Placenta
Volume 30, Issue 6 , Pages 516-522 , June 2009

Endocannabinoid System in First Trimester Placenta: Low FAAH and High CB1 Expression Characterize Spontaneous Miscarriage

  • E. Trabucco

      Affiliations

    • Dipartimento di Scienze Ginecologiche, Ostetriche e della Riproduzione, II Università degli Studi di Napoli, Largo Madonna delle Grazie 1, 80138 Naples, Italy
    • These authors contributed equally to the work.
  • ,
  • G. Acone

      Affiliations

    • Dipartimento di Scienze Ginecologiche, Ostetriche e della Riproduzione, II Università degli Studi di Napoli, Largo Madonna delle Grazie 1, 80138 Naples, Italy
    • These authors contributed equally to the work.
  • ,
  • A. Marenna

      Affiliations

    • Dipartimento di Scienze Ginecologiche, Ostetriche e della Riproduzione, II Università degli Studi di Napoli, Largo Madonna delle Grazie 1, 80138 Naples, Italy
  • ,
  • R. Pierantoni

      Affiliations

    • Dipartimento di Medicina Sperimentale, Sez. “F. Bottazzi”, II Università degli Studi di Napoli, Via Costantinopoli 16, 80138 Napoli, Italy
    • Corresponding Author InformationCorresponding author. Tel.: +39 081 566 7617; fax: +39 081 566 7617.
  • ,
  • G. Cacciola

      Affiliations

    • Dipartimento di Medicina Sperimentale, Sez. “F. Bottazzi”, II Università degli Studi di Napoli, Via Costantinopoli 16, 80138 Napoli, Italy
  • ,
  • T. Chioccarelli

      Affiliations

    • Dipartimento di Medicina Sperimentale, Sez. “F. Bottazzi”, II Università degli Studi di Napoli, Via Costantinopoli 16, 80138 Napoli, Italy
  • ,
  • K. Mackie

      Affiliations

    • Department of Psychological and Brain Sciences and the Gill Center, Indiana University, Bloomington, IN 47401, USA
  • ,
  • S. Fasano

      Affiliations

    • Dipartimento di Medicina Sperimentale, Sez. “F. Bottazzi”, II Università degli Studi di Napoli, Via Costantinopoli 16, 80138 Napoli, Italy
  • ,
  • N. Colacurci

      Affiliations

    • Dipartimento di Scienze Ginecologiche, Ostetriche e della Riproduzione, II Università degli Studi di Napoli, Largo Madonna delle Grazie 1, 80138 Naples, Italy
  • ,
  • R. Meccariello

      Affiliations

    • Dipartimento di Studi Delle Istituzioni Dei Sistemi Territoriali, Università “Parthenope” di Napoli, Via Medina 40, 80133 Napoli, Italy
  • ,
  • G. Cobellis

      Affiliations

    • Dipartimento di Medicina Sperimentale, Sez. “F. Bottazzi”, II Università degli Studi di Napoli, Via Costantinopoli 16, 80138 Napoli, Italy
    • These authors contributed equally to the coordination of the research.
  • ,
  • L. Cobellis

      Affiliations

    • Dipartimento di Scienze Ginecologiche, Ostetriche e della Riproduzione, II Università degli Studi di Napoli, Largo Madonna delle Grazie 1, 80138 Naples, Italy
    • These authors contributed equally to the coordination of the research.

,Accepted 30 March 2009.

References 

  1. Di Marzo V. Endocannabinoids and other fatty acid derivatives with cannabimimetic properties: biochemistry and possible physiopathological relevance. Biochim Biophys Acta. 1998;1392:153–175
  2. Okamoto Y, Morishita J, Tsuboi K, Tonai T, Ueda N. Molecular characterization of a phospholipase D generating anandamide and its congeners. J Biol Chem. 2004;279:5298–5305
  3. Schmid HH. Pathways and mechanisms of N-acylethanolamine biosynthesis: can anandamide be generated selectively?. Chem Phys Lipids. 2000;108:71–87
  4. Taylor AH, Ang C, Bell SC, Konje JC. The role of the endocannabinoid system in gametogenesis, implantation and early pregnancy. Hum Reprod Update. 2007;13:501–513
  5. 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
  6. Cacciola G, Chioccarelli T, Ricci G, Meccariello R, Fasano S, Pierantoni R, et al. The endocannabinoid system in vertebrate male reproduction: a comparative overview. Mol Cell Endocrinol. 2008;286:S24–S30
  7. Schuel H, Burkman LJ. A tale of two cells: endocannabinoid-signaling regulates functions of neurons and sperm. Biol Reprod. 2005;73:1078–1086
  8. Chianese R, Cobellis G, Pierantoni R, Fasano S, Meccariello R. Non-mammalian vertebrate models and the endocannabinoid system: relationships with gonadotropin-releasing hormone. Mol Cell Endocrinol. 2008;286:S46–S51
  9. Zuckerman B, Frank DA, Hingson R, Amaro H, Levenson SM, Kayne H, et al. Effects of maternal marijuana and cocaine use on fetal growth. N Engl J Med. 1989;320:762–768
  10. McCance-Katz EF. The consequences of maternal substance abuse for the child exposed in utero. Psychosomatics. 1991;32:268–274
  11. Horne AW, Phillips JA, Kane N, Lourenco PC, McDonald SE, Williams AR, et al. CB1 expression is attenuated in Fallopian tube and decidua of women with ectopic pregnancy. PLoS ONE. 2008;3(12):e3969
  12. Wang H, Dey SK, Maccarrone M. Jekyll and Hyde: two faces of cannabinoid signaling in male and female fertility. Endocr Rev. 2006;27:427–448
  13. Habayeb OM, Bell SC, Konje JC. Endogenous cannabinoids: metabolism and their role in reproduction. Life Sci. 2002;70:1963–1977
  14. Wang H, Guo Y, Wang D, Kingsley PJ, Marnett LJ, Das SK, et al. Aberrant cannabinoid signaling impairs oviductal transport of embryos. Nat Med. 2004;10:1074–1080
  15. Liu WM, Duan EK, Cao YJ. Effects of anandamide on embryo implantation in the mouse. Life Sci. 2002;71:1623–1632
  16. 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
  17. 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 periimplantation period. Mol Reprod Dev. 1996;45:183–192
  18. Paria BC, Ma W, Andrenyak DM, Schmid PC, Schmid HH, Moody DE, et al. Effects of cannabinoids on preimplantation mouse embryo development and implantation are mediated by brain-type cannabinoid receptors. Biol Reprod. 1998;58:1490–1495
  19. Paria BC, Dey SK. Ligand-receptor signaling with endocannabinoids in preimplantation embryo development and implantation. Chem Phys Lipids. 2000;108:211–220
  20. 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 USA. 2003;100:14914–14919
  21. Habayeb OM, Taylor AH, Bell SC, Taylor DJ, Konje JC. Expression of the endocannabinoid system in human first trimester placenta and its role in trophoblast proliferation. Endocrinology. 2008;149:5052–5060
  22. Habayeb OM, Taylor AH, Evans MD, Cooke MS, Taylor DJ, Bell SC, et al. Plasma levels of the endocannabinoid in women – a potential role in pregnancy maintenance and labor?. J Clin Endocrinol Metab. 2004;89:5482–5487
  23. Maccarrone M, Valensise H, Bari M, Lazzarin N, Romanini C, Finazzi-Agrò A. Relation between decreased anandamide hydrolase concentrations in human lymphocytes and miscarriage. Lancet. 2000;355:1326–1329
  24. Maccarrone M, Bisogno T, Valensise H, Lazzarin N, Fezza F, Manna C, et al. 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. 2002;8:188–195
  25. Habayeb OM, Taylor AH, Finney M, Evans MD, Konje JC. Plasma anandamide concentration and pregnancy outcome in women with threatened miscarriage. JAMA. 2008;299:1135–1136
  26. Helliwell RJ, Chamley LW, Blake-Palmer K, Mitchell MD, Wu J, Kearn CS, et al. Characterization of the endocannabinoid system in early human pregnancy. J Clin Endocrinol Metab. 2004;89:5168–5174
  27. Acone G, Trabucco E, Cacciola G, Chioccarelli T, Colacurci N, Cobellis L, et al. Low type I cannabinoid receptor levels characterize placental villous in labouring delivery. Placenta. 2009;30:203–215
  28. Griebel CP, Halvorsen J, Golemon TB, Day AA. Management of spontaneous abortion. Am Fam Physician. 2005;72:1243–1250
  29. Sugiura T, Yoshinaga N, Waku K. Rapid generation of 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand, in rat brain after decapitation. Neurosci Lett. 2001;297:175–178
  30. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987;162:156–159
  31. Lowry WS, Farmer FT. A combined temperature and pressure correction meter. Br J Radiol. 1955;28:516
  32. Twitchell W, Brown S, Mackie K. Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J Neurophysiol. 1997;78:43–50
  33. Tsou K, Brown S, Sañudo-Peña MC, Mackie K, Walker JM. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience. 1998;83:393–411
  34. Salio C, Fischer J, Franzoni MF, Conrath M. Pre- and postsynaptic localizations of the CB1 cannabinoid receptor in the dorsal horn of the rat spinal cord. Neuroscience. 2002;110:755–764
  35. Chamley LW, Bhalla A, Stone PR, Liddell H, O'Carroll S, Kearn C, et al. Nuclear localisation of the endocannabinoid metabolizing enzyme fatty acid amide hydrolase (FAAH) in invasive trophoblasts and an association with recurrent miscarriage. Placenta. 2008;29:970–975
  36. ESHRE Capri Workshop Group . Genetic aspects of female reproduction. Hum Reprod Update. 2008;14:293–307
  37. Jauniaux E, Watson A, Burton G. Evaluation of respiratory gases and acid-base gradients in human fetal fluids and uteroplacental tissue between 7 and 16weeks gestation. Am J Obstet Gynecol. 2001;184:998–1003
  38. 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;181:718–724
  39. 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
  40. Harkany T, Keimpema E, Barabás K, Mulder J. Endocannabinoid functions controlling neuronal specification during brain development. Mol Cell Endocrinol. 2008;286:S84–S90
  41. Watson S, Chambers D, Hobbs C, Doherty P, Graham A. The endocannabinoid receptor, CB1, is required for normal axonal growth and fasciculation. Mol Cell Neurosci. 2008;38:89–97
  42. Glass M, Dragunow M, Faull RL. Cannabinoid receptors in the human brain: a detailed anatomical and quantitative autoradiographic study in the fetal, neonatal and adult human brain. Neuroscience. 1997;77:299–318
  43. Buckley NE, Hansson S, Harta G, Mezey E. Expression of the CB1 and CB2 receptor messenger RNAs during embryonic development in the rat. Neuroscience. 1998;82:1131–1149
  44. Schuel H, Burkman LJ, Lippes J, Crickard K, Forester E, Piomelli D, et al. N-Acylethanolamines in human reproductive fluids. Chem Phys Lipids. 2002;121:211–227
  45. 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. J Biol Chem. 2003;278:32726–32732
  46. Maccarrone M, Cecconi S, Rossi G, Battista N, Paeselli R, Finazzi-Agrò A. Anandamide activity and degradation are regulated by early postnatal aging and follicle-stimulating hormone in mouse Sertoli cells. Endocrinology. 2003;144:20–28

PII: S0143-4004(09)00110-6

doi: 10.1016/j.placenta.2009.03.015

Placenta
Volume 30, Issue 6 , Pages 516-522 , June 2009