Stage-variations of anandamide hydrolase activity in the mouse uterus during the natural oestrus cycle

  • Francesca G Klinger
  • Natalia Battista
  • Massimo De Felici
  • Mauro Maccarrone
Open Access
Hypothesis

Abstract

Recent studies have demonstrated that the endogenous cannabinoids are important modulators of fertility in mammals. In particular, a role of the endocannabinoid system in early stages of embryo development, oviductal transport of embryos, pregnancy maintenance and labour has been demonstrated in rodents and/or in humans. In the present paper, we report the analysis of FAAH activity and protein content in the mouse uterus as a function of the natural oestrus cycle stages. Variations of FAAH activity are discussed in relationship to changes in sex steroid levels and to the possible action of AEA on remodelling of uterine tissues.

Notes

Acknowledgements

This work was supported by the Italian MIUR PRIN grant 2004–2005.

References

  1. 1.
    Park B, McPartland JM, Glass M: Cannabis, cannabinoids and reproduction. Prostaglandins Leukot Essent Fatty Acids. 2004, 70: 189-97. 10.1016/j.plefa.2003.04.007.CrossRefPubMedGoogle Scholar
  2. 2.
    Maccarrone M, Finazzi-Agro A: Anandamide hydrolase: a guardian angel of human reproduction?. Trends Pharmacol Sci. 2004, 25: 353-7. 10.1016/j.tips.2004.05.002.CrossRefPubMedGoogle Scholar
  3. 3.
    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: 1074-80. 10.1038/nm1104.CrossRefPubMedGoogle Scholar
  4. 4.
    Maccarrone M, De Felici M, Bari M, Klinger F, Siracusa G, Finazzi-Agro A: Down-regulation of anandamide hydrolase in mouse uterus by sex hormones. Eur J Biochem. 2000, 267: 2991-7. 10.1046/j.1432-1033.2000.01316.x.CrossRefPubMedGoogle Scholar
  5. 5.
    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 labor?. J Clin Endocrinol Metab. 2004, 89: 5482-7. 10.1210/jc.2004-0681.CrossRefPubMedGoogle Scholar
  6. 6.
    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: 183-92. 10.1002/(SICI)1098-2795(199610)45:2<183::AID-MRD11>3.0.CO;2-2.CrossRefPubMedGoogle Scholar
  7. 7.
    Paria BC, Dey SK: Ligand-receptor signaling with endocannabinoids in preimplantation embryo development and implantation. Chem Phys Lipids. 2000, 108: 211-20. 10.1016/S0009-3084(00)00197-3.CrossRefPubMedGoogle Scholar
  8. 8.
    Liu WM, Duan EK, Cao YJ: Effects of anandamide on embryo implantation in the mouse. Life Sci. 2002, 23: 1623-32. 10.1016/S0024-3205(02)01928-8.CrossRefGoogle Scholar
  9. 9.
    Paria BC, Wang H, Dey SK: Endocannabinoid signaling in synchronizing embryo development and uterine receptivity for implantation. Chem Phys Lipids. 2002, 121: 201-10. 10.1016/S0009-3084(02)00156-1.CrossRefPubMedGoogle Scholar
  10. 10.
    Xiao AZ, Zhao YG, Duan EK: Expression and regulation of the fatty acid amide hydrolase gene in the rat uterus during the estrous cycle and peri-implantation period. Mol Hum Reprod. 2002, 8: 651-8. 10.1093/molehr/8.7.651.CrossRefPubMedGoogle Scholar
  11. 11.
    Maccarrone M, Fride E, Bisogno T, Bari M, Cascio MG, Battista N, Finazzi Agro A, Suris R, Mechoulam R, Di Marzo V: Up-regulation of the endocannabinoid system in the uterus of leptin knockout (ob/ob) mice and implications for fertility. Mol Hum Reprod. 2005, 11: 21-8. 10.1093/molehr/gah130.CrossRefPubMedGoogle Scholar
  12. 12.
    Bronson FH: Male-induced precocial puberty in female mice: confirmation of the role of estrogen. Endocrinology. 1975, 96: 511-4.CrossRefGoogle Scholar
  13. 13.
    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. 2003, 144: 20-8. 10.1210/en.2002-220544.CrossRefPubMedGoogle Scholar
  14. 14.
    Gubellini P, Picconi B, Bari M, Battista N, Calabresi P, Centonze D, Bernardi G, Finazzi-Agro A, Maccarrone M: Experimental parkinsonism alters endocannabinoid degradation: implications for striatal glutamatergic transmission. J Neurosci. 2002, 22: 6900-7.CrossRefGoogle Scholar
  15. 15.
    Lazzarin N, Valensise H, Bari M, Ubaldi F, Battista N, Finazzi-Agro A, Maccarrone M: Fluctuations of fatty acid amide hydrolase and anandamide levels during the human ovulatory cycle. Gynecol Endocrinol. 2004, 18: 212-8. 10.1080/09513590410001692492.CrossRefPubMedGoogle Scholar
  16. 16.
    Walmer DK, Wrona MA, Hughes CL, Nelson KG: Lactoferrin expression in the mouse reproductive tract during the natural estrous cycle: correlation with circulating estradiol and progesterone. Endocrinology. 1992, 131: 1458-66. 10.1210/en.131.3.1458.CrossRefPubMedGoogle Scholar
  17. 17.
    Fata JE, Chaudhary V, Khokha R: Cellular turnover in the mammary gland is correlated with systemic levels of progesterone and not 17beta-estradiol during the estrous cycle. Biol Reprod. 2001, 65: 680-8. 10.1095/biolreprod65.3.680.CrossRefPubMedGoogle Scholar
  18. 18.
    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. 10.1016/j.ajog.2003.07.013.CrossRefPubMedGoogle Scholar
  19. 19.
    Guzman M: Cannabinoids: potential anticancer agents. Nat Rev Cancer. 2003, 3: 745-55. 10.1038/nrc1188.CrossRefPubMedGoogle Scholar
  20. 20.
    Pomelli D: The molecular logic of endocannabinoid signalling. Nat Rev Neurosci. 2003, 4: 873-84. 10.1038/nrn1247.CrossRefGoogle Scholar
  21. 21.
    Maccarrone M, Finazzi-Agro A: The endocannabinoid system, anandamide and the regulation of mammalian cell apoptosis. Cell Death Differ. 2003, 10: 946-55. 10.1038/sj.cdd.4401284.CrossRefPubMedGoogle Scholar
  22. 22.
    Di Marzo V, Bifulco M, De Petrocellis L: The endocannabinoid system and its therapeutic exploitation. Nat Rev Drug Discov. 2004, 3: 771-84. 10.1038/nrd1495.CrossRefPubMedGoogle Scholar
  23. 23.
    Huet-Hudson YM, Andrews GK, Dey SK: Cell type-specific localization of c-myc protein in the mouse uterus: modulation by steroid hormones and analysis of the periimplantation period. Endocrinology. 1989, 125: 1683-90.CrossRefGoogle Scholar
  24. 24.
    Pampfer S, Cordi S, Dutrieux C, Vanderheyden I, Marchand C, De Hertogh R: Interleukin 1beta mediates the effect of high D-glucose on the secretion of TNF-alpha by mouse uterine epithelial cells. Cytokine. 1999, 11: 500-9. 10.1006/cyto.1998.0459.CrossRefPubMedGoogle Scholar
  25. 25.
    Joswig A, Gabriel HD, Kibschull M, Winterhager E: Apoptosis in uterine epithelium and decidua in response to implantation: evidence for two different pathways. Reprod Biol Endocrinol. 2003, 26: 1-44.Google Scholar
  26. 26.
    Short RV: Role of hormones in sex cycle. Reproduction In Mammals. 1972, Cambridge University Press, 3: 42-72.Google Scholar
  27. 27.
    Sato T, Nakajima H, Fujio K, Mori Y: Enhancement of prostaglandin E2 production by epidermal growth factor requires the coordinate activation of cytosolic phospholipase A2 and cyclooxygenase 2 in human squamous carcinoma A431 cells. Prostaglandins. 1997, 53: 355-69. 10.1016/0090-6980(97)00036-1.CrossRefPubMedGoogle Scholar
  28. 28.
    Dahmoun M, Boman K, Cajander S, Westin P, Backstrom T: Apoptosis, proliferation and sex hormone receptors in superficial parts of human endometrium at the end of the secretory phase. J Clin Endocrin Metab. 2005, 84: 1737-1743. 10.1210/jc.84.5.1737.CrossRefGoogle Scholar

Copyright information

© Klinger et al; licensee BioMed Central Ltd. 2006

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Authors and Affiliations

  • Francesca G Klinger
    • 1
  • Natalia Battista
    • 2
  • Massimo De Felici
    • 1
  • Mauro Maccarrone
    • 2
    • 3
  1. 1.Department of Public Health and Cell BiologyUniversity of Rome Tor VergataRomeItaly
  2. 2.Department of Biomedical SciencesUniversity of TeramoTeramoItaly
  3. 3.IRCCS C. Mondino, Mondino-Tor Vergata Center for Experimental NeurobiologyRomeItaly

Personalised recommendations