Effects of cannabinoids on preimplantation mouse embryo development and implantation are mediated by brain-type cannabinoid receptors

Biology of Reproduction

Volumn 58, Issue 6, 1998, Pages 1490-1495

  Paria, B C ^a   Ma, W ^a   Andrenyak, D M ^b   Schmid, P C ^c   Schmid, H H O ^c   Moody, D E ^b   Deng, H ^d   Makriyannis, A ^d   Dey, S K ^a  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b UNIVERSITY OF UTAH   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANANDAMIDE; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR; CYTOCHROME P450; CYTOCHROME P450 INHIBITOR; DRONABINOL; RECEPTOR SUBTYPE; RIMONABANT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG METABOLISM; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; MOUSE; NIDATION; NONHUMAN; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; REGULATORY MECHANISM; STEREOISOMERISM;

ANIMALS; ARACHIDONIC ACIDS; BRAIN; CANNABINOIDS; CYTOCHROME P-450 ENZYME SYSTEM; EMBRYO; EMBRYO IMPLANTATION; EMBRYONIC AND FETAL DEVELOPMENT; EMBRYONIC DEVELOPMENT; ENZYME INHIBITORS; FEMALE; GLYCERIDES; MALE; MICE; PIPERIDINES; POLYUNSATURATED ALKAMIDES; PREGNANCY; PYRAZOLES; RECEPTORS, CANNABINOID; RECEPTORS, DRUG; TETRAHYDROCANNABINOL;

ANIMALIA; MAMMALIA;

EID: 0031811671     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod58.6.1490     Document Type: Article

References (43)

1. Psychoyos A. Endocrine control of egg implantation. In: Greep RO, Astwood EG, Geiger SR (eds.), Handbook of Physiology. Washington, DC: American Physiological Society; 1973: 187-215.
2. Paria BC, Huet-Hudson YM, Dey SK. Blastocysts state of activity determines the "window" of implantation in the receptive mouse uterus. Proc Natl Acad Sci USA 1993; 90:10159-10162.
3. Enders AC, Schlafke S. A morphological analysis of the early implantation stages in the rat. Am J Anat 1967; 120:185-226.
4. Das SK, Wang X-N, Paria BC, Damm D, Abraham JA, Klagsbrun M, Andrews GK, Dey SK. Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation. Development 1994; 120:1071-1083.
5. Parr EL, Tung HN, Parr MB. Apoptosis as the mode of uterine epithelial cell death during embryo implantation in mice and rats. Biol Reprod 1987; 36:211-225.
6. Schlafke S, Enders AC. Cellular basis of interaction between trophoblast and uterus at implantation. Biol Reprod 1975; 12:41-65.
7. Yoshinaga K. Inhibition of implantation by advancement of uterine sensitivity and refractoriness. In: Leroy F, Finn CA, Psychoyos A, Hubinot PO (eds.), Blastocyst-Endometrial Relationships: Progressin Reproductive Biology. Basel: Karger 1980; 7:189-199.
8. Yoshinaga K, Adams CE. Delayed implantation in spayed, progesterone-treated adult mouse. J Reprod Fertil 1966; 12:593-595.
9. Nilsson O. The morphology of blastocyst implantation. J Reprod Fertil 1974; 39:187-194.
10. Dewey WL. Cannabinoid pharmacology. Pharmacol Rev 1986; 38: 151-178.
11. 9-THC: reassessment of the putative three-point cannabinoid-receptor interaction. Drug Alcohol Depend 1995; 37:231-240.
12. Bloch E, Thysen B, Morrill GA, Gardner E, Fujimoto G. Effects of cannabinoids on reproduction and development. Vitam Horm 1978; 36:203-258.
13. Smith CG, Asch RH. Drug abuse and reproduction. Fertil Steril 1987; 48:355-373.
14. Chang MC, Berkery D, Schuel R, Laychock SG, Zimmerman AM, Zimmerman S, Schuel H. Evidence for a cannabinoid receptor in sea urchin sperm and its role in blockade of the acrosome reaction. Mol Reprod Dev 1993; 36:507-516.
15. Schuel H, Goldstein E, Mechoulam R, Zimmerman AM, Zimmerman S. Anandamide (arachidonylethanolamide), a brain cannabinoid receptor agonist, reduces sperm fertilizing capacity in sea urchins by inhibiting the acrosome reaction. Proc Natl Acad Sci USA 1994; 91: 7678-7682.
16. Howlett AC. Pharmacology of cannabinoid receptor. Annu Rev Pharmacol Toxicol 1995; 35:607-634.
17. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990; 346:561-564.
18. Munro S, Thomas KL, Abu-sharr M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993; 365:61-65.
19. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevvenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 1992; 258:1946-1949.
20. Felderr CC, Veluz JS, Williams HL, Briley EM, Matsuda LA. Cannabinoid agonists stimulate both receptor-and non-receptor-mediated signal transduction pathways in cells transfected with and expressing cannabinoid receptor clones. Mol Pharmacol 1992; 42:838-845.
21. Schmid PC, Paria BC, Krebsbach RJ, Schmid HHO, Dey SK. Changes in anandamide levels in mouse uterus are associated with uterine receptivity for embryo implantation. Proc Natl Acad Sci USA 1997; 94:4188-4192.
22. Mechoulam R, Ben Shabat S, Hanus L, Ligumsky M, Kaminski NE, Schatz AR, Gopher A, Almog S, Martin BR, Compton DR, Pertwee RG, Griffin G, Bayewitch M, Barg J, Vogel Z. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 1995; 50:83-90.
23. Sugiura T, Kondo S, Sukagawa A, Nakane S, Shinoda A, Itoh K, Yamashita A, Waku K. 2-arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 1995; 215:89-97.
24. Stella N, Schweitzer P, Piomelli D. A second endogenous cannabinoid that modulates long-term potentiation. Nature 1997; 388:773-777.
25. Paria BC, Das SK, Dey SK. The preimplantation mouse embryo is a target for cannabinoid ligand-receptor signaling. Proc Natl Acad Sci USA 1995; 92:9460-9464.
26. Yang ZM, Paria BC, Dey SK. Activation of brain-type cannabinoid receptors interferes with preimplantation mouse embryo development. Biol Reprod 1996; 55:756-761.
27. Paria BC, Kapur S, Dey SK. Effects of 9-ene-tetrahydrocannabinol on uterine estrogenicity in the mouse. J Steroid Biochem Mol Biol 1992; 42:713-719.
28. 9-tetrahydrocannabinol by fractionated isoenzymes of mouse hepatic cytochrome P-450. Res Commun Subst Abuse 1986; 7:89-97.
29. Bonnin A, Miguel RD, Fernandez-Ruiz JJ, Cebeira M, Ramos JA. Possible role of the cytochrome P-450-linked monooxygenase system in preventing delta-tetrahydrocannabinol-induced stimulation of tuberoinfundibular dopaminergic activity in female rats. Biochem Pharmacol 1994; 48:1387-1392.
30. Rinaldi-Carmona M, Barth F, Heaulme M, Alonso R, Shire D, Congy C, Soubrie P, Brelieree J-C, Le Fur G. Biochemical and pharmacological characterization of SR141716A, the first potent and selective brain cannabinoid receptor antagonist. Life Sci 1995; 56:1941-1947.
31. Rinaldi-Carmona M, Barth F, Heaulme M, Shire D, Calandra B, Congy C, Martinez S, Maruani J, Neliat G, Caputt D, Ferrara P, Soubrie P, Breliere JC, Le Fur G. SR141716A, a potent and selective antagonist of the brain cannabinoid receptor. FEBS Lett 1994; 350:240-244.
32. Rinaldi-Carmona M, Barth F, Millan J, Derocq J-M, Casellas P, Congy, C, Oustric D, Sarran M, Bouaboula M, Calandra B, Portier M, Shire D, Breliere JC, Le Fur G. SR 144528: The first potent and selective antagonist of the CB2 cannabinoid receptor. J Pharmacol Exp Ther 1998; (in press).
33. 123-labeled AM251: a radioiodinated ligand which binds in vivo to mouse brain cannabinoid CB1 receptors. Eur J Pharmacol 1996; 307:331-338.
34. Lan R, Gately JS, Makriyannis A. Preparation of iodine-123 labeled AM 251: a potential SPECT radioligand for the brain cannabinoid CB1 receptor. J Labelled Compd Radiopharm 1996; 38:875-881.
35. Paria BC, Dey SK. Preimplantation embryo development in vitro: cooperative interactions among embryos and role of growth factors. Proc Natl Acad Sci USA 1990; 87:4756-4760.
36. Whitten WK. Nutrient requirements for the culture of preimplantation mouse embryos in vitro. Adv Biosci 1971; 6:129-139.
37. Kantor BS, Dey SK, Johnson DC. Catechol oestrogen induced initiation of implantation in delayed implanting rat. Act Endocrinol 1985; 109:418-422.
38. 9-tetrahydrocannabinol and two major metabolites in physiological specimens using capillary column gas chromatography negative ion chemical ionization mass spectrophotometry. Biomed Mass Spectrom 1983; 10:316-323.
39. Paria BC, Deutsch DD, Dey SK. The uterus is a potential site for anandamide synthesis and hydrolysis: differential profiles of anandamide synthase and hydrolase activities in the mouse uterus during the preimplantation period. Mol Reprod Dev 1996; 45:183-192.
40. Matsunaga T, Iwawaki Y, Watanabe K, Yamamoto I, Kageyama T, Yoshimura H. Metabolism of 9-tetrahydrocannabinol by cytochrome P450 isozymes purified from hepatic microsomes of monkeys. Life Sci 1995; 56:2089-2095.
41. Harvey DJ, Paton WDM. Metabolism of the cannabinoids. Rev Biochem Toxicol 1986; 6:221-259.
42. Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, De Costa BR, Rice KC. Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA 1990; 87:1932-1936.
43. Das SK, Paria BC, Chakraborty I, Dey SK. Cannabinoid ligand-receptor signaling in the mouse uterus. Proc Natl Acad Sci USA 1995; 92:4332-4336.