Immunity and early pregnancy events: Are endocannabinoids the missing link?

Journal of Reproductive Immunology

Volumn 96, Issue 1-2, 2012, Pages 8-18

  Bambang, Katerina N ^a   Lambert, David G ^b   Lam, Patricia M W ^a   Quenby, Siobhan ^c   Maccarrone, Mauro ^d   Konje, Justin C ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b LEICESTER ROYAL INFIRMARY   (United Kingdom)

^c UNIVERSITY OF WARWICK   (United Kingdom)

^d UNIVERSITY OF TERAMO   (Italy)

Author keywords

Endocannabinoids; Female fertility; Immunity; Pregnancy

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ANANDAMIDE; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CD209 ANTIGEN; CD83 ANTIGEN; ENDOCANNABINOID; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 4; PLACENTAL GROWTH FACTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN;

CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL LINEAGE; CELL PROLIFERATION; CHEMOTAXIS; CYTOKINE PRODUCTION; DATA BASE; DENDRITIC CELL; FIRST TRIMESTER PREGNANCY; HUMAN; IMMUNE SYSTEM; IMMUNITY; IMMUNOCOMPETENT CELL; MACROPHAGE; MEDLINE; MOLECULAR INTERACTION; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL;

ANIMALS; CELL MOVEMENT; CYTOKINES; EMBRYO IMPLANTATION; ENDOCANNABINOIDS; FEMALE; FERTILITY; HUMANS; IMMUNE TOLERANCE; KILLER CELLS, NATURAL; PLACENTA; PREGNANCY; RECEPTOR, CANNABINOID, CB1; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84872391406     PISSN: 01650378     EISSN: 18727603     Source Type: Journal    
DOI: 10.1016/j.jri.2012.10.003     Document Type: Review

References (104)

1. Abrahams V.M., Kim Y.M., Straszewski S.L., Romero R., Mor G. Macrophages and apoptotic cell clearance during pregnancy. Am. J. Reprod. Immunol. 2004, 51(4):275-282. (New York, N.Y.: 1989).
2. Aluvihare V.R., Kallikourdis M., Betz A.G. Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 2004, 5(3):266-271.
3. Aris A., Lambert F., Bessette P., Moutquin J.M. Maternal circulating interferon-gamma and interleukin-6 as biomarkers of Th1/Th2 immune status throughout pregnanc. J. Obstet. Gynaecol. Res. 2008, 34(1):7-11.
4. Arruvito L., Billordo A., Capucchio M., Prada M.E., Fainboim L. IL-6 trans-signaling and the frequency of CD4+ FOXP3+ cells in women with reproductive failure. J. Reprod. Immunol. 2009, 82(2):158-165.
5. Ashkar A.A., Croy B.A. Functions of uterine natural killer cells are mediated by interferon gamma production during murine pregnancy. Semin. Immunol. 2001, 13(4):235-241.
6. Ashkar A.A., Di Santo J.P., Croy B.A. Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J. Exp. Med. 2000, 192(2):259-270.
7. Askelund K., Liddell H.S., Zanderigo A.M., Fernando N.S., Khong T.Y., Stone P.R., Chamley L.W. CD83(+)dendritic cells in the decidua of women with recurrent miscarriage and normal pregnancy. Placenta 2004, 25(2-3):140-145.
8. Bambang K.N., Karasu T., Gebeh A., Taylor A.H., Marczylo T.H., Lam P., Willets J.M., Konje J.C. From fertilisation to implantation in mammalian pregnancy-modulation of early human reproduction by the endocannabinoid system. Pharmaceuticals 2010, 3:2910-2929.
9. Bates M.D., Quenby S., Takakuwa K., Johnson P.M., Vince G.S. Aberrant cytokine production by peripheral blood mononuclear cells in recurrent pregnancy loss?. Human Reprod. (Oxford, England) 2002, 17(9):2439-2444.
10. Battista N., Pasquariello N., Di Tommaso M., Maccarrone M. Interplay between endocannabinoids, steroids and cytokines in the control of human reproduction. J. Neuroendocrinol. 2008, 20(Suppl. 1):82-89.
11. Bisogno T., Maurelli S., Melck D., De Petrocellis L., Di Marzo V. Biosynthesis, uptake, and degradation of anandamide and palmitoylethanolamide in leukocytes. J. Biol. Chem. 1997, 272(6):3315-3323.
12. Bouaboula M., Poinot-Chazel C., Bourrie B., Canat X., Calandra B., Rinaldi-Carmona M., Le Fur G., Casellas P. Activation of mitogen-activated protein kinases by stimulation of the central cannabinoid receptor CB1. Biochem. J. 1995, 312(Pt 2):637-641. (no. Pt 2).
13. Butts C.L., Shukair S.A., Duncan K.M., Bowers E., Horn C., Belyavskaya E., Tonelli L., Sternberg E.M. Progesterone inhibits mature rat dendritic cells in a receptor-mediated fashion. Int. Immunol. 2007, 19(3):287-296.
14. Cencioni M.T., Chiurchiu V., Catanzaro G., Borsellino G., Bernardi G., Battistini L., Maccarrone M. Anandamide suppresses proliferation and cytokine release from primary human T-lymphocytes mainly via CB2 receptors. PloS one 2010, 5(1):e8688.
15. Chaouat G., Assal Meliani A., Martal J., Raghupathy R., Elliott J.F., Mosmann T., Wegmann T.G. IL-10 prevents naturally occurring fetal loss in the CBA x DBA/2 mating combination, and local defect in IL-10 production in this abortion-prone combination is corrected by in vivo injection of IFN-tau. J. Immunol. 1995, 154(9):4261-4268. (Baltimore, Md.: 1950).
16. Chaouat G., Zourbas S., Ostojic S., Lappree-Delage G., Dubanchet S., Ledee N., Martal J. A brief review of recent data on some cytokine expressions at the materno-foetal interface which might challenge the classical Th1/Th2 dichotomy. J. Reprod. Immunol. 2002, 53(1-2):241-256.
17. Cosmi L., Liotta F., Angeli R., Mazzinghi B., Santarlasci V., Manetti R., Lasagni L., Vanini V., Romagnani P., Maggi E., Annunziato F., Romagnani S. Th2 cells are less susceptible than Th1 cells to the suppressive activity of CD25+ regulatory thymocytes because of their responsiveness to different cytokines. Blood 2004, 103(8):3117-3121.
18. Croxford J.L., Yamamura T. Cannabinoids and the immune system: potential for the treatment of inflammatory diseases?. J. Neuroimmunol. 2005, 166(1-2):3-18.
19. Croy B.A., Esadeg S., Chantakru S., van den Heuvel M., Paffaro V.A., He H., Black G.P., Ashkar A.A., Kiso Y., Zhang J. Update on pathways regulating the activation of uterine Natural Killer cells, their interactions with decidual spiral arteries and homing of their precursors to the uterus. J. Reprod. Immunol. 2003, 59(2):175-191.
20. Croy B.A., van den Heuvel M.J., Borzychowski A.M., Tayade C. Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol. Rev. 2006, 214:161-185.
21. Devane W.A., Dysarz F.A., Johnson M.R., Melvin L.S., Howlett A.C. Determination and characterization of a cannabinoid receptor in rat brain. Mol. Pharmacol. 1988, 34(5):605-613.
22. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., 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(5090):1946-1949. (New York, N.Y.).
23. Di Marzo V., Petrosino S. Endocannabinoids and the regulation of their levels in health and disease. Curr. Opin. Lipidol. 2007, 18(2):129-140.
24. Do Y., McKallip R.J., Nagarkatti M., Nagarkatti P.S. Activation through cannabinoid receptors 1 and 2 on dendritic cells triggers NF-kappaB-dependent apoptosis: novel role for endogenous and exogenous cannabinoids in immunoregulation. J. Immunol. 2004, 173(4):2373-2382. (Baltimore, Md.: 1950).
25. Dosiou C., Giudice L.C. Natural killer cells in pregnancy and recurrent pregnancy loss: endocrine and immunologic perspectives. Endocr. Rev. 2005, 26(1):44-62.
26. Felder C.C., Joyce K.E., Briley E.M., Mansouri J., Mackie K., Blond O., Lai Y., Ma A.L., Mitchell R.L. Comparison of the pharmacology and signal transduction of the human cannabinoid CB1 and CB2 receptors. Mol. Pharmacol. 1995, 48(3):443-450.
27. Fest S., Aldo P.B., Abrahams V.M., Visintin I., Alvero A., Chen R., Chavez S.L., Romero R., Mor G. Trophoblast-macrophage interactions: a regulatory network for the protection of pregnancy. Am. J. Reprod. Immunol. 2007, 57(1):55-66. (New York, N.Y.: 1989).
28. Fukui A., Fujii S., Yamaguchi E., Kimura H., Sato S., Saito Y. Natural killer cell subpopulations and cytotoxicity for infertile patients undergoing in vitro fertilization. Am. J. Reprod. Immunol. 1999, 41(6):413-422. (New York, N.Y.: 1989).
29. 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(1):54-61. (/FEBS).
30. Gregori S., Casorati M., Amuchastegui S., Smiroldo S., Davalli A.M., Adorini L. Regulatory T cells induced by 1 alpha, 25-dihydroxyvitamin D3 and mycophenolate mofetil treatment mediate transplantation tolerance. J. Immunol. 2001, 167(4):1945-1953. (Baltimore, Md.: 1950).
31. Guerin L.R., Prins J.R., Robertson S.A. Regulatory T-cells and immune tolerance in pregnancy: a new target for infertility treatment?. Hum. Reprod. Update 2009, 15(5):517-535.
32. Habayeb O.M.H., Bell S.C., Konje J.C. Endogenous cannabinoids: metabolism and their role in reproduction. Life Sci. 2002, 70(17):1963-1977.
33. Henderson T.A., Saunders P.T., Moffett-King A., Groome N.P., Critchley H.O. Steroid receptor expression in uterine natural killer cells. J. Clin. Endocrinol. Metab. 2003, 88(1):440-449.
34. Hillard C.J. Biochemistry and pharmacology of the endocannabinoids arachidonylethanolamide and 2-arachidonylglycerol. Prostag. Oth. Lipid M. 2000, 61(1-2):3-18.
35. Howlett A.C., Barth F., Bonner T.I., Cabral G., Casellas P., Devane W.A., Felder C.C., Herkenham M., Mackie K., Martin B.R., Mechoulam R., Pertwee R.G. International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol. Rev. 2002, 54(2):161-202.
36. Ivanova E., Kyurkchiev D., Altankova I., Dimitrov J., Binakova E., Kyurkchiev S. CD83 monocyte-derived dendritic cells are present in human decidua and progesterone induces their differentiation in vitro. Am. J. Reprod. Immunol. 2005, 53(4):199-205. (New York, N.Y.: 1989).
37. Jasper M.J., Tremellen K.P., Robertson S.A. Primary unexplained infertility is associated with reduced expression of the T-regulatory cell transcription factor Foxp3 in endometrial tissue. Mol. Hum. Reprod. 2006, 12(5):301-308.
38. Joseph J., Niggemann B., Zaenker K.S., Entschladen F. Anandamide is an endogenous inhibitor for the migration of tumor cells and T lymphocytes. Cancer Immunol. Immunother. 2004, 53(8):723-728.
39. Kammerer U., Eggert A.O., Kapp M., McLellan A.D., Geijtenbeek T.B., Dietl J., van Kooyk Y., Kampgen E. Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. Am. J. Pathol. 2003, 162(3):887-896.
40. Karimi K., Blois S.M., Arck P.C. The upside of natural killers. Nat. Med. 2008, 14(11):1184-1185.
41. Killestein J., Hoogervorst E.L., Reif M., Blauw B., Smits M., Uitdehaag B.M., Nagelkerken L., Polman C.H. Immunomodulatory effects of orally administered cannabinoids in multiple sclerosis. J. Neuroimmunol. 2003, 137(1-2):140-143.
42. King A., Burrows T.D., Hiby S.E., Bowen J.M., Joseph S., Verma S., Lim P.B., Gardner L., Le Bouteiller P., Ziegler A., Uchanska-Ziegler B., Loke Y.W. Surface expression of HLA-C antigen by human extravillous trophoblast. Placenta 2000, 21(4):376-387.
43. Kishimoto S., Muramatsu M., Gokoh M., Oka S., Waku K., Sugiura T. Endogenous cannabinoid receptor ligand induces the migration of human natural killer cells. J. Biochem. 2005, 137(2):217-223.
44. Klein T.W., Newton C., Friedman H. Inhibition of natural killer cell function by marijuana components. J. Toxicol. Environ. Health 1987, 20(4):321-332.
45. Klein T.W., Newton C., Widen R., Friedman H. Delta 9-tetrahydrocannabinol injection induces cytokine-mediated mortality of mice infected with Legionella pneumophila. J. Pharmacol. Exp. Ther. 1993, 267(2):635-640.
46. Krey G., Frank P., Shaikly V., Barrientos G., Cordo-Russo R., Ringel F., Moschansky P., Chernukhin I.V., Metodiev M., Fernandez N., Klapp B.F., Arck P.C., Blois S.M. In vivo dendritic cell depletion reduces breeding efficiency, affecting implantation and early placental development in mice. J. Mol. Med. (Berlin, Germany) 2008, 86(9):999-1011.
47. Krishnan L., Guilbert L.J., Wegmann T.G., Belosevic M., Mosmann T.R. T helper 1 response against Leishmania major in pregnant C57BL/6 mice increases implantation failure and fetal resorptions. Correlation with increased IFN-gamma and TNF and reduced IL-10 production by placental cells. J. Immunol. 1996, 156(2):653-662. (Baltimore, Md.: 1950).
48. Lee S.F., Newton C., Widen R., Friedman H., Klein T.W. Differential expression of cannabinoid CB(2) receptor mRNA in mouse immune cell subpopulations and following B cell stimulation. Eur. J. Pharmacol. 2001, 423(2-3):235-241.
49. Lenschow D.J., Walunas T.L., Bluestone J.A. CD28/B7 system of T cell costimulation. Annu. Rev. Immunol. 1996, 14:233-258.
50. Lissoni P., Tintori A., Fumagalli L., Brivio F., Messina G., Parolini D., Biondi A., Balestra A., D'Amico G. The endocannabinoid anandamide neither impairs in vitro T-cell function nor induces regulatory T-cell generation. Anticancer Res. 2008, 28(6A):3743-3748.
51. Liu Z., Chen Y., Yang Y., Peng J.P. The effect on MHC class II expression and apoptosis in placenta by IFNgamma administration. Contraception 2002, 65(2):177-184.
52. 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(35):32726-32732.
53. Maccarrone M., Dainese E., Oddi S. Intracellular trafficking of anandamide: new concepts for signaling. Trends Biochem. Sci. 2010, 35(11):601-608.
54. Maccarrone M., De Petrocellis L., Bari M., Fezza F., Salvati S., Di Marzo V., Finazzi-Agro A. Lipopolysaccharide downregulates fatty acid amide hydrolase expression and increases anandamide levels in human peripheral lymphocytes. Arch. Biochem. Biophys. 2001, 393(2):321-328.
55. 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.
56. Maccarrone M., Valensise H., Bari M., Lazzarin N., Romanini C., Finazzi-Agro A. Relation between decreased anandamide hydrolase concentrations in human lymphocytes and miscarriage. Lancet 2000, 355(9212):1326-1329.
57. Mackie K., Lai Y., Westenbroek R., Mitchell R. Cannabinoids activate an inwardly rectifying potassium conductance and inhibit Q-type calcium currents in AtT20 cells transfected with rat brain cannabinoid receptor. J. Neurosci. 1995, 15(10):6552-6561.
58. Maestroni G.J. The endogenous cannabinoid 2-arachidonoyl glycerol as in vivo chemoattractant for dendritic cells and adjuvant for Th1 response to a soluble protein. FASEB J. 2004, 18(15):1914-1916.
59. Massi P., Fuzio D., Vigano D., Sacerdote P., Parolaro D. Relative involvement of cannabinoid CB(1) and CB(2) receptors in the Delta(9)-tetrahydrocannabinol-induced inhibition of natural killer activity. Eur. J. Pharmacol. 2000, 387(3):343-347.
60. Massi P., Vaccani A., Parolaro D. Cannabinoids, immune system and cytokine network. Curr. Pharm. Des. 2006, 12(24):3135-3146.
61. Matias I., Pochard P., Orlando P., Salzet M., Pestel J., Di Marzo V. Presence and regulation of the endocannabinoid system in human dendritic cells. Eur. J. Biochem. 2002, 269(15):3771-3778. (/FEBS).
62. Miyazaki S., Tanebe K., Sakai M., Michimata T., Tsuda H., Fujimura M., Nakamura M., Kiso Y., Saito S. Interleukin 2 receptor gamma chain (gamma(c)) knockout mice show less regularity in estrous cycle but achieve normal pregnancy without fetal compromise. Am. J. Reprod. Immunol. 2002, 47(4):222-230. (New York, N.Y.: 1989).
63. Mor G., Cardenas I. The immune system in pregnancy: a unique complexity. Am. J. Reprod. Immunol. 2010, 63(6):425-433. (New York, N.Y.: 1989).
64. Nakamura H., Jasper M.J., Hull M.L., Aplin J.D., Robertson S.A. Macrophages regulate expression of alpha1,2-fucosyltransferase genes in human endometrial epithelial cells. Mol. Hum. Reprod. 2012, 18(4):204-215.
65. Nakano Y., Pross S.H., Friedman H. Modulation of interleukin 2 activity by delta 9-tetrahydrocannabinol after stimulation with concanavalin A, phytohemagglutinin, or anti-CD3 antibody. Proc. Soc. Exp. Biol. Med. 1992, 201(2):165-168. (New York, N.Y.).
66. Nakashima A., Ito M., Shima T., Bac N.D., Hidaka T., Saito S. Accumulation of IL-17-positive cells in decidua of inevitable abortion cases. Am. J. Reprod. Immunol. 2010, 64(1):4-11. (New York, N.Y.: 1989).
67. Norwitz E.R., Schust D.J., Fisher S.J. Implantation and the survival of early pregnancy. N. Engl. J. Med. 2001, 345(19):1400-1408.
68. Oddi S., Fezza F., Pasquariello N., D'Agostino A., Catanzaro G., De Simone C., Rapino C., Finazzi-Agro A., Maccarrone M. Molecular identification of albumin and Hsp70 as cytosolic anandamide-binding proteins. Chem. Biol. 2009, 16(6):624-632.
69. Paradisi A., Pasquariello N., Barcaroli D., Maccarrone M. Anandamide regulates keratinocyte differentiation by inducing DNA methylation in a CB1 receptor-dependent manner. J. Biol. Chem. 2008, 283(10):6005-6012.
70. Paria B.C., Dey S.K. Ligand-receptor signaling with endocannabinoids in preimplantation embryo development and implantation. Chem. Phys. Lipids 2000, 108(1-2):211-220.
71. Paria B.C., Wang H., Dey S.K. Endocannabinoid signaling in synchronizing embryo development and uterine receptivity for implantation. Chemistry and Physics of Lipids; Symposium on Cannabinoids: Chemistry and Biology 2002, 201.
72. Pearson H. Reproductive immunology: immunity's pregnant pause. Nature 2002, 420(6913):265-266.
73. Pestonjamasp V.K., Burstein S.H. Anandamide synthesis is induced by arachidonate mobilizing agonists in cells of the immune system. Biochim. Biophys. Acta 1998, 1394(2-3):249-260.
74. Petroff M.G., Chen L., Phillips T.A., Azzola D., Sedlmayr P., Hunt J.S. B7 family molecules are favorably positioned at the human maternal-fetal interface. Biol. Reprod. 2003, 68(5):1496-1504.
75. Piccinni M.P. T cells in normal pregnancy and recurrent pregnancy loss. Reprod. Biomed. Online 2007, 14(1):95-99.
76. Plaks V., Birnberg T., Berkutzki T., Sela S., BenYashar A., Kalchenko V., Mor G., Keshet E., Dekel N., Neeman M., Jung S. Uterine DCs are crucial for decidua formation during embryo implantation in mice. J. Clin. Invest. 2008, 118(12):3954-3965.
77. Quenby S., Nik H., Innes B., Lash G., Turner M., Drury J., Bulmer J. Uterine natural killer cells and angiogenesis in recurrent reproductive failure. Human Reprod. (Oxford, England) 2009, 24(1):45-54.
78. Renaud S.J., Postovit L.M., Macdonald-Goodfellow S.K., McDonald G.T., Caldwell J.D., Graham C.H. Activated macrophages inhibit human cytotrophoblast invasiveness in vitro. Biol. Reprod. 2005, 73(2):237-243.
79. Ribeiro A., Ferraz-de-Paula V., Pinheiro M.L., Sakai M., Costa-Pinto F.A., Palermo-Neto J. Anandamide prior to sensitization increases cell-mediated immunity in mice. Int. Immunopharmacol. 2010, 10(4):431-439.
80. Robson A., Harris L.K., Innes B.A., Lash G.E., Aljunaidy M.M., Aplin J.D., Baker P.N., Robson S.C., Bulmer J.N. Uterine natural killer cells initiate spiral artery remodeling in human pregnancy. FASEB J. 2012.
81. Ross R.A., Brockie H.C., Pertwee R.G. Inhibition of nitric oxide production in RAW264.7 macrophages by cannabinoids and palmitoylethanolamide. Eur. J. Pharmacol. 2000, 401(2):121-130.
82. Rutella S., Danese S., Leone G. Tolerogenic dendritic cells: cytokine modulation comes of age. Blood 2006, 108(5):1435-1440.
83. Sacerdote P., Martucci C., Vaccani A., Bariselli F., Panerai A.E., Colombo A., Parolaro D., Massi P. The nonpsychoactive component of marijuana cannabidiol modulates chemotaxis and IL-10 and IL-12 production of murine macrophages both in vivo and in vitro. J. Neuroimmunol. 2005, 159(1-2):97-105.
84. Sasaki Y., Sakai M., Miyazaki S., Higuma S., Shiozaki A., Saito S. Decidual and peripheral blood CD4+ CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol. Hum. Reprod. 2004, 10(5):347-353.
85. Schuel H. Tuning the oviduct to the anandamide tone. J. Clin. Invest. 2006, 116(8):2087-2090.
86. Srivastava M.D., Srivastava B.I., Brouhard B. Delta9 tetrahydrocannabinol and cannabidiol alter cytokine production by human immune cells. Immunopharmacology 1998, 40(3):179-185.
87. Stewart C.L., Kaspar P., Brunet L.J., Bhatt H., Gadi I., Kontgen F., Abbondanzo S.J. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 1992, 359(6390):76-79.
88. Sugamura K., Sugiyama S., Nozaki T., Matsuzawa Y., Izumiya Y., Miyata K., Nakayama M., Kaikita K., Obata T., Takeya M., Ogawa H. Activated endocannabinoid system in coronary artery disease and antiinflammatory effects of cannabinoid 1 receptor blockade on macrophages. Circulation 2009, 119(1):28-36.
89. Sun L., Crotty M.L., Sensel M., Sather H., Navara C., Nachman J., Steinherz P.G., Gaynon P.S., Seibel N., Mao C., Vassilev A., Reaman G.H., Uckun F.M. Expression of dominant-negative Ikaros isoforms in T-cell acute lymphoblastic leukemia. Clin. Cancer Res. 1999, 5(8):2112-2120.
90. Svensson L., Arvola M., Sallstrom M.A., Holmdahl R., Mattsson R. The Th2 cytokines IL-4 and IL-10 are not crucial for the completion of allogeneic pregnancy in mice. J. Reprod. Immunol. 2001, 51(1):3-7.
91. Taylor A.H., Amoako A.A., Bambang K., Karasu T., Gebeh A., Lam P.M., Marzcylo T.H., Konje J.C. Endocannabinoids and pregnancy. Clin. Chim. Acta 2010, 411(13-14):921-930.
92. Taylor A.H., Ang C., Bell S.C., Konje J.C. The role of the endocannabinoid system in gametogenesis, implantation and early pregnancy. Hum. Reprod. Update 2007, 13(5):501-513.
93. Tekelioglu-Uysal M., Edwards R.G., Kisnisci H.A. Ultrastructural relationships between decidua, trophoblast and lymphocytes at the beginning of human pregnancy. J. Reprod. Fertil. 1975, 42(3):431-438.
94. Thornton A.M., Korty P.E., Tran D.Q., Wohlfert E.A., Murray P.E., Belkaid Y., Shevach E.M. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J. Immunol. 2010, 184(7):3433-3441. (Baltimore, Md.: 1950).
95. Valk P., Verbakel S., Vankan Y., Hol S., Mancham S., Ploemacher R., Mayen A., Lowenberg B., Delwel R. Anandamide, a natural ligand for the peripheral cannabinoid receptor is a novel synergistic growth factor for hematopoietic cells. Blood 1997, 90(4):1448-1457.
96. Wang H.B., Matsumoto H., Guo Y., Paria B.C., Roberts R.L., Dey S.K. Differential G protein-coupled cannabinoid receptor signaling by anandamide directs blastocyst activation for implantation. Proc. Natl. Acad. Sci. U.S.A. 2003, 100(25):14914-14919.
97. Wang H., Xie H., Guo Y., Zhang H., Takahashi T., Kingsley P.J., Marnett L.J., Das S.K., Cravatt B.F., Dey S.K. Fatty acid amide hydrolase deficiency limits early pregnancy events. J. Clin. Invest. 2006, 116(8):2122-2131.
98. Wang W.J., Hao C.F., Qu Q.L., Wang X., Qiu L.H., Lin Q.D. The deregulation of regulatory T cells on interleukin-17-producing T helper cells in patients with unexplained early recurrent miscarriage. Human Reprod. (Oxford, England) 2010, 25(10):2591-2596.
99. Wang W.J., Hao C.F., Yi-Lin, Yin G.J., Bao S.H., Qiu L.H., Lin Q.D. Increased prevalence of T helper 17 (Th17) cells in peripheral blood and decidua in unexplained recurrent spontaneous abortion patients. J. Reprod. Immunol. 2010, 84(2):164-170.
100. Wegmann T.G., Lin H., Guilbert L., Mosmann T.R. Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon?. Immunol. Today 1993, 14(7):353-356.
101. Weisman Y., Harell A., Edelstein S., David M., Spirer Z., Golander A. 1α,25-Dihydroxyvitamin D3 and 24,25-dihydroxyvitamin D3 in vitro synthesis by human decidua and placenta. Nature 1979, 281(5729):317-319.
102. Wilczynski J.R. Th1/Th2 cytokines balance - yin and yang of reproductive immunology. Eur. J. Obstet. Gynecol. Reprod. Biol. 2005, 122(2):136-143.
103. Yuan M., Kiertscher S.M., Cheng Q., Zoumalan R., Tashkin D.P., Roth M.D. Delta 9-Tetrahydrocannabinol regulates Th1/Th2 cytokine balance in activated human T cells. J. Neuroimmunol. 2002, 133(1-2):124-131.
104. Zenclussen A.C., Gerlof K., Zenclussen M.L., Sollwedel A., Bertoja A.Z., Ritter T., Kotsch K., Leber J., Volk H.D. Abnormal T-cell reactivity against paternal antigens in spontaneous abortion: adoptive transfer of pregnancy-induced CD4+ CD25+ T regulatory cells prevents fetal rejection in a murine abortion model. Am. J. Pathol. 2005, 166(3):811-822.