The grass isn't always greener: The effects of cannabis on embryological development

BMC Pharmacology and Toxicology

Volumn 17, Issue 1, 2016, Pages

  Friedrich, Joseph ^a   Khatib, Dara ^a   Parsa, Keon ^a   Santopietro, Ariana ^a   Gallicano, G Ian ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Angiogenesis; Cannabis; Folic acid; Metabolism; Neurogenesis; Pre implantation; Pregnancy

Indexed keywords

CANNABIS; CERAMIDE; CYCLINE; FOLIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; VASCULOTROPIN;

ADVERSE OUTCOME; APOPTOSIS; CANNABIS SMOKING; CANNABIS USE; CELL MIGRATION; CONCENTRATION (PARAMETERS); EMBRYO DEVELOPMENT; HUMAN; METABOLISM; NERVE CELL DIFFERENTIATION; NONHUMAN; PLACENTAL TRANSFER; PREIMPLANTATION EMBRYO; REVIEW;

EID: 84988933544     PISSN: None     EISSN: 20506511     Source Type: Journal    
DOI: 10.1186/s40360-016-0085-6     Document Type: Review

References (53)

1. Wang H, Dey SK, Maccarrone M. Jekyll and hyde: two faces of cannabinoid signaling in male and female fertility. Endocr Rev. 2006;27(5):427-48.
2. Khare M, Taylor AH, Konje JC, Bell SC. Delta9-tetrahydrocannabinol inhibits cytotrophoblast cell proliferation and modulates gene transcription. Mol Hum Reprod. 2006;12(5):321-33.
3. Ganapathy V. Drugs of abuse and human placenta. Life Sci. 2011;88(21-22):926-30.
4. Noland JS, Singer LT, Short EJ, Minnes S, Arendt RE, Lester Kirchner H, Bearer C. Prenatal drug exposure and selective attention in preschoolers. Neurotoxicol Teratol. 2005;27(3):429-38.
5. 9-tetrahydrocannabinol disrupts neural development in chick. Birth Defects Res. 2008;83(5):477-88.
6. Ohlsson A, Lindgren JE, Wahlen A, Agurell S, Hollister LE, Gillespie HK. Plasma delta-9 tetrahydrocannabinol concentrations and clinical effects after oral and intravenous administration and smoking. Clin Pharmacol Ther. 1980;28(3):409-16.
7. Heishman SJ, Huestis MA, Henningfield JE, Cone EJ. Acute and residual effects of marijuana: profiles of plasma THC levels, physiological, subjective, and performance measures. Pharmacol Biochem Behav. 1990;37(3):561-5.
8. Azorlosa JL, Heishman SJ, Stitzer ML, Mahaffey JM. Marijuana smoking: effect of varying delta 9-tetrahydrocannabinol content and number of puffs. J Pharmacol Exp Ther. 1992;261(1):114-22.
9. Heishman SJ, Stitzer ML, Yingling JE. Effects of tetrahydrocannabinol content on marijuana smoking behavior, subjective reports, and performance. Pharmacol Biochem Behav. 1989;34(1):173-9.
10. Perez-Reyes M. Marijuana smoking: factors that influence the bioavailability of tetrahydrocannabinol. NIDA Res Monogr. 1990;99:42-62.
11. Huestis MA. Human Cannabinoid Pharmacokinetics. Chem Biodivers. 2007;4(8):1770-804.
12. Huestis MA, Henningfield JE, Cone EJ. Blood cannabinoids. I. Absorption of THC and formation of 11-OH-THC and THCCOOH during and after smoking marijuana. J Anal Toxicol. 1992;16(5):276-82.
13. Mehmedic Z, Chandra S, Slade D, Denham H, Foster S, Patel AS, Ross SA, Khan IA, ElSohly MA. Potency trends of Delta9-THC and other cannabinoids in confiscated cannabis preparations from 1993 to. J Forensic Sci 2010. 2008;55(5):1209-17.
14. Law B, Mason PA, Moffat AC, Gleadle RI, King LJ. Forensic aspects of the metabolism and excretion of cannabinoids following oral ingestion of cannabis resin. J Pharm Pharmacol. 1984;36(5):289-94.
15. Wang GS, Roosevelt G, Le Lait MC, Martinez EM, Bucher-Bartelson B, Bronstein AC, Heard K. Association of unintentional pediatric exposures with decriminalization of marijuana in the United States. Ann Emerg Med. 2014;63(6):684-9.
16. Hopfer C. Implications of marijuana legalization for adolescent substance use. Subst Abus. 2014;35(4):331-5.
17. Vandrey R, Raber JC, Raber ME, Douglass B, Miller C, Bonn-Miller MO. Cannabinoid Dose and Label Accuracy in Edible Medical Cannabis Products. JAMA. 2015;313(24):2491-93.
18. Schou J, Prockop LD, Dahlström G, Rohde C. Penetration of delta-9-tetrahydrocannabinol and 11-OH-delta-9-tetrahydrocannabinol through the Blood-brain Barrier. Acta Pharmacol Toxicol. 2009;41(1):33-8.
19. Bailey JR, Cunny HC, Paule MG, Slikker WJ. Fetal disposition of delta-9-tetrahydrocannabinol (THC) during late pregnancy in the rhesus monkey. Toxicol Appl Pharmacol. 1987;90(2):315-21.
20. Martin BR, Dewey WL, Harris LS, Beckner JS. 3H-delta9-tetrahydrocannabinol distribution in pregnant dogs and their fetuses. Res Commun Chem Pathol Pharmacol. 1977;17(3):457-70.
21. Paria BC, Das SK, Dey SK. The preimplantation mouse embryo is a target for cannabinoid ligand-receptor signaling. Proc Natl Acad Sci U S A. 1995;92(21):9460-4.
22. Das SK, Paria BC, Chakraborty I, Dey SK. Cannabinoid ligand-receptor signaling in the mouse uterus. Proc Natl Acad Sci U S A. 1995;92(10):4332-6.
23. Paria BC, Song H, Wang X, Schmid PC, Krebsbach RJ, Schmid HH, Bonner TI, Zimmer A, Dey SK. Dysregulated cannabinoid signaling disrupts uterine receptivity for embryo implantation. J Biol Chem. 2001;276(23):20523-8.
24. Schmid PC, Paria BC, Krebsbach RJ, Schmid HH, Dey SK. Changes in anandamide levels in mouse uterus are associated with uterine receptivity for embryo implantation. Proc Natl Acad Sci U S A. 1997;94(8):4188-92.
25. Lauckner JE, Hille B, Mackie K. The cannabinoid agonist WIN55,212-2 increases intracellular calcium via CB1 receptor coupling to Gq/11 G proteins. Proc Natl Acad Sci U S A. 2005;102(52):19144-9.
26. Vogel Z, Barg J, Levy R, Saya D, Heldman E, Mechoulam R. Anandamide, a brain endogenous compound, interacts specifically with cannabinoid receptors and inhibits adenylate cyclase. J Neurochem. 1993;61(1):352-5.
27. Sun X, Dey SK. Aspects of endocannabinoid signaling in periimplantation biology. Mol Cell Endocrinol. 2008;286(1-2 Suppl 1):S3-11.
28. Derkinderen P, Ledent C, Parmentier M, Girault J. Cannabinoids activate p38 mitogen-activated protein kinases through CB1 receptors in hippocampus. J Neurochem. 2001;77(3):957-60.
29. Xie H, Sun X, Piao Y, Jegga AG, Handwerger S, Ko MS, Dey SK. Silencing or amplification of endocannabinoid signaling in blastocysts via CB1 compromises trophoblast cell migration. J Biol Chem. 2012;287(38):32288-97.
30. Cravatt BF, Demarest K, Patricelli MP, Bracey MH, Giang DK, Martin BR, Lichtman AH. Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc Natl Acad Sci U S A. 2001;98(16):9371-6.
31. Wang H, Guo Y, Wang D, Kingsley PJ, Marnett LJ, Das SK, DuBois RN, Dey SK. Aberrant cannabinoid signaling impairs oviductal transport of embryos. Nat Med. 2004;10(10):1074-80.
32. Gebeh AK, Willets JM, Bari M, Hirst RA, Marczylo TH, Taylor AH, Maccarrone M, Konje JC. Elevated anandamide and related N-acylethanolamine levels occur in the peripheral blood of women with ectopic pregnancy and are mirrored by changes in peripheral fatty acid amide hydrolase activity. J Clin Endocrinol Metab. 2013;98(3):1226-34.
33. Wang H, Matsumoto H, Guo Y, Paria BC, Roberts RL, Dey SK. Differential G protein-coupled cannabinoid receptor signaling by anandamide directs blastocyst activation for implantation. Proc Natl Acad Sci U S A. 2003;100(25):14914-9.
34. Burdge GC, Lillycrop KA. Folic acid supplementation in pregnancy: Are there devils in the detail? Br J Nutr. 2012;108(11):1924-30.
35. Araujo JR, Goncalves P, Martel F. Effect of cannabinoids upon the uptake of folic acid by BeWo cells. Pharmacology. 2009;83(3):170-6.
36. Blazquez C, Gonzalez-Feria L, Alvarez L, Haro A, Casanova ML, Guzman M. Cannabinoids inhibit the vascular endothelial growth factor pathway in gliomas. Cancer Res. 2004;64(16):5617-23.
37. Carmeliet P. Angiogenesis in health and disease. Nat Med. 2003;9(6):653-60.
38. Kerbel R, Folkman J. Clinical translation of angiogenesis inhibitors. Nat Rev Cancer. 2002;2(10):727-39.
39. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J. Vascular-specific growth factors and blood vessel formation. Nature. 2000;407(6801):242-8.
40. Sarfaraz S, Afaq F, Adhami VM, Mukhtar H. Cannabinoid receptor as a novel target for the treatment of prostate cancer. Cancer Res. 2005;65(5):1635-41.
41. Solinas M, Massi P, Cantelmo AR, Cattaneo MG, Cammarota R, Bartolini D, Cinquina V, Valenti M, Vicentini LM, Noonan DM, Albini A, Parolaro D. Cannabidiol inhibits angiogenesis by multiple mechanisms. Br J Pharmacol. 2012;167(6):1218-31.
42. Blazquez C, Casanova ML, Planas A, Gomez Del Pulgar T, Villanueva C, Fernandez-Acenero MJ, Aragones J, Huffman JW, Jorcano JL, Guzman M. Inhibition of tumor angiogenesis by cannabinoids. FASEB J. 2003;17(3):529-31.
43. Casanova ML, Blázquez C, Martínez-Palacio J, Villanueva C, Fernández-Aceñero MJ, Huffman JW, Jorcano JL, Guzmán M. Inhibition of skin tumor growth and angiogenesis in vivo by activation of cannabinoid receptors. J Clin Invest. 2003;111(1):43-50.
44. Diaz-Alonso J, Guzman M, Galve-Roperh I. Endocannabinoids via CB(1) receptors act as neurogenic niche cues during cortical development. Philos Trans R Soc Lond B Biol Sci. 2012;367(1607):3229-41.
45. Compagnucci C, Di Siena S, Bustamante MB, Di Giacomo D, Di Tommaso M, Maccarrone M, Grimaldi P, Sette C. Type-1 (CB1) Cannabinoid Receptor Promotes Neuronal Differentiation and Maturation of Neural Stem Cells. PLoS One. 2013;8(1):e54271.
46. Jiang W, Zhang Y, Xiao L, Van Cleemput J, Ji SP, Bai G, Zhang X. Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic- and antidepressant-like effects. J Clin Invest. 2005;115(11):3104-16.
47. Cameron HA, Mckay RDG. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 2001. 2001;435(4):406-17.
48. Aouadi M, Bost F, Caron L, Laurent K, Le Marchand Brustel Y, Binétruy B. p38 Mitogen-Activated Protein Kinase Activity Commits Embryonic Stem Cells to Either Neurogenesis or Cardiomyogenesis. Stem Cells. 2006;24(5):1399-406.
49. Derkinderen P, Valjent E, Toutant M, Corvol JC, Enslen H, Ledent C, Trzaskos J, Caboche J, Girault JA. Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus. J Neurosci. 2003;23(6):2371-82.
50. Rueda D, Navarro B, Martinez-Serrano A, Guzman M, Galve-Roperh I. The endocannabinoid anandamide inhibits neuronal progenitor cell differentiation through attenuation of the Rap1/B-Raf/ERK pathway. J Biol Chem. 2002;277(48):46645-50.
51. Nadeau V, Charron J. Essential role of the ERK/MAPK pathway in blood-placental barrier formation. Development. 2014;141(14):2825-37.
52. Corson LB, Yamanaka Y, Lai KM, Rossant J. Spatial and temporal patterns of ERK signaling during mouse embryogenesis. Development. 2003;130(19):4527-37.
53. Almeida LE, Roby CD, Krueger BK. Increased BDNF expression in fetal brain in the valproic acid model of autism. Mol Cell Neurosci. 2014;59:57-62.