 2008. J. Forensic Sci. 55:5 (2010), 1209–1217.
98. Meier, M.H., et al. Persistent cannabis users show neuropsychological decline from childhood to midlife. Proc. Natl. Acad. Sci. U. S. A. 109:40 (2012), E2657–E2664.
99. Mittleman, M.A., et al. Triggering myocardial infarction by marijuana. Circulation 103:23 (2001), 2805–2809.
100. Montecucco, F., Di Marzo, V., At the heart of the matter: the endocannabinoid system in cardiovascular function and dysfunction. Trends Pharmacol. Sci. 33:6 (2012), 331–340.
101. Montecucco, F., et al. CB2 cannabinoid receptor agonist JWH-015 modulates human monocyte migration through defined intracellular signaling pathways. Am. J. Physiol. Heart Circ. Physiol. 294:3 (2008), H1145–H1155.
102. Montecucco, F., et al. CB(2) cannabinoid receptor activation is cardioprotective in a mouse model of ischemia/reperfusion. J. Mol. Cell. Cardiol. 46:5 (2009), 612–620.
103. Montecucco, F., et al. The activation of the cannabinoid receptor type 2 reduces neutrophilic protease-mediated vulnerability in atherosclerotic plaques. Eur. Heart J. 33:7 (2012), 846–856.
104. Morris, C.V., et al. Molecular mechanisms of maternal cannabis and cigarette use on human neurodevelopment. Eur. J. Neurosci. 34:10 (2011), 1574–1583.
105. Mukhopadhyay, P., et al. CB1 cannabinoid receptor inhibition: promising approach for heart failure?. Congest. Heart Fail. 14:6 (2008), 330–334.
106. Mukhopadhyay, P., et al. CB1 cannabinoid receptors promote oxidative stress and cell death in murine models of doxorubicin-induced cardiomyopathy and in human cardiomyocytes. Cardiovasc. Res. 85:4 (2010), 773–784.
107. Mulder, J., et al. Endocannabinoid signaling controls pyramidal cell specification and long-range axon patterning. Proc. Natl. Acad. Sci. U. S. A. 105:25 (2008), 8760–8765.
108. Munro, S., Thomas, K.L., Abu-Shaar, M., Molecular characterization of a peripheral receptor for cannabinoids. Nature 365:6441 (1993), 61–65.
109. Navarro, M., Rubio, P., de Fonseca, F.R., Behavioural consequences of maternal exposure to natural cannabinoids in rats. Psychopharmacology 122:1 (1995), 1–14.
110. Pacher, P., Mechoulam, R., Is lipid signaling through cannabinoid 2 receptors part of a protective system?. Prog. Lipid Res. 50:2 (2011), 193–211.
111. Pacher, P., Batkai, S., Kunos, G., Blood pressure regulation by endocannabinoids and their receptors. Neuropharmacology 48:8 (2005), 1130–1138.
112. Pandey, R., et al. Endocannabinoids and immune regulation. Pharmacol. Res. 60:2 (2009), 85–92.
113. Paria, B.C., et al. Dysregulated cannabinoid signaling disrupts uterine receptivity for embryo implantation. J. Biol. Chem. 276:23 (2001), 20523–20528.
114. Pernia-Andrade, A.J., et al. Spinal endocannabinoids and CB1 receptors mediate C-fiber-induced heterosynaptic pain sensitization. Science 325:5941 (2009), 760–764.
115. Pertwee, R.G., et al. International Union of Basic and Clinical Pharmacology. LXXIX. Cannabinoid receptors and their ligands: beyond CB(1) and CB(2). Pharmacol. Rev. 62:4 (2010), 588–631.
116. Radwan, M.M., et al. Non-cannabinoid constituents from a high potency Cannabis sativa variety. Phytochemistry 69:14 (2008), 2627–2633.
117. Radwan, M.M., et al. Isolation and characterization of new Cannabis constituents from a high potency variety. Planta Med. 74:3 (2008), 267–272.
118. Radwan, M.M., et al. Biologically active cannabinoids from high-potency Cannabis sativa. J. Nat. Prod. 72:5 (2009), 906–911.
119. Rajesh, M., et al. Cannabinoid-2 receptor agonist HU-308 protects against hepatic ischemia/reperfusion injury by attenuating oxidative stress, inflammatory response, and apoptosis. J. Leukoc. Biol. 82:6 (2007), 1382–1389.
120. Randall, M.D., Kendall, D.A., O'Sullivan, S., The complexities of the cardiovascular actions of cannabinoids. Br. J. Pharmacol. 142:1 (2004), 20–26.
121. Regehr, W.G., Carey, M.R., Best, A.R., Activity-dependent regulation of synapses by retrograde messengers. Neuron 63:2 (2009), 154–170.
122. Renard, J., et al. Long-term consequences of adolescent cannabinoid exposure in adult psychopathology. Front. Neurosci., 8, 2014, 361.
123. Rice, D., Barone, S. Jr., Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ. Health Perspect. 108:Suppl. 3 (2000), 511–533.
124. Schneider, M., Cannabis use in pregnancy and early life and its consequences: animal models. Eur. Arch. Psychiatry Clin. Neurosci. 259:7 (2009), 383–393.
125. Silva, L., et al. Prenatal tetrahydrocannabinol (THC) alters cognitive function and amphetamine response from weaning to adulthood in the rat. Neurotoxicol. Teratol. 34:1 (2012), 63–71.
126. Smith, A.M., et al. Effects of prenatal marijuana on visuospatial working memory: an fMRI study in young adults. Neurotoxicol. Teratol. 28:2 (2006), 286–295.
127. Sonon, K.E., et al. Prenatal marijuana exposure predicts marijuana use in young adulthood. Neurotoxicol. Teratol. 47 (2015), 10–15.
128. State Medical Marijuana Laws 2016.
129. Steffens, S., Pacher, P., Targeting cannabinoid receptor CB(2) in cardiovascular disorders: promises and controversies. Br. J. Pharmacol. 167:2 (2012), 313–323.
130. Steg, P.G., et al. Heart rate and use of beta-blockers in stable outpatients with coronary artery disease. PLoS One, 7(5), 2012, e36284.
131. Sugamura, K., et al. Activated endocannabinoid system in coronary artery disease and antiinflammatory effects of cannabinoid 1 receptor blockade on macrophages. Circulation 119:1 (2009), 28–36.
132. Sugiura, T., et al. 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem. Biophys. Res. Commun. 215:1 (1995), 89–97.
133. Sundram, S., Cannabis and neurodevelopment: implications for psychiatric disorders. Hum. Psychopharmacol. 21:4 (2006), 245–254.
134. Szutorisz, H., et al. Parental THC exposure leads to compulsive heroin-seeking and altered striatal synaptic plasticity in the subsequent generation. Neuropsychopharmacology 39:6 (2014), 1315–1323.
135. Tan, B., et al. Targeted lipidomics: discovery of new fatty acyl amides. AAPS J. 8:3 (2006), E461–E465.
136. Thompson, B.L., Levitt, P., Stanwood, G.D., Prenatal exposure to drugs: effects on brain development and implications for policy and education. Nat. Rev. Neurosci. 10:4 (2009), 303–312.
137. Tikkanen, J., Heinonen, O.P., Risk factors for ventricular septal defect in Finland. Public Health 105:2 (1991), 99–112.
138. Tortoriello, G., et al. Miswiring the brain: Delta9-tetrahydrocannabinol disrupts cortical development by inducing an SCG10/stathmin-2 degradation pathway. EMBO J. 33:7 (2014), 668–685.
139. Trezza, V., et al. Effects of perinatal exposure to delta-9-tetrahydrocannabinol on the emotional reactivity of the offspring: a longitudinal behavioral study in Wistar rats. Psychopharmacology 198:4 (2008), 529–537.
140. Trezza, V., et al. Altering endocannabinoid neurotransmission at critical developmental ages: impact on rodent emotionality and cognitive performance. Front. Behav. Neurosci., 6, 2012, 2.
141. van Gelder, M.M., et al. Characteristics of pregnant illicit drug users and associations between cannabis use and perinatal outcome in a population-based study. Drug Alcohol Depend. 109:1–3 (2010), 243–247.
142. Varner, M.W., et al. Association between stillbirth and illicit drug use and smoking during pregnancy. Obstet. Gynecol. 123:1 (2014), 113–125.
143. Vorhees, C.V., Concepts in teratology and developmental toxicology derived from animal research. Ann. N. Y. Acad. Sci. 562 (1989), 31–41.
144. Wagner, J.A., et al. Hemodynamic effects of cannabinoids: coronary and cerebral vasodilation mediated by cannabinoid CB(1) receptors. Eur. J. Pharmacol. 423:2–3 (2001), 203–210.
145. Walsh, S.K., et al. Acute administration of cannabidiol in vivo suppresses ischaemia-induced cardiac arrhythmias and reduces infarct size when given at reperfusion. Br. J. Pharmacol. 160:5 (2010), 1234–1242.
146. Watkins, M., Botto, L.D., Maternal prepregnancy weight and congenital heart defects in the offspring. Epidemiology 11:4 (2001), 439–446.
147. Weis, F., et al. Substantially altered expression pattern of cannabinoid receptor 2 and activated endocannabinoid system in patients with severe heart failure. J. Mol. Cell. Cardiol. 48:6 (2010), 1187–1193.
148. Weiser, M., Noy, S., Interpreting the association between cannabis use and increased risk for schizophrenia. Dialogues Clin. Neurosci. 7:1 (2005), 81–85.
149. Williams, L.J., Correa, A., Rasmussen, S., Maternal lifestyle factors and risk for ventricular septal defects. Birth Defects Res. A Clin. Mol. Teratol. 70:2 (2004), 59–64.
150. Wu, T.C., et al. Pulmonary hazards of smoking marijuana as compared with tobacco. N. Engl. J. Med. 318:6 (1988), 347–351.
151. Yang, S., Fombonne, E., Kramer, M.S., Duration of gestation, size at birth and later childhood behaviour. Paediatr. Perinat. Epidemiol. 25:4 (2011), 377–387.
152. Youngson, N.A., Whitelaw, E., Transgenerational epigenetic effects. Annu. Rev. Genomics Hum. Genet. 9 (2008), 233–257.
153. Zimmer, A., et al. Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc. Natl. Acad. Sci. U. S. A. 96:10 (1999), 5780–5785.
154. Zubrzycki, M., et al. A new face of endocannabinoids in pharmacotherapy. Part II: role of endocannabinoids in inflammation-derived cardiovaascular diseases. J. Physiol. Pharmacol. 65:2 (2014), 183–191.
155. Zumbrun, E.E., et al. Epigenetic regulation of immunological alterations following prenatal exposure to marijuana cannabinoids and its long term consequences in offspring. J. NeuroImmune Pharmacol., 10(2), 2015, 9.