The role of the endocannabinoid system in gametogenesis, implantation and early pregnancy

Human Reproduction Update

Volumn 13, Issue 5, 2007, Pages 501-513

  Taylor, A H ^a   Ang, C ^a   Bell, S C ^a   Konje, J C ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Anandamide; Cannabinoid; Fetal growth restriction; Pregnancy; Vascular bed

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 4 [6 METHOXY 2 (4 METHOXYPHENYL) 3 BENZOFURANYLCARBONYL]BENZONITRILE; ANANDAMIDE; CANNABINOID RECEPTOR; DELTA8 TETRAHYDROCANNABINOL; DRONABINOL; ENDOCANNABINOID; RIMONABANT; VANILLOID RECEPTOR 1;

CANNABIS ADDICTION; CLINICAL TRIAL; CONGENITAL MALFORMATION; ECTOPIC PREGNANCY; EMBRYO DEVELOPMENT; FEMALE INFERTILITY; FERTILIZATION; FETUS DEVELOPMENT; GAMETOGENESIS; HORMONAL REGULATION; HUMAN; INTRAUTERINE GROWTH RETARDATION; MALE INFERTILITY; MATERNAL SMOKING; NIDATION; NONHUMAN; OBESITY; OOCYTE MATURATION; OVARY FOLLICLE DEVELOPMENT; OVULATION; PLACENTA DEVELOPMENT; PREGNANCY OUTCOME; PREMATURE LABOR; PRIORITY JOURNAL; REVIEW; SPERMATOGENESIS; SPERMATOZOON ABNORMALITY; SPERMATOZOON MATURATION; SPONTANEOUS ABORTION; TESTOSTERONE RELEASE; TOXICOKINETICS;

ANIMALS; ARACHIDONIC ACIDS; EMBRYO; EMBRYO IMPLANTATION; ENDOCANNABINOIDS; FEMALE; GAMETOGENESIS; HUMANS; MARIJUANA SMOKING; POLYUNSATURATED ALKAMIDES; PREGNANCY; RECEPTOR, CANNABINOID, CB1;

EID: 34548125431     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmm018     Document Type: Review

References (175)

1. Abel EL. Marihuana and sex: A critical survey. Drug Alcohol Depend 1981;8:1-22.
2. Ambrosini A, Zolese G, Ambrosi S, Bertoli E, Mantero F, Boscano M, Balercoia G. Idiopathic infertility: Effect of palmitoylethanolamide (a homologue of anandamide) on hyperactivated sperm cell motility and Ca2 + influx. J Androl 2005;26:429-436.
3. Aug C, Hillier C, Johnston F, Cameron A, Greer I, Lumaden MA. Endothelial function is preserved in pregnant women with well-controlled type 1 diabetes. Br J Obstet Gynaecol 2002;109:699-707.
4. Ayalon D, Nir I, Cordova T, Bauminger S, Puder M, Naor Z, Kashi R, Zor U, Harell A, Linder HR. Acute effect of delta 1-tetrahydrocannabinol on the hypothalamo-pituitaty-ovarian axis in the rat. Neuroendocrinology 1977;23:31-42.
5. Bajari TM, Nimpf J, Schneider WJ. Role of leptin reproduction. Curr Opin Lipidol 2004;15:315-319.
6. Baker D, Pryce G, Davies WL, Hiley CR. In silico patent searching reveals a new cannabinoid receptor. Trends Pharm Sci 2006;27 1-4.
7. Bari M, Battista N, Fezza F, Gasperi V, Maccarrone M. New insights into endocannabinoid degradation and its therapeutic potential. Mini Rev Med Chem 2006;6:257 268.
8. Battaglia FC, Regnault TR. Placental transport and metabolism of amino acids. Placenta 2001;22:145-161.
9. Brayden JE, Quayle JM, Standen NB, Nelson MT. Role of potassium channels in the vascular response to endogenous and pharmacological dilators. Blood Vessels 1991;29:147-153.
10. Buckley NE, Hansson S, Harta G, Mezey E. Expression of the CB1 and CB2 receptor messenger RNAs during embryonic development in the rat. Neuroscieace 1998;82:1131-1149.
11. Burton GJ, Jauniaux E, Watson AL. Maternal arterial connections to the placental intervillous space during the first trimester of human pregnancy: The Boyd collection revisited. Am J Obstet Gynecol 1999;181:718-772.
12. Cartwright JE, Kenny JC, Dash PR, Crocker IP, Aplin JD, Baker PN, Whitley GS. Trophoblast invasion of spiral arteries: A novel in vitro model. Placenta 2002;23:232-235.
13. Castellucci M, Scheper M, Scheffen I. Celona A, Kaufmann P. The development of the human placental villous tree. Anat Embryol 1990;181:117-128.
14. Chataigneau T, Feletou M, Thollon C, Villeneuve N, Vilaine JP, Duhault J, Vanhoutte PM. Cannabinoid CB1 receptor and endothelium-dependent hyperpolarization in guinea-pig carotid, rat mesenteric and porcine coronary arteries. Br J Pharmacol 1998;123:968-974.
15. Chaytor AT, Martin PEM, Evans WH, Randall MD, Griffith TM. The endothelial component of cannabincid-induced relaxation in rabbit mesenteric artery depends on gap junctional communication. J Physiol 1999;520:539-550.
16. Clapp JF, Wesle M, Cooke R, Pekala R, Holstein C. The effects of marijuana smoke on gas exchange in ovine pregnancy. Alcohol Drug Res 1987;7:85-92.
17. Clarke IJ, Henry BA. Leptin and reproduction. Rev Reprod 1999;4 48-55.
18. Cleland JG, Ghosj J, Freemantle N, Kaye GC, Nasir M, Clark AL, Colletta AP. Clinical trials update and cumulative meta-analyses from the American College of Cardiology: WATCH, SCD-HeFT, DINAMIT, CASINO, INSPIRE, STRATUS-US, RIO-Lipids and cardiac resynchronisation therapy in heart failure. Eur J Heart Fail 2004;6:501-518.
19. Compton DR, Aceto MD. Lowe J, Martin BR. In vivo characterisation of a specific cannabinoid receptor antagonist (SR141716A): Inhibition of Delta9-tetrahydrocannabinol-induced responses and apparent agonist activity. J Pharmacol Exp Ther 1996;277:586-594.
20. Cravatt BF, Giang DK, Mayfield SP, Boger DL, Lerner RA, Gilula NB. Molecular characterisation of an enzyme that degrades neuromodulatory fatty-acide amides. Nature 1996;384:83-87.
21. Dalterio S, Barike A, Burstein S. Cannabinoids inhibit testosterone secretion by mouse testis in vitro. Science 1977;196 1472-1473.
22. Dennedy MC, Friel AM, Houlihan DD, Broderick VM, Smith T, Morrison JJ. Cannabinoids and the human uterus during pregnancy. Am J Obstet Gynecol 2004:190:2-9.
23. Deutsch DG, Goligorsky MS, Schmid PC, Krebsbach RJ, Schmid HH, Das SK, Devane WA, Hanus L, Breuer A, Pertwee R et al. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 1992;258:1946-1949.
24. Dewey WL. Cannabinoid pharmacology. Pharmacol Rev 1986;38 151-178.
25. Di S, Boudaba C, Popescu IR, Weng FJ, Harris C, Marcheselli VL. Bazan NG, Tasker JG. Activity-dependent release and actions of endocannabinoids in the rat hypothalamic supraoptic nucleus. J Physiol 2005;569:751-760.
26. Di Marzo V, Fontana A, Cadas H, Schinelli S, Cimino G, Schwartz JC, Piomelli D. Formation and inactivation of cannabinoid anandamide in central neurons. Nature 1994;372:686-691.
27. Di Marzo V, De Petrocellis L, Sepe N, Buono A. Biosynthesis of anandamide and related acylethanolamides in mouse J774 macrophages and N18 neuroblastoma cells. Biochem J 1996a;316:977-984.
28. Di Marzo V, De Petrocellis L, Sugiura T, Waku K. Potential biosynthetic connections between the two cannabimimetic eicosanoids, anandamide and 2-arachidonoyl-glycerol, in mouse neuroblastoma cells. Biochem Biophys Res Commun 1996b;227:281-288.
29. Di Matzo V, Bisogno T, Melck D, Ross P, Brockie H, Stevenson L, Pertwee R, De Petrocellis L. Interactions between synthetic vanilloids and the endogenous cannabinoid system. FEBS Letts 1998;436:449-454.
30. Di Matzo V, Goparju SK, Wang L, Lui J, Batkal S, Jaral Z, Fezza F, Miura GI, Palmiter RD, Sugiura T et al. Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 2001;410:822-825.
31. Di Marzo V, Ligresti A, Morera E, Nalli M, Ortar G. The anandamide membrane transporter. Structure-activity relationships of anandamide and oleoylethanolamine analogs with phenyl rings in the polar head group region. Bioorg Med Chem 2004;12:5161-5169.
32. Edwards RM, Stack EJ, Trizna W. Calcitonin gene-related peptide stimulayes adenylate cyclase and relaxes intracerebral arterioles. J Pharmacol Exp Ther 1991;257:1020-1024.
33. Fedorscak P, Dale PO, Storeng R, Ertzeid G, Bjercke S, Oldereid N, Omland AK, Abyholm T, Tanbo T. Impact of overweight and underweight on assised reproduction treatment. Hum Reprod 2004;11:2523-2528.
34. Felder CC, Joyce KE, Briley EM, Mansouri J. Mackie K, Blond O, Lai Y, Ma AL, Mitchell RL. Comparison of the pharmacology and signal transduction of the human cannabinoid CB1 and CB2 receptors. Mol Pharmacol 1995;8:443-450.
35. Felder CC, Joyce KE, Briley EM, Glass M. Mackie KP, Fahey KJ, Cullinan GJ, Hunden DC, Johnson DW, Chaney MO et al. LY320135, a novel cannabinoid CB1 receptor antagonist, unmasks coupling of the CB1 receptor to stimulation of cAMP accumulation. J Pharmacol Exp Ther 1998;284:291-297.
36. Fimiani C, Mattocks D, Cavani F, Salzet M, Deutsch DG, Pryor S, Bilfinger TV, Stefano GB. Morphine and anandamide stimulate intracellular calcium transients in human arterial endothelial cells: coupling to nitric oxide release. Cell Signal 1999;11 189-193.
37. Frank DA, Bauchner H, Parker S, Huber AM, Kyei-Aboagye K, Cabral H, Zuckerman B. Neonatal body proportionality and body composition after in utero exposure to cocaine and marijuana. J Pediatr 1990;117 622-626.
38. Fried PA, Buckingham M. Von Kulmiz P. Marijuana use during pregnancy and perineatl risk factors. Am J Obstet Gynecol 1983;146:992-994.
39. Fried PA, Watkinson B, Willan A. Marijuana use dining pregnancy and decreased length of gestation. Am J Obstet Gynecol 1984;150 23-37.
40. Fride E, Foox A, Rosenberg F. Faigenboim M, Cohen V. Barda L. Blau H, Mechoulam R. Milk intake and survival in newborn cannabinoid CB1 receptor knockout mice: Evidence for a "CB3" receptor. Eur J Pharmacol 2003;461:27-34.
41. Galiegue S, Mary S, Marchand J, Dussossoy D, Carriere D, Carayon P, Bouaboula M, Shire D, Le Fur G, Casellas P. Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur J Biochem 1995;232:54-61.
42. Gangula PRR, Wimalawansa S, Yallampalli C. Progesterone up-regulates vasodilator effects of calcitonin gene-related peptide in NG-nitro-L-arginine methyl ester-induced hypertension. Am J Obstet Gynecol 1997;176:894-900.
43. Gangula PRR, Zhao H, Supowit S, Wimalawansa S, DiPette D, Yallampalli C. Pregnancy and steroid hormones enhance the vasodilation responses to CGRP in rats. Am J Phys Heart Circ Physiol 1999;276 H284-H288.
44. Gaoui Y, Mechoulam R. Isolation, structure and partial synthesis of an active constituent of hashish. J Am Chem Soc 1964;86 1646-1647.
45. Gaoni Y, Mechoulam. R. The isolation and structure of delta-1-tetrahydrocannabinol and other neutral cannabinoids, from hashish. J Am Chem Soc 1971;93:217-224.
46. Gebremedhin D, Lange AR, Campbell WB, Hillard CJ, Harder DR. Cannabinoid CB1 receptor of cat cerebral arterial muscle functions to inhibit L-type Ca2+ channel current. Am J Physiol Heat Circ Physiol 1999;276 H2085-H2093.
47. Giang DY, Cravatt BF. Molecular characterization of human and mouse fatty acid amide hydrolases. Proc Natl Acad Sci USA 1997;94 2238-2242.
48. Gibson GT, Baghurst PA, Colley DP. Maternal alcohol, tobacco and cannabis consumption and the outcome of pregnancy. Aust NZ J Obstet Gynaecol 1983;23:15-19.
49. Goumenou AG, Matalliotakis IM, Koumantakis GE, Panidi DK. The role of leptin in fertility. Eur J Obstet Gynecol 2003;106:118-124.
50. Greenland S, Staisch KJ, Brown N, Gross SJ. The effects of marijuana use during pregnancy. I. Am J Obstet Gynecol 1982;143:408-413.
51. Guo Y, Wang H, Okamoto Y, Ueda N, Kingsley PJ, Marnett LJ, Schmid HH, Das SK, Dey SK. N-acylphosphatidylethanolamine-hydrolyzing phospholipase D is an important determinant of uterine anandamide levels dining implantation. J Biol Chem 2005;280:23429-23432.
52. Habayeb OMH, Bell SC, Konje JC. Endogenous cannabinoids: Metabolism and their role in reproduction. Life Sci 2001;70:1963-1977.
53. Habayeb OM, Taylor AH, Evans MD, Cooke MS, Taylor DJ, Bell SC, Konje JC. Plasma levels of the endocannabinoid, anandamide, in women - a potential role in pregnancy maintenance and labour? J Clin Endocrinol Metab 2004;89:5482-5487.
54. Haggarty P. Placental regulation of fatty acid delivery and its effects on fetal growth - a review. Placenta 2002;23:S28-S38.
55. Harris D, Kendall DA, Randall MD. Characterisation of cannabinoid receptors coupled to vasorelaxation by endothelium-derived hyperpolarising factor. N-S Arch Pharmacol 1999;359:48-52.
56. Harris D, McCulloch AI, Kendall DA, Randall MD. Characterisation of vasorelaxant responses to anandamide in the rat mesenteric arterial bed. J Physiol 2002;539:893-902.
57. Helliwell RJ, Chamley LW, Blake-Palmer K, Mitchell MD. Wu J, Kearn CS, Glass M. Characterization of the endocannabinoid system in early human pregnancy. J Clin Endocrinol Metab 2004;89:5168-5174.
58. Hillard CJ. Endocannabinoids and vascular function. J Pharmacol Exp Ther 2000;294:27-32.
59. Ho WS, Hiley CR. Endothelium-independent relaxation to cannabinoids in rat-isolated mesenteric artery and role of Ca2+ influx. Br J Pharmacol 2003a;139:585-597.
60. Ho WS. Hiley CR. Vasodilator actions of abnormal cannabidiol in rat isolated small mesenteric artery. Br J Pharmacol 2003b;138 1320-1332.
61. Hollander P. Endocannabinoid blockade for improving glycemic control and lipids in patients with Type 2 diabetes mellitus. Am J Med 2007; 120:S18-S28.
62. Huffman JW, Yu S, Showalter VM, Abood ME, Wiley JL, Compton DR, Martin BR, Bramblett RD, Reggio PH. Synthesis and pharmacology of a very potent cannabinoid lacking a phenolic hydroxyl with high affinity for the CB2 receptor, J Med Chem 1996;39:3875-3877.
63. Hutchings DE, Martin BR, Gamagaris Z, Miller N, Fico T. Plasma concentrations of delta-9-tetrahydrocannabinol in dams and fetuses following acute or multiple prenatal dosing in rats. Life Sci 1989;44:697-701.
64. Illsley NP. Glucose transporters in the human placenta. Placenta 2002;21:14-22.
65. Jaffe RB. Fetoplacental endocrine and metabolic physiology. Clin Perinatol 1983;10:669-693.
66. Jarai Z, Wagner JA. Varga K. Lake KD, Compton DR, Martin BR, Zimmer AM, Bonnet TI, Buckley NE, Mezey E et al. Cannabinoid-induced mesenteric vasodilation through an endothehal site distinct from CB1 or CB2 receptors. Proc Natl Acad Sci USA 1999;96:14136-14141.
67. Jung KM, Mangieri R, Stapleton C, Kim J, Fegley D, Wallace M, Mackie K, Piomelli D. Stimulation of endocannabinoid formation in brain slice cultures through activation of group I metabotropic glutamate receptors. Mol Pharmacol 2005;68:1196-1202.
68. Kayisli UA. Demir R, Erguler G. Arici A. Vasodilator-stimulated phosphoprotein expression and its cytokine-mediated regulation in vasculogenesis during human placental development. Mol Hum Reprod 2002;8:1023-1030.
69. 9-Tetrahydrocannabinol inhibits cytotrophoblast cell proliferation and modulates gene transcription. Mol Hum Reprod 2006;12:321-333.
70. Kim YM, Chaiworapongsa T, Gomez R, Bujold E, Yoon BH, Rotmensch S, Thaler HT, Romero R. Failure of physiologic transformation of the spiral arteries in the placental bed in preterm premature rupture of membranes. Am J Obstet Gynecol 2002;187:1137-1142.
71. Kishimoto Y, Kano M. Endogenous cannabinoid signaling through the CB1 receptor is essential for cerebellum-dependent discrete motor learning. J Neuroscience 2006;26:8829-8837.
72. Kolodny RC, Masters WH, Kolodner RM, Toro G. Depression of plasma testosterone levels after chronic intensive marijuana use. N Engl J Med 1974;290:872-874.
73. Lewysohn O, Cordova T, Nimrod A, Ayalon D. The suppressive effect of delta 1-tetrahydrocannabinol on the steroidogenic activity of rat granulosa cells in culture. Horm Res 1984;19:43-51.
74. Linne Y. Effects of obesity on women's reproduction and complications during pregnancy. Obes Rev 2004;5:137-143.
75. Liu J, Wang L, Harvey-White J, Osei-Hyiaman D. Razdan R, Gong Q, Chan AC, Zhou Z, Huang BY, Kim H-Y et al. A biosynthetic pathway for anandamide. Proc Natl Acad Sci USA 2006;103:13345-13350.
76. Lockitch G. Clinical biochemistry of pregnancy. Crit Rev Clin Lab Sci 1997;34:67-139.
77. Lockwood CJ. Prediction of pregnancy loss. Lancet 2000;355 1292-1293.
78. Maccarrone M, Bari M, Lorenzon T, Bisogno T, Di Matzo V, Finazzi-Agro A. Anandamide uptake by human endothelial cells and its regulation by nitric oxide. J Biol Chem 2000a;275:13484-13492.
79. Maccarrone M, Finazzi-Agro A. The endocannabinoid system, anandamide and the regulation of mammalian cell apoptosis. Cell Death Differ 2003;10:946-955.
80. Maccarrone M, Finazzi-Agro A. Anandamide hydrolase: A guardian angel of human reproduction? Trends Pharmacol Sci 2004;25:353-357.
81. Maccarrone M, Do Felici M, Bari M, Klinger FG, Siracusa G, Finazzi-Agro A. Down-regulation of anandamide hydrolase in mouse uterus by sex hormones. Eur J Biochem 2000b;267:2991-2997.
82. Maccarrone M, Lorenzon T, Bari M, Melino G, Finazzi-Agro A. Anandamide induces apoptosis in human cells via vanilloid receptors. Evidence for a protective role of cannabinoid receptors. J Biol Chem 2000c;275 31938-31945.
83. Maccarrone M, Valensise H, Bari M, Lazzarin N, Romanini C, Finazzi-Agro A. Relation between decreased anandamide hydrolase concentrations in human-lymphocytes and miscarriage. Lancer 2000d;355 1326-1329.
84. Maccarrone M, Valensise H, Bari M, Lazzarin N, Romanini C, Finnazzi-Agro A. Progesterone up-regulates, anandamide hydrolase in human lymphocytes: role of cytokines and implications for fertility. J Immunol 2001;166:7183-7189.
85. Maccarrone M, Bari M, Battista N, Finazzi-Agro A. Estrogen stimulates arachidonoylethanolamide release from human endothelial cells and platelet activation. Blood 2002a;100:4040-4048.
86. Maccarrone M, Bisogno T, Valensise H, Lazzarin N, Fezza F, Manna C, Di Marzo V, Finazzi-Agro A. Low fatty acid amide hydrolase and high anandamide levels are associated with failure to achieve an ongoing pregnancy after IVF and embryo transfer. Mol Hum Reprod 2002b;8 188-195.
87. Maccarrone M, Falciglia K, Di Rienzo M, Finazzi-Agro A. Eadocannabinoids, hormone-cytokine networks and human fertility. Prostaglandins Leukot. Essent. Fatty Acids. 2002c;66:309-317.
88. Maccarrone M, Bari M, Di Rienzo M, Finazzi-Agro A, Rossi A. Progesterone activates fatty acid amide hydrolase (FAAH) promoter in human T lymphocytes through the transcription factor Ikaros. Evidence for a synergistic effect of leptin. J Biol Chem 2003a;278 32726-32732.
89. Maccarrone M, Di Rienzo M, Finazzi-Agro A, Rossi A. Leptin activates the anandamide hydrolase promoter in human T lymphocytes through STAT3. J Biol Chem 2003b;278:13318-13324.
90. Maccarrone M, Cecconi S, Rossi G, Battista N, Pauselli R, Finazzi-Agro A. Anandamide activity and degradation are regulated by early postnatal aging and follicle-stimulating hormone in mouse Sertoli cells. Endocrinology 2003c;144:20-28.
91. Maccarone M, Barboni B, Paradisi A, Bernabo N, Gasperi V, Pistilli MG, Fezza F, Lucidi P, Mattioli M. Characterization of the endocannabinoid system in boar spermatozoa and implications for sperm capacitation and acrosome reaction. J Cell Sci 2005;118:4393-4404.
92. Martin BR, Compton DR, Thomas BF, Prescott WR, Little PJ, Razdan RK, Johnson MR, Melvin LS, Mechoulam R, Ward SJ. Behavioral, biochemical, and molecular modeling evaluations of cannabinoid analogs. Pharmacol Biochem Behav 1991;40:471-478.
93. 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.
94. McCulloch AI, Randall MD. Sex differences in the relative contributions of nitric oxide and EDHF to agonist-stimulated endothelium-dependent relaxations in the rat isolated mesenteric arterial bed. Br J Pharmacol 1998;123:1700-1706.
95. McMaster MT, Zhou Y, Fisher SJ. Abnormal placentation and the syndrome of pre-eclampsia. Semin Nephrol 2004;24:540-547.
96. Mechoulam R, Hanus L. A historical overview of chemical research on cannabinoids. Chem Phys Lipids 2000;108: 1-13.
97. Mechoulam R, Fride E. A hunger for cannabinoids. Nature. 2001; 410:783-785.
98. Messinis IE, Milingos SD. Leptin in human reproduction. Hum Reprod Update 1999;5:52-63.
99. Moore C, Negrusz A, Lewis D. Determination of drugs of abuse in meconium. J Chromatogr B 1998;713:137-146.
100. Moore SA, Nomikos GG, Dickason-Chesterfield AK, Schober DA, Schans JM, Ying BP, Xu YC, Phebus L, Simmons RM, Li D et al. Identification of a high-affinity binding site involved in the transport of endocannabinoids. Proc Natl Acad Sci USA 2005;102 17852-17857.
101. Mueller BA, Daling JR, Weiss N S, Moore DE. Recreational drug use and the risk of primary infertility. Epidemiology 1990;1:195-200.
102. Mukhopadhyay S, Chapnick BM, Howlett AC. Anandamide-induced vasorelaxation in rabbit aortic rings has two components: G protein dependent and independent. Am J Phys Heart Circ Physiol 2002; 282:H2046-H2054.
103. Munro S, Thomas KL, Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993;365:61-65.
104. Murphy LL, Gher J, Steger RW, Bartke A. Effects of Δ9-tetrahydrocannabinol on copulatory behaviour and neuroendocrine responses of male rats to female rat conspecifics. Pharmacol Biochem Behav 1994;48:1011-1017.
105. Nahas GG, Frick HC, Lattimer JK, Latour C. Harvey D. Pharmacokinetics of THC in brain and testis, male gametotoxicity and premature apoptosis of spermatozoa. Hum Psychopharmacol 2002;17:103-113.
106. Nir I, Ayalon D, Tsafriri A, Cordova T, Lindner HR. Suppression of the cyclic surge of LH and of ovulation in the rat by Delta 1-tetrahydrocannabinol. Nature 1973:234:470-471.
107. Nygren KG, Andersen AN. Assisted reproductive technology in Europe, 1998. Results generated from European registers by ESHRE. Hum Reprod 2001;16:2459-2471.
108. Pardi GAM, Marconi AM, Cetin I. Pathophysiology of intrauterine growth retardation: Role of the placenta, Acta Paediatr Suppl 1997; 423:170-172.
109. Paria BC, Dey SK. Ligand-receptor signalling with endocannabinoids in preimplantation embryo development and implantation. Chem Phys Lipids 2000;108:211-220.
110. Paris BC, Das. SK, Dey SK. The preimplantation mouse embryo is a target for endocannabinoid ligand-receptor signalling. Proc Natl Acad Sci USA 1995;92:9460-9464.
111. 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 mouse uterus during the preimplantation period. Mol Reprod Dev 1996;45:183-192.
112. Paria BC, Ma W, Andrenyak DM, Schmid PC, Schmid HH, Moody DE, Deng H, Makriyannis A, Dey SK. Effects of cannabinoids on preimplantation mouse embryo development and implantation are mediated by brain-type cannabinoid receptors. Biol Reprod 1998;58:1490-1495.
113. Paria BC, Zhao X, Wang J, Das SK, Dey SK. Fatty acid amide hydrolase is expressed in the mouse uterus and embryo during the periimplantation period. Biol Reprod 1999,60:1151-1157.
114. Paria BC, Song H, Wang X, Schmid PC, Krebsbach RJ, Schmid HH, Bonner TJ, Zimmer A, Dey SK. Dysregulated cannabinoid sgnaling disrupts uterine receptivity for embryo implantation. J Biol Chem 2001;276 20523-20528.
115. Paria BC, Wang H, Dey SK. Endocannabinoid signalling in synchronizing embryo development and uterine receptivity for implantation. Chem Phys Lipids 2002;121:201-210.
116. Park B, Gibbons HM, Mitchell MD, Glass M. Identification of the CB1 cannabinoid receptor and fatty acid amide hydmlase (FAAH) in the human placenta. Placenta 2003;24:473-470
117. Patra PB, Wadworth RM. Effect of synthetic cannabinoid nabalone on spermatogenesis in mice. Experimentia 1990;46:852-854.
118. Pertwee R. Pharmacology of cannabinoid CB1 and CB2 receptors. Pharmacol Ther 1997;74:129-180.
119. Piomelli D, Giuffrida A, Calignano A, Rodriguez de Fonseca F. The endocannabinoid system as a target for therapeutic drugs. Trends Pharmacol Sci 2000;21:218-224.
120. Plane F, Holland M, Waldron GJ, Garland CJ, Boyle JP. Evidence that anandamide and EDHF act via different mechanisms in rat isolated mesenteric arteries. Br J Pharmacol 1997;121:1509-1511.
121. Powell DJ, Fuller RW. Marijuana and sex: Strange bedpartners. J Psychoactive Drugs 1983;15:269-280.
122. Pratt PF, Hillard CJ, Edgemond WS, Campbell WB. N-arachidonylethamiamide relaxation of bovine coronary artery is not mediated by CB1 cannabinoid receptor. Am J Phys 1999;274:H375-H381.
123. Rajashekhar G, Loganath A, Roy AC, Chong SS, Wong YC. Hypoxia up-regulated angiogenin and down-regulated vascular cell adhesion molecule-1 expression and semdon in human placental trophoblasts. J Soc Gynecol Invest 2005;12:310-319.
124. Randall MD, Kendall DA. Anandamide and endothelium-drived hyperpolarising factor act via a common vasorelaxant mechanism in rat mesentery. Eur J Pharmacol 1998;346:51-53.
125. Randall MD, Alexander SP, Bennet T, Boyd EA, Fry JR, Gardiner SM, Kemp PA, McCulloch AI, Kendall DA. An endogenous cannabinoid as an endothelium-derived vasorelaxant. Biochem Biophys Res Comm 1996; 229:114-120.
126. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science 2005;308:1592-1594.
127. Reich R, Laufer N, Lewysohn O, Cordova T, Ayalon D, Tsafriri A. In vitro effects of cannabinoids on follicular function in the rat. Biol Reprod 1982;27:223-231.
128. Ross R. Anandamide and vanilloid TRPV1 receptors. Br J Pharmacol 2003;140:790-801.
129. Rossato M, Ion Popa F, Ferigo M, Clarim G, Foresta C. Human sperm express cannabinoid receptor CB1, the activation of which inhibits motility, acrosome reaction, and mitochondrial function. J Clin Endocrinol Metab 2005;90:984-991.
130. Salafia CM. Placental pathology, of fetal growth restriction. Clin Obstet Gynecol 1997;40:740-749.
131. 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 USA 1997;94:4188-4192.
132. Schuel HL, Burkman LJ, A tale of two cells: Endocannabinoid-signaling, regulates functions of neurons and sperm. Biol Reprod 2005;73 1078-1086.
133. Schuel H, Burkman LJ, Lippes J, Crickard K, Forester E, Piomelli D, Giuffrida A. N-Acylethanolamines in human reproductive fluids: Chem Phys Lipids 2002a;121:211-227.
134. Schuel H, Burkman LJ, Lippes J, Crickard K, Mahony MC, Giuffrida A, Picone RP, Makriyannis A. Evidence that anandamide signaling regulates human sperm functions required for fertilazation. Mol Reprod Dev 2002b;63:376-387.
135. Sharov AA, Piao Y, Matoba R, Dudekula DB, Qian Y, Van Buren V, Falco G, Martin PR, Stagg CA, Bassey UC et al. Transcriptome analysis of mouse stem cells and early embryos. PLoS Biol 2003;1:E74.
136. Shire D, Carillon C, Kaghad M, Calandra B, Rinaldi-Carmona M, Le Fur G, Caput D, Ferrara P. An amino-terminal variant of the central cannabinoid receptor resulting from alternative splicing. J Biol Chem 1995; 270:3726-3731.
137. Showalter VM, Compton DR, Martin BR, Bood ME. Evaluation of binding in a transfected cell line expressing a peripheral cannabinoid receptor (CB2): Identification of cannabinoid receptor subtype selective ligands. J Pharmacol 1996;278:989-999.
138. Sidney S. Cardiovascular consequences of marijuana use. J Clin Pharmacol 2002;42:64S-70S.
139. Simon GM, Cravatt BF. Endocannabinoid biosynthesis proceeding through glycerophospho-N-acyl ethanolamine and a role for α/β-hydrolase 4 in this pathway. J Biol Chem 2006;281:26465-26472.
140. Sladek SM, Magness RR, Conrad KP. Nitric oxide and pregnancy. Am J Phys 1997;272:R441-R463.
141. Straiker AJ, Maguire G, Mackie K, Lindsey J. Localisation of cannabinoid CB1 receptors in the human anterior eye and retina. Invest Ophthalmol Vis Sci 1999;40:2442-2448.
142. Straszewski-Cavez SL, Abrahams VM, Mor G. The role of apoptosis in the regulation of trophoblast survival and differentiation during pregnancy. Endocr Rev 2005;26:877-897.
143. Suarez SS, Ho HC. Hyperactivated motility in sperm. Reprod Domest Anim 2003;38:119-124.
144. Takagi Y, Nikaido T, Toki T, Kita N, Kanai M, Ashida T, Ohira S, Konishi I. Levels of oxidative stress and redox-related molecules in the placenta in preeclampsia and fetal growth restriction.Vir Arch 2004;444:49-55.
145. Taylor AH, Abbas MS, Bell SC, Konje JC. The inhibitory effect of Δ9-tetrahydrocannabinol on trophoblast cell proliferation and transcription is mediated via the CB-2 receptor. Br J Obstet Gynecol 2007.
146. Thadani PV, Strauss JF, III, Dey SK, Anderson VM, Audus KL, Coats KS, Cross JC, Erlebacher A, Ganapathy V, Linzer DI. National Institute on Drug Abuse Conference report on placental proteins, drug transport, and fetal development. Amer J Obstet Gynecol 2004;191:1858-1862.
147. Thaete LG, Dewey ER, Neerhof MG. Endothelin and the regulation of uterine and placental perfusion in hypoxia-induced fetal growth restriction. J Soc Gynecol Invest 2004;11:16-21.
148. Treinen KA, Sneeden JL, Heindel JJ. Specific inhibition of FSH-stimulated cAMP accumulation by delta 9-tetrahydrocannabinol in cultured rat granulosa cells. Toxicol Appl Pharmacol 1993;118 53-57.
149. Van Der Stelt M, Di Marzo V, Endovanilloids. Putative endogenous ligands of transient receptor potential vanilloid 1 channels. Eur J Biochem 2004;271:1827-1834.
150. Van Gaal LF, Rissanen A, Scheen A, Ziegler AM, Rossner S. Effect of rimonabant on weight reduction and cardiovascular risk. Lancet 2005;366:369-370.
151. Van Oosten BW, Killestein J, Mathus-Vliegen EMH, Polman CH. Multiple sclerosis following treatment with a cannabinoid receptor-1 antagonist. Mult Scler 2004;10:330-331.
152. Vardaris RM, Weisz DJ, Fazel A, Rawitch AB. Chronic administration of delta-9-tetrahydrocannabinol to pregnant rats: Studies of pup behavior and placental transfer. Pharmarol Biochem Behav 1976;4 249-254.
153. Varga K, Lake KD, Kunos G. Novel antagonist implicates the CB1 cannabinoid receptor in the hypotensive action of anandamide. Eur J Pharmacol 1995;278:279-283.
154. Vogeser M, Hauer D, Christina Azad S, Huber E, Storr M, Schelling G. Release of anandamide from blood cells. Clin Chem Lab Med 2006; 44:488-491.
155. Vuorela P, Hatva E, Lymboussaki A, Kaipainen A, Joukov V, Persico MG, Alitalo K, Halmesmaki E. Expression of vascular endothelial growth factor and placenta growth factor in human placenta. Biol Reprod 1997;56:489-494.
156. Wagner JA, Varga K, Jarai Z, Kunos G. Mesenteric vasodilation mediated by endothelial anandamide receptors. Hypertension 1999;33 429-434.
157. Walter I, Schonkypl. S. Extracellular matrix components and matrix degrading enzymes in the feline placenta during gestation. Placenta 2006;27: 291-306.
158. Wang J, Paria BC, Dey SK, Armant DR. Stage-specific excitation of cannabinoid receptor exhibits differential effects on mouse embryonic development. Biol Reprod 1999;60:839-844.
159. Wang H, Matsumoto H, Guo Y, Paria BC, Roberts RL. Dey SK. Differential G protein-coupled cannabinoid receptor signaling by anandamide directs balstocyst activation for implantation. Proc Natl Acad Sci 2003; 100:14914-14919.
160. Wang H, Guo Y, Wang D, Kingsley PJ, Marnett L, Das SK, DuBois RN, Dey SK. Aberrant cannabinoid signaling impairs oviductal transport of embryos. Nat Med 2004;10:1074-1080.
161. Wang H, Dey SK, Maccarrone M. Jekyll and Hyde: Two faces of cannabinoid signaling in male and female fertility. Endocr Rev 2006a27 427-448.
162. Wang J, Okamoto Y, Morishita J, Tsuboi K, Miyatake A, Ueda N. Functional analysis of the purified anandamide-generating phospholipase D as a member of the metallo-β-lactamase family. J Biol Chem 2006b; 281: 12353-12335.
163. Wei BQ, Mikkelsen TS, McKinney MK, Lander ES, Cravatt BF. A second fatty acid amide hydrolase with variable distribution among placental mammals. J Biol Chem 2006;281:36569-36578.
164. Wenger T, Ledent C, Csernus V, Gerendai I. The central cannabinoid receptor inactivation suppresses endocrine reproductive function. Biochem Biophys Res Commun 2001;284:363-368.
165. White R, Hiley CR. A comparison of EDHF-mediated and anandamide-induced relaxations in the rat isolated mesenteric artery. Br J Pharmacol 1997;122:1573-1584.
166. Woods JR, Jr. Adverse consequences of prenatal illicit drug exposure. Curr Opin Obstet Gynecol 1996;8:403-411.
167. Wray S, Jones K, Kupittayanant S, Li Y, Matthew A, Monir-Bishty E, Noble K, Pierce SJ, Quenby S, Shmygol AV. Calcium signaling and uterine contractility. J Soc Gynecol Invest 2003;10:252-264.
168. Yamaji K, Sarker KP, Kawahara K, Iino S, Yamakuchi M, Abeyama K, Hashiguchi T, Maruyama I. Anandamide induces apoptosis in human endothelial cells: Its regulation system and clinical implications. Thromb Haemost 2003;89:875-884.
169. Yang ZM, Paria BC, Dey SK. Activation of brain-type cannabinoid receptors interferes with preimplantation mouse embryo development. Biol Reprod 1996;55:756-761.
170. Zimmerman AM, Bruce WR, Zimmerman S. Effects of cannabinoids on sperm morphology. Pharmacology 1979;18:143-148.
171. Zuckerman B, Frank DA, Hingson R, Amaro H, Levenson SM, Kayne H, Parker S, Vinci R, Aboagye K, Fried LE et al. Effects of maternal marijuana and cocaine use on fetal growth. New Engl J Med 1989; 320:762-768.
172. Zygmunt PM, Hogestatt ED, Waldeck K, Edwards G, Kirkup AJ, Weston AH. Studies on the effects of anandamide in rat hepatic artery, Br J Pharmacol 1997;122:1679-1686.
173. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, Julius D, Hogestatt ED. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 1999;400 452-457.
174. Zygmunt PM, Hogestatt ED, Julius D, Di Marzo V. Anandamide - the other side of the coin. Trends Pharmacol Sci 2000;21:43-44.
175. Zygmunt PM, Andersson DA, Hogestatt ED. Delta -9-tetrahydrocannabinol and cannabinol activate capsaicin-sensitive sensory nerves via a CB1 and CB2 cannabinoid receptor-independent mechanism. J Neurosci 2002; 22:4720-4727.