Elevated Systemic Levels of Endocannabinoids and Related Mediators Across the Menstrual Cycle in Women with Endometriosis

Reproductive Sciences

Volumn 23, Issue 8, 2016, Pages 1071-1079

  Sanchez, Ana Maria ^a   Cioffi, Raffaella ^a   Viganò, Paola ^a   Candiani, Massimo ^a   Verde, Roberta ^b   Piscitelli, Fabiana ^b   Di Marzo, Vincenzo ^b   Garavaglia, Elisabetta ^a   Panina Bordignon, Paola ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b CNR   (Italy)

Author keywords

endocannabinoids; endometriosis; pain

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ANANDAMIDE; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; ENDOCANNABINOID; ENZYME; FATTY ACID AMIDASE; FATTY ACID AMIDE HYDROLASE 1; MESSENGER RNA; N ACYLPHOSPHATIDYLETHANOLAMINE HYDROLYZING PHOSPHOLIPASE D; N OLEOYLETHANOLAMINE; PALMIDROL; PHOSPHOLIPASE; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; ACYLGLYCEROL; AMIDASE; ARACHIDONIC ACID DERIVATIVE; CNR2 PROTEIN, HUMAN; ETHANOLAMINE DERIVATIVE; FATTY-ACID AMIDE HYDROLASE; GLYCERYL 2-ARACHIDONATE; N-ARACHIDONOYLETHANOLAMINE; N-OLEOYLETHANOLAMINE; NAPEPLD PROTEIN, HUMAN; OLEIC ACID; PALMITIC ACID DERIVATIVE; PHOSPHOLIPASE D; TRPV1 PROTEIN, HUMAN; VANILLOID RECEPTOR;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATIONAL STUDY; DISEASE SEVERITY; DYSMENORRHEA; DYSPAREUNIA; ENDOMETRIOSIS; ENDOMETRIUM; ENDOMETRIUM BIOPSY; ENZYME SYNTHESIS; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; LAPAROSCOPY; MEDIATOR; MENSTRUAL CYCLE; NEGATIVE FEEDBACK; PELVIS PAIN SYNDROME; PLASMA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; STROMA CELL; BLOOD; METABOLISM; MIDDLE AGED; YOUNG ADULT;

ADULT; AMIDOHYDROLASES; ARACHIDONIC ACIDS; ENDOCANNABINOIDS; ENDOMETRIOSIS; ETHANOLAMINES; FEMALE; GLYCERIDES; HUMANS; MENSTRUAL CYCLE; MIDDLE AGED; OLEIC ACIDS; PALMITIC ACIDS; PHOSPHOLIPASE D; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; RNA, MESSENGER; STROMAL CELLS; TRPV CATION CHANNELS; YOUNG ADULT;

EID: 84978285979     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719116630414     Document Type: Article

References (47)

1. Burney RO, Giudice LC,. Pathogenesis and pathophysiology of endometriosis. Fertil Sterility. 2012; 98 (3): 511-519.
2. Giudice LC., Clinical practice. Endometriosis. N Engl J Med. 2010; 362 (25): 2389-2398.
3. Gentilini D, Besana A, Vigano P, et al. Endocannabinoid system regulates migration of endometrial stromal cells via cannabinoid receptor 1 through the activation of PI3K and ERK1/2 pathways. Fertil Steril. 2010; 93 (8): 2588-2593.
4. Dmitrieva N, Nagabukuro H, Resuehr D, et al. Endocannabinoid involvement in endometriosis. Pain. 2010; 151 (3): 703-710.
5. Leconte M, Nicco C, Ngo C, et al. Antiproliferative effects of cannabinoid agonists on deep infiltrating endometriosis. Am J Pathol. 2010; 177 (6): 2963-2970.
6. Indraccolo U, Barbieri F,. Effect of palmitoylethanolamide-polydatin combination on chronic pelvic pain associated with endometriosis: preliminary observations. Eur J Obstet Gynecol Reprod Biol. 2010; 150 (1): 76-79.
7. Cobellis L, Castaldi MA, Giordano V, et al. Effectiveness of the association micronized N-palmitoylethanolamine (PEA)-transpolydatin in the treatment of chronic pelvic pain related to endometriosis after laparoscopic assessment: a pilot study. Eur J Obstet Gynecol Reprod Biol. 2011; 158 (1): 82-86.
8. Sanchez AM, Vigano P, Mugione A, Panina-Bordignon P, Candiani M,. The molecular connections between the cannabinoid system and endometriosis. Mol Hum Reprod. 2012; 18 (12): 563-571.
9. Giugliano E, Cagnazzo E, Soave I, Lo Monte G, Wenger JM, Marci R,. The adjuvant use of N-palmitoylethanolamine and transpolydatin in the treatment of endometriotic pain. Eur J Obstet Gynecol Reprod Biol. 2013; 168 (2): 209-213.
10. Iuvone T, Affaitati G, De Filippis D, et al. Ultramicronized palmitoylethanolamide reduces viscero-visceral hyperalgesia in a rat model of endometriosis plus ureteral calculosis: role of mast cells. Pain. 2016; 157 (1): 80-91.
11. Rapino C, Battista N, Bari M, Maccarrone M,. Endocannabinoids as biomarkers of human reproduction. Hum Reprod Update. 2014; 20 (4): 501-516.
12. De Petrocellis L, Di Marzo V,. An introduction to the endocannabinoid system: from the early to the latest concepts. Best Pract Res Clin Endocrinol Metab. 2009; 23 (1): 1-15.
13. Walker JM, Krey JF, Chu CJ, Huang SM,. Endocannabinoids and related fatty acid derivatives in pain modulation. Chem Phys Lipids. 2002; 121 (1-2): 159-172.
14. Zygmunt PM, Petersson J, Andersson DA, et al. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature. 1999; 400 (6743): 452-457.
15. Akopian AN, Ruparel NB, Jeske NA, Patwardhan A, Hargreaves KM,. Role of ionotropic cannabinoid receptors in peripheral antinociception and antihyperalgesia. Trends Pharmacol Sci. 2009; 30 (2): 79-84.
16. Taylor AH, Abbas MS, Habiba MA, Konje JC,. Histomorphometric evaluation of cannabinoid receptor and anandamide modulating enzyme expression in the human endometrium through the menstrual cycle. Histochem Cell Biol. 2010; 133 (5): 557-565.
17. Liu J, Liu X, Duan K, Zhang Y, Guo SW,. The expression and functionality of transient receptor potential vanilloid 1 in ovarian endometriomas. Reprod Sci. 2012; 19 (10): 1110-1124.
18. Petrosino S, Schiano Moriello A, Cerrato S, et al. The anti-inflammatory mediator palmitoylethanolamide enhances the levels of 2-arachidonoyl-glycerol and potentiates its actions at TRPV1 cation channels [published online January 19, 2015]. Br J Pharmacol. 2015.
19. Di Blasio AM, Vignali M, Gentilini D,. The endocannabinoid pathway and the female reproductive organs. J Mol Endocrinol. 2013; 50 (1): R1-R9.
20. 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): 4332-4336.
21. Resuehr D, Glore DR, Taylor HS, Bruner-Tran KL, Osteen KG,. Progesterone-dependent regulation of endometrial cannabinoid receptor type 1 (CB1-R) expression is disrupted in women with endometriosis and in isolated stromal cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Fertil Steril. 2012; 98 (4): 948-956. e941.
22. Balvers MG, Verhoeckx KC, Bijlsma S, et al. Fish oil and inflammatory status alter the n-3 to n-6 balance of the endocannabinoid and oxylipin metabolomes in mouse plasma and tissues. Metabolomics. 2012; 8 (6): 1130-1147.
23. Karasu T, Marczylo TH, Maccarrone M, Konje JC,. The role of sex steroid hormones, cytokines and the endocannabinoid system in female fertility. Hum Reprod Update. 2011; 17 (3): 347-361.
24. Piomelli D, Hohmann AG, Seybold V, Hammock BD,. A lipid gate for the peripheral control of pain. J Neurosci. 2014; 34 (46): 15184-15191.
25. Vincent K, Kennedy S, Stratton P,. Pain scoring in endometriosis: entry criteria and outcome measures for clinical trials. Report from the Art and Science of Endometriosis meeting. Fertil Steril. 2010; 93 (1): 62-67.
26. Annuzzi G, Piscitelli F, Di Marino L, et al. Differential alterations of the concentrations of endocannabinoids and related lipids in the subcutaneous adipose tissue of obese diabetic patients. Lipids Health Dis. 2010; 9: 43.
27. Di Marzo V, Cote M, Matias I, et al. Changes in plasma endocannabinoid levels in viscerally obese men following a 1 year lifestyle modification programme and waist circumference reduction: associations with changes in metabolic risk factors. Diabetologia. 2009; 52 (2): 213-217.
28. Scotchie JG, Savaris RF, Martin CE, Young SL,. Endocannabinoid regulation in human endometrium across the menstrual cycle. Reprod Sci. 2015; 22 (1): 113-123.
29. Maccarrone M, Valensise H, Bari M, Lazzarin N, Romanini C, Finazzi-Agro A,. Progesterone up-regulates anandamide hydrolase in human lymphocytes: role of cytokines and implications for fertility. J Immunol. 2001; 166 (12): 7183-7189.
30. Guo Y, Wang H, Okamoto Y, et al. N-acylphosphatidylethanolamine-hydrolyzing phospholipase D is an important determinant of uterine anandamide levels during implantation. J Biol Chem. 2005; 280 (25): 23429-23432.
31. Ho WS, Barrett DA, Randall MD,. 'Entourage' effects of N-palmitoylethanolamide and N-oleoylethanolamide on vasorelaxation to anandamide occur through TRPV1 receptors. Br J Pharmacol. 2008; 155 (6): 837-846.
32. Caterina MJ, Leffler A, Malmberg AB, et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science. 2000; 288 (5464): 306-313.
33. Hayes P, Meadows HJ, Gunthorpe MJ, et al. Cloning and functional expression of a human orthologue of rat vanilloid receptor-1. Pain. 2000; 88 (2): 205-215.
34. Sadofsky LR, Ramachandran R, Crow C, Cowen M, Compton SJ, Morice AH,. Inflammatory stimuli up-regulate transient receptor potential vanilloid-1 expression in human bronchial fibroblasts. Exp Lung Res. 2012; 38 (2): 75-81.
35. Poli-Neto OB, Filho AA, Rosa e Silva JC, Barbosa Hde F, Candido Dos Reis FJ, Nogueira AA,. Increased capsaicin receptor TRPV1 in the peritoneum of women with chronic pelvic pain. Clin J Pain. 2009; 25 (3): 218-222.
36. Rocha MG, e Silva JC, Ribeiro da Silva A, Candido Dos Reis FJ, Nogueira AA, Poli-Neto OB,. TRPV1 expression on peritoneal endometriosis foci is associated with chronic pelvic pain. Reprod Sci. 2011; 18 (6): 511-515.
37. Fernandes ES, Fernandes MA, Keeble JE,. The functions of TRPA1 and TRPV1: moving away from sensory nerves. Br J Pharmacol. 2012; 166 (2): 510-521.
38. Martini L, Waldhoer M, Pusch M, et al. Ligand-induced down-regulation of the cannabinoid 1 receptor is mediated by the G-protein-coupled receptor-associated sorting protein GASP1. FASEB J. 2007; 21 (3): 802-811.
39. Smith TH, Blume LC, Straiker A, et al. Cannabinoid receptor-interacting protein 1a modulates CB1 receptor signaling and regulation. Mol Pharmacol. 2015; 87 (4): 747-765.
40. Howard FM,. Endometriosis and mechanisms of pelvic pain. J Minim Invasive Gynecol. 2009; 16 (5): 540-550.
41. Jarrell J, Giamberardino MA, Robert M, Nasr-Esfahani M,. Bedside testing for chronic pelvic pain: discriminating visceral from somatic pain. Pain Res Treat. 2011; 2011: 692102.
42. Laux-Biehlmann A, d'Hooghe T, Zollner TM,. Menstruation pulls the trigger for inflammation and pain in endometriosis. Trends Pharmacol Sci. 2015; 36 (5): 270-276.
43. Beste MT, Pfaffle-Doyle N, Prentice EA, et al. Molecular network analysis of endometriosis reveals a role for c-Jun-regulated macrophage activation. Sci Transl Med. 2014; 6 (222): 222 ra 216.
44. Brederson JD, Kym PR, Szallasi A,. Targeting TRP channels for pain relief. Eur J Pharmacol. 2013; 716 (1-3): 61-76.
45. Wang ZY, McDowell T, Wang P, Alvarez R, Gomez T, Bjorling DE,. Activation of CB1 inhibits NGF-induced sensitization of TRPV1 in adult mouse afferent neurons. Neuroscience. 2014; 277: 679-689.
46. Pertwee RG,. Emerging strategies for exploiting cannabinoid receptor agonists as medicines. Br J Pharmacol. 2009; 156 (3): 397-411.
47. Bisogno T, Maccarrone M,. Endocannabinoid signaling and its regulation by nutrients. Biofactors. 2014; 40 (4): 373-380.