A cannabinoid analogue of Δ9-tetrahydrocannabinol disrupts neural development in chick

Birth Defects Research Part B - Developmental and Reproductive Toxicology

Volumn 83, Issue 5, 2008, Pages 477-488

  Psychoyos, Delphine ^a   Hungund, Basalingappa ^b,c,d   Cooper, Thomas ^b,c,d   Finnell, Richard H ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b Columbia University ^*  (United States)

^c NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^d NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

Author keywords

Anencephaly; Animal model; Brain malformation; Cannabinoids; Chick embryo; CNS development; Neural folds; Neural plate; Neural tube defects

Indexed keywords

CANNABINOID; DRONABINOL; O 2545; UNCLASSIFIED DRUG; PSYCHOTROPIC AGENT; TETRAHYDROCANNABINOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; BRAIN MALFORMATION; CANNABIS ADDICTION; CHICK; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYOTOXICITY; GASTRULATION; NEURAL TUBE DEFECT; NEUROECTODERM; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; SOMITE; SPINAL CORD MALFORMATION; ANIMAL; CHEMICALLY INDUCED DISORDER; CYTOLOGY; DRUG EFFECT; MESODERM; NERVOUS SYSTEM DEVELOPMENT;

ANIMALIA; CANNABIS SATIVA;

ANIMALS; CHICK EMBRYO; MESODERM; NEURAL TUBE DEFECTS; NEUROGENESIS; PSYCHOTROPIC DRUGS; SOMITES; TETRAHYDROCANNABINOL;

EID: 55449108707     PISSN: 15429733     EISSN: None     Source Type: Journal    
DOI: 10.1002/bdrb.20166     Document Type: Article

References (69)

1. Abel EL. 1983. Marihuana. Tobacco. Alcohol and Reproduction. Boca Raton: CRC Press.
2. Aguado T, Romero E, Monory K, Palazuelos J, Sendtner M, Marsicano G, Lutz B, Guzmán M, Galve-Roperh I. 2007. The CB1 cannabinoid receptor mediates excitotoxicity-induced neural progenitor proliferation and neurogenesis. J Biol Chem 282:23892-23898.
3. Antonelli T, Tomasini MC, Tattoli M, Ferraro L. 2005. Prenatal exposure to the CB1 receptor agonist WIN 55,212-2 causes learning disruption associated with impaired cortical NMDA receptor function and emotional reactivity changes in rat offspring. Cereb Cortex 15:2013-2020.
4. Balinsky BI. 1975. An Introduction to Embryology. New York: WB Saunders.
5. Bally-Cuif L, Gulisano M, Broccoli V, Boncinelli E. 1995. c-Otx2 is expressed in two different phases of gastrulation and is sensitive to retinoic acid treatment in chick embryo. Mech Dev 49:49-63.
6. Banerjee BN, Galbreath C, Sofia RD. 1975. Teratologic evaluation of synthetic delta-9-tetrahydrocannabinol in rats. Teratology 11:99-101.
7. Begbie J, Doherty P, Graham A. 2004. Cannabinoid receptor, CB1, expression follows neuronal differentiation in the early chick embryo. J Anat 205:213-218.
8. Blackard C, Tennes K. 1984. Human placental transfer of cannabinoids. N Engl J Med 311:797-799.
9. Buckley NE, Hansson S, Harta G, Mezey E. 1998. Expression of the CB1 and CB2 receptor messenger RNAs during embryonic development in the rat. Neuroscience 82:1131-1149.
10. Butler H, Juurlink BHJ. 1987. An atlas for staging mammalian and chick embryos. Florida: CRC Press.
11. Carakushansky RL, Neu RL, Gardner LI. 1969. Lysergide and cannabis as possible teratogens in man. Lancet 1:150-151.
12. Christiansen J, Coles E, Robinson V, Pasini A, Wilkinson, DG. 2001. Screening from a subtracted embryonic chick hindbrain cDNA library: identification of genes expressed during hindbrain, midbrain and cranial neural crest development. Mech Dev 102:119-133.
13. Connolly DJ, Patel K, Cooke J. 1997. Chick Noggin is expressed in the organizer and neural plate during axial development, but offers no evidence of involvement in primary axis formation. Int J Dev Biol 41:389-396.
14. Day NL, Richardson G. 1991. Prenatal marijuana use: epidemiology, methodological issues and infant outcome. In: Chasnoff IJ, editor. Clinics in Perinatology. Philadelphia: WB Saunders. p 77-92.
15. Fleischman RW, Hayden DW, Rosenkrantz H, Braude MC. 1975. Teratologic evaluation of delta-9-tetrahydrocannabinol in mice, including a review of the literature. Teratology 12:47-50.
16. Fleischman RW, Naqvi RH, Rosenkrantz H, Hayden DW. 1980. The embryotoxic effects of cannabinoids in rats and mice. J Environ Pathol Toxicol 4:471-482.
17. Fried PA, Watkinson B, Gray R. 2005. Neurocognitive consequences of marihuana - a comparison with pre-drug performance. Neurotoxicol Teratol 27:231-239.
18. Gaoni Y, Mechoulam R. 1971. The isolation and structure of delta-1-tetrahydrocannabinol and other neutral cannabinoids from hashish. J Am Chem Soc 93:217-224.
19. Geber WF, Schramm LC. 1969. Effect of marihuana extract on fetal hamsters and rabbits. Toxicol Appl Pharmacol 14:276-282.
20. Gebhardt DE. 1972. The use of chick embryo in applied teratology. In: Woolam DHM, editor. Advances in Teratology. London: Academic Press. p 97-111.
21. Gianutsos G, Abbatiello ER. 1972. The effect of prenatal cannabis sativa on maze learning ability in the rat. Psychopharmacology 27:117-122.
22. Goldschmidt L, Richardson GA, Cornelius MD, Day NL. 2004. Prenatal marijuana and alcohol exposure and academic achievement at age 10. Neurotoxicol Teratol 26:521-532.
23. Goulding MD, Lumsden A, Gruss P. 1993. Signals from the notochord and floor plate regulate the region-specific expression of two Pax genes in the developing spinal cord. Development 117:1001-1016.
24. Haley SL, Wright PL, Plank JB, Keplinger ML, Braude MC, Calandra JC. 1975. The effect of natural and synthetic delta-9-tetrahydrocannabinol on fetal development. Toxicol Applied Pharmacol 25:450-457.
25. Hamburger V, Hamilton HL. 1951. A series of normal stages in the development of the chick. J Morphol 88:49-92.
26. Harbison RD, Mantilla-Plata B. 1972. Prenatal toxicity, maternal distribution and placental transfer of tetrahydrocannabinol. J Pharmacol Exp Ther 180:1446-1453.
27. Harbison RD, Mantilla-Plata B, Lubin DJ. 1977. Alteration of delta-9-tetrahydrocannabinol-induced teratogenicity by stimulation and inhibition of its metabolism. J Pharmacol Exp Ther 202:455-465.
28. Harkness LM, Baird DT. 1997. Morphological and molecular characteristics of living human fetuses between Carnegie stages 7 and 23: developmental stages in the post-implantation embryo. Hum Reprod Update 3:3-23.
29. Hecht F, Beals RK, Lees MH, Jolly H, Roberts P. 1968. Lysergic-acid-diethylamide and cannabis as possible teratogens in man. Lancet 2:1087.
30. Henrique D, Adam J, Myat A, Chitnis A, Lewis J, Ish-Horowicz D. 1995. Expression of a Delta homologue in prospective neurons in the chick. Nature 375:787-790.
31. Hingson R, Alpert JJ, Day N, Dooling E, Kayne H, Morelock S, Oppenheimer E, Zuckerman B. 1982. Effects of maternal drinking and marijuana use on fetal growth and development. Pediatrics 70:539-546.
32. Irving C, Nieto MA, DasGupta R, Charnay P, Wilkinson DG. 1996. Progressive spatial restriction of Sek-1 and Krox-20 gene expression during hindbrain segmentation. Dev Biol 173:26-38.
33. Jelinek R. 1982. Use of chick embryo in screening for embryotoxicity. Teratog Carcinog Mutagen 2:255-561.
34. Jonega MG. 1976. A study of teratological effects of intravenous, subcutaneous, and intragastric administration of delta 9-tetrahydrocannabinol in mice. Teratology 36:151-162.
35. Jonega MG. 1977. Effects of delta 9-tetrahydrocannabinol on hamster fetuses. J Toxicol Environ Health 2:1031-1040.
36. Kotwani A. 1998. Use of chick embryo in screening for teratogenicity. Indian J Physiol Pharmacol 42:189-204.
37. Levin M, Johnson RL, Stern CD, Kuehn M, Tabin C. 1995. A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 82:803-814.
38. Mantilla-Plata B, Clewe CL, Harbison RD. 1973. Teratogenic and mutagenic studies of -9-tetrahydrocannabinol in mice. Fed Proc 32:746-756.
39. Mantilla-Plata B, Clewe CL, Harbison RD. 1975. 9-tetrahydrocannabinol- induced changes in prenatal growth and development of animals. Toxicol Appl Pharmacol 33:333-340.
40. Martin BR, Wiley JL, Beletskaya I, Sim-Selley, LJ, Smith FL, Dewey WL, Cottney J, Adams J, Baker J, Hill D., et al. 2006. Pharmacological characterization of novel water-soluble cannabinoids. Pharmacol Exp Ther 318:1230-1239.
41. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI. 1990. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346:561-564.
42. McGilveray IJ. 2005. Pharmacokinetics of cannabinoids. Pain Res Manag 10:15A-22A.
43. Nakatsuji N, Johnson KE. 1984. Effects of ethanol on the primitive streak stage mouse embryo. Teratology 29:369-375.
44. New DAT. 1955. A new technique for the cultivation of the chick embryo in vitro. J Embryol Exp Morph 3:326-331.
45. NIDA, National Institute on Drug Abuse. 2001. National Household Survey on Drug Abuse Volume I: Summary of National Findings - Prevalence & Correlates of Alcohol, Tobacco, and Illegal Drug Use. Bethesda: NIDA. http://www.oas.samhsa.gov/nhsda/2k1nhsda/vol1/toc.htm.
46. Nishimura H, Tanimura T, Semba R, Uwabe C. 1974. Normal development of early human embryos: observation of 90 specimens at Carnegie stages 7 to 13. Teratology 10:1-5.
47. Noland JS, Singer LT, Short EJ, Minnes S, Arendt RE, Kirchner, HL, Bearer C. 2005. Prenatal drug exposure and selective attention in preschoolers. Neurotoxicol Teratol 27:429-438.
48. O'Rahilly R, Müller F. 1987. Developmental Stages in Human Embryos, Carnegie Institution of Washington, Washington Publication 637.
49. Paria BC, Das SK, Dey SK. 1995. The pre-implantation mouse embryo is a target for cannabinoid ligand-receptor signaling. Proc Natl Acad Sci USA 92:9460-9464.
50. Paria BC, Dey SK. 2000. Ligand-receptor signaling with endocannabinoids in pre-implantation embryo development and implantation. Chem Phys Lipids 108:211-220.
51. Persaud TV, Ellington AC. 1967. Cannabis in early pregnancy. Lancet 2:1306.
52. Persaud TV, Ellington AC. 1968a. Teratogenic activity of cannabis resin. Lancet 2:406-407.
53. Persaud TV, and Ellington AC. 1968b. The effects of cannabis sativa L. (Ganja) on developing rat embryos - preliminary observations. West Indian Med J 4:232-234.
54. Piomelli D. 2004. THC: moderation during implantation. Nature Med 10:19-20.
55. Psychoyos D, Stern CD. 1996a. Fates and migratory routes of primitive streak cells in the chick embryo. Development 122:1523-1534.
56. Psychoyos D, Stern CD. 1996b. Restoration of the organizer after radical ablation of Hensen's node and the anterior primitive streak in the chick embryo. Development 122:3263-3273.
57. Rex M, Orme A, Uwanogho D, Tointon K, Wigmore PM, Sharpe PT, Scotting PJ. 1997. Dynamic expression of chicken Sox2 and Sox3 genes in ectoderm induced to form neural tissue. Dev Dyn 209:323-332.
58. Romanof f AL. 1960. The Avian Embryo: Structural and Functional Development. New York: MacMillan.
59. Rosenkrantz H. 1978. Effects of cannabis on fetal development of rodents. Adv Biosc 22:479-499.
60. Rosenkrantz H. 1983. Cannabis, marijuana and cannabinoid toxicological manifestations in man and animals. In Cannabis and Health Hazards (Fehr KO and Kalant H editors). Toronto: Addiction Research Foundation. p 91-175.
61. Schmidt M, Patterson M, Farrell E, Munsterberg A. 2004. Dynamic expression of Lef/Tcf family members and beta-catenin during chick gastrulation, neurulation, and early limb development. Dev Dyn 229:703-707.
62. Stern CD. 2002. Induction and initial patterning of the nervous system - the chick embryo enters the scene. Curr Opin Genet Dev 12:447-451.
63. Straiker A, Stella N, Piomelli D, Mackie K, Karten HJ, Maguire G. 1999. Cannabinoid CB1 receptors and ligands in vertebrate retina: localization and function of an endogenous signaling system. Proc Natl Acad Sci USA 96:14565-14570.
64. Sulik K. 2008. Carnegie Stages - Scanning Electron Micrography, The University of New South Wales, Sydney, Australia. http://embryology.med.unsw. edu.au/wwwhuman/Stages/Stagesem.htm.
65. Uyeno ET. 1973. delta-9-tetrahydrocannabinol administered during pregnancy of the rat. Proc. West Pharmacol Soc 16:614-667.
66. WHO, World Health Organization. 1997. Epidemiology of Cannabis Use. In: Programme on Substance Abuse. Cannabis: A Health Perspective and Research Agenda. Geneva: WHO. http://whqlibdoc.who.int/hq/1997/WHO_MSA_PSA_97.4.pdf.
67. Wilkinson D. 1992. In situ Hybridization: A Practical Approach. Oxford: IRL Press. p 75-83.
68. Wilson JG. 1978. Survey of in vitro systems: Their potential uses in teratogenicity screening. In: Wilson JG, Fraser FC, editors. Handbook of Teratology. New York: Plenum Press. Vol 4, p 135-158.
69. Wright PL, Smith SH, Keplinger ML, Calandra LC, Braude MC. 1976. Reproductive and teratologic studies with D-9-tetrahydrocannabinol and crude marihuana extract. Toxicol Appl Pharmacol 38:223-235.