The effect of endocannabinoid system in ischemia-reperfusion injury: A friend or a foe?

Expert Opinion on Therapeutic Targets

Volumn 19, Issue 9, 2015, Pages 1261-1275

  Moris, Demetrios ^a   Georgopoulos, Sotirios ^a   Felekouras, Evangelos ^a   Patsouris, Efstratios ^a   Theocharis, Stamatios ^a  

^a UNIVERSITY OF ATHENS   (Greece)

Author keywords

cannabinoid receptors; Cannabinoids; endocannabinoids; ischemia reperfusion injury; organ; system

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; CANNABINOID 2 RECEPTOR; ENDOCANNABINOID; STAT3 PROTEIN;

ATHEROSCLEROSIS; BIBLIOGRAPHIC DATABASE; CELL ADHESION; CEREBROVASCULAR ACCIDENT; ELECTROACUPUNCTURE; HEART FAILURE; HEART INFARCTION; HUMAN; IN VIVO STUDY; KIDNEY FAILURE; LEUKOCYTE; LIVER FAILURE; MACROPHAGE; MONOCYTE; NEUROPROTECTION; NITROSATIVE STRESS; NONHUMAN; REPERFUSION INJURY; RESTENOSIS; REVIEW; UPREGULATION; ANIMAL; DRUG EFFECTS; INFLAMMATION; METABOLISM; MYOCARDIAL REPERFUSION INJURY; PATHOPHYSIOLOGY;

ANIMALS; ENDOCANNABINOIDS; HUMANS; INFLAMMATION; MYOCARDIAL REPERFUSION INJURY; RECEPTOR, CANNABINOID, CB2; REPERFUSION INJURY;

EID: 84940044300     PISSN: 14728222     EISSN: 17447631     Source Type: Journal    
DOI: 10.1517/14728222.2015.1043268     Document Type: Review

References (95)

1. Apstein CS, Deckelbaum L, Mueller M, et al. Graded global ischemia and reperfusion. Cardiac function and lactate metabolism. Circulation 1977; 55 (6): 864-72
2. Hess ML, Manson NH. Molecular oxygen: friend and foe. The role of the oxygen free radical system in the calcium paradox, the oxygen paradox and ischemia/reperfusion injury. J Mol Cell Cardiol 1984; 16 (11): 969-85
3. McCord JM. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 1985; 312 (3): 159-63
4. Pacher P, Hasko G. Endocannabinoids and cannabinoid receptors in ischaemia-reperfusion injury and preconditioning. Br J Pharmacol 2008; 153 (2): 252-62
5. Vasileiou I, Fotopoulou G, Matzourani M, et al. Evidence for the involvement of cannabinoid receptors polymorphisms in the pathophysiology of human diseases. Expert Opin Ther Targets 2013; 17 (4): 363-77
6. Zogopoulos P, Vasileiou I, Patsouris E, Theocharis SE. The role of endocannabinoids in pain modulation. Fundam Clin Pharmacol 2013; 27 (1): 64-80
7. Pacher P, Kunos G. Modulating the endocannabinoid system in human health and disease-successes and failures. FEBS J 2013; 280 (9): 1918-43
8. Zogopoulos P, Korkolopoulou P, Patsouris E, Theocharis S. The antitumor action of cannabinoids on glioma tumorigenesis. Histol Histopathol 2014. [Epub ahead of print]
9. Steffens S, Pacher P. Targeting cannabinoid receptor CB(2) in cardiovascular disorders: promises and controversies. Br J Pharmacol 2012; 167 (2): 313-23
10. Guzman M, Sanchez C, Galve-Roperh I. Cannabinoids and cell fate. Pharmacol Ther 2002; 95 (2): 175-84
11. Bisogno T, Martire A, Petrosino S, et al. Symptom-related changes of endocannabinoid and palmitoylethanolamide levels in brain areas of R6/2 mice, a transgenic model of Huntingtons disease. Neurochem Int 2008; 52 (1-2): 307-13
12. Bari M, Battista N, Fezza F, et al. New insights into endocannabinoid degradation and its therapeutic potential. Mini Rev Med Chem 2006; 6 (3): 257-68
13. Porter AC, Sauer JM, Knierman MD, et al. Characterization of a novel endocannabinoid, virodhamine, with antagonist activity at the CB1 receptor. J Pharmacol Exp Ther 2002; 301 (3): 1020-4
14. Calignano A, La Rana G, Giuffrida A, Piomelli D. Control of pain initiation by endogenous cannabinoids. Nature 1998; 394 (6690): 277-81
15. Mackie K. Cannabinoid receptors: where they are and what they do. J Neuroendocrinol 2008; 20 (Suppl 1): 10-14
16. Di Marzo V, Petrosino S. Endocannabinoids and the regulation of their levels in health and disease. Curr Opin Lipidol 2007; 18 (2): 129-40
17. Pertwee RG. Pharmacological actions of cannabinoids. Handb Exp Pharmacol 2005 (168): 1-51
18. Szoke E, Balla Z, Csernoch L, et al. Interacting effects of capsaicin and anandamide on intracellular calcium in sensory neurones. Neuroreport 2000; 11 (9): 1949-52
19. Shen M, Thayer SA. The cannabinoid agonist Win55,212-2 inhibits calcium channels by receptor-mediated and direct pathways in cultured rat hippocampal neurons. Brain Res 1998; 783 (1): 77-84
20. Nicholson RA, Liao C, Zheng J, et al. Sodium channel inhibition by anandamide and synthetic cannabimimetics in brain. Brain Res 2003; 978 (1-2): 194-204
21. De Petrocellis L, Vellani V, Schiano-Moriello A, et al. Plant-derived cannabinoids modulate the activity of transient receptor potential channels of ankyrin type-1 and melastatin type-8. J Pharmacol Exp Ther 2008; 325 (3): 1007-15
22. Woelkart K, Salo-Ahen OM, Bauer R. CB receptor ligands from plants. Curr Top Med Chem 2008; 8 (3): 173-86
23. Ashton JC. The atypical cannabinoid O-1602: targets, actions, and the central nervous system. Cent Nerv Syst Agents Med Chem 2012; 12 (3): 233-9
24. Han S, Thatte J, Buzard DJ, Jones RM. Therapeutic utility of cannabinoid receptor type 2 (CB(2)) selective agonists. J Med Chem 2013; 56 (21): 8224-56
25. Bikis C, Moris D, Vasileiou I, et al. FAK/Src family of kinases: protective or aggravating factor for ischemia reperfusion injury in nervous system? Expert Opin Ther Targets 2015; 19 (4): 539-49
26. Chan PH. Oxygen radicals in focal cerebral ischemia. Brain Pathol 1994; 4 (1): 59-65
27. Kinouchi H, Epstein CJ, Mizui T, et al. Attenuation of focal cerebral ischemic injury in transgenic mice overexpressing CuZn superoxide dismutase. Proc Natl Acad Sci USA 1991; 88 (24): 11158-62
28. Lambeth JD. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 2004; 4 (3): 181-9
29. Littauer A, de Groot H. Release of reactive oxygen by hepatocytes on reoxygenation: three phases and role of mitochondria. Am J Physiol 1992; 262 (6 Pt 1): G1015-20
30. Toledo-Pereyra LH, Lopez-Neblina F, Toledo AH. Protein kinases in organ ischemia and reperfusion. J Invest Surg 2008; 21 (4): 215-26
31. Yang S, Yip R, Polena S, et al. Reactive oxygen species increased focal adhesion kinase production in pulmonary microvascular endothelial cells. Proc West Pharmacol Soc 2004; 47: 54-6
32. Wang PF, Jiang LS, Bu J, et al. Cannabinoid-2 receptor activation protects against infarct and ischemia-reperfusion heart injury. J Cardiovasc Pharmacol 2012; 59 (4): 301-7
33. Zhang M, Martin BR, Adler MW, et al. Cannabinoid CB(2) receptor activation decreases cerebral infarction in a mouse focal ischemia/reperfusion model. J Cereb Blood Flow Metab 2007; 27 (7): 1387-96
34. Zogopoulos P, Vasileiou I, Patsouris E, Theocharis S. The neuroprotective role of endocannabinoids against chemical-induced injury and other adverse effects. J Appl Toxicol 2013; 33 (4): 246-64
35. Feizi A, Jafari MR, Hamedivafa F, et al. The preventive effect of cannabinoids on reperfusion-induced ischemia of mouse kidney. Exp Toxicol Pathol 2008; 60 (4-5): 405-10
36. Fouad AA, Al-Mulhim AS, Jresat I. Cannabidiol treatment ameliorates ischemia/reperfusion renal injury in rats. Life Sci 2012; 91 (7-8): 284-92
37. Batkai S, Mukhopadhyay P, Horvath B, et al. Delta8-Tetrahydrocannabivarin prevents hepatic ischaemia/reperfusion injury by decreasing oxidative stress and inflammatory responses through cannabinoid CB2 receptors. Br J Pharmacol 2012; 165 (8): 2450-61
38. Batkai S, Osei-Hyiaman D, Pan H, et al. Cannabinoid-2 receptor mediates protection against hepatic ischemia/reperfusion injury. FASEB J 2007; 21 (8): 1788-800
39. Horvath B, Magid L, Mukhopadhyay P, et al. A new cannabinoid CB2 receptor agonist HU-910 attenuates oxidative stress, inflammation and cell death associated with hepatic ischaemia/reperfusion injury. Br J Pharmacol 2012; 165 (8): 2462-78
40. Rodriguez de Fonseca F, Del Arco I, Bermudez-Silva FJ, et al. The endocannabinoid system: physiology and pharmacology. Alcohol Alcohol 2005; 40 (1): 2-14
41. Bosier B, Muccioli GG, Hermans E, Lambert DM. Functionally selective cannabinoid receptor signalling: therapeutic implications and opportunities. Biochem Pharmacol 2010; 80 (1): 1-12
42. Klein TW, Newton C, Larsen K, et al. The cannabinoid system and immune modulation. J Leukoc Biol 2003; 74 (4): 486-96
43. Derocq JM, Jbilo O, Bouaboula M, et al. Genomic and functional changes induced by the activation of the peripheral cannabinoid receptor CB2 in the promyelocytic cells HL-60. Possible involvement of the CB2 receptor in cell differentiation. J Biol Chem 2000; 275 (21): 15621-8
44. Rajesh M, Mukhopadhyay P, Batkai S, et al. CB2-receptor stimulation attenuates TNF-alpha-induced human endothelial cell activation, transendothelial migration of monocytes, and monocyte-endothelial adhesion. Am J Physiol Heart Circ Physiol 2007; 293 (4): H2210-18
45. Schuehly W, Paredes JM, Kleyer J, et al. Mechanisms of osteoclastogenesis inhibition by a novel class of biphenyl-type cannabinoid CB(2) receptor inverse agonists. Chem Biol 2011; 18 (8): 1053-64
46. Zoratti C, Kipmen-Korgun D, Osibow K, et al. Anandamide initiates Ca(2+) signaling via CB2 receptor linked to phospholipase C in calf pulmonary endothelial cells. Br J Pharmacol 2003; 140 (8): 1351-62
47. Mackie K, Stella N. Cannabinoid receptors and endocannabinoids: evidence for new players. AAPS J 2006; 8 (2): E298-306
48. Sang N, Zhang J, Chen C. COX-2 oxidative metabolite of endocannabinoid 2-AG enhances excitatory glutamatergic synaptic transmission and induces neurotoxicity. J Neurochem 2007; 102 (6): 1966-77
49. Nirodi CS, Crews BC, Kozak KR, et al. The glyceryl ester of prostaglandin E2 mobilizes calcium and activates signal transduction in RAW264.7 cells. Proc Natl Acad Sci USA 2004; 101 (7): 1840-5
50. Breivogel CS, Childers SR, Deadwyler SA, et al. Chronic delta9-tetrahydrocannabinol treatment produces a time-dependent loss of cannabinoid receptors and cannabinoid receptor-activated G proteins in rat brain. J Neurochem 1999; 73 (6): 2447-59
51. Smith TH, Sim-Selley LJ, Selley DE. Cannabinoid CB1 receptor-interacting proteins: novel targets for central nervous system drug discovery? Br J Pharmacol 2010; 160 (3): 454-66
52. Shoemaker JL, Joseph BK, Ruckle MB, et al. The endocannabinoid noladin ether acts as a full agonist at human CB2 cannabinoid receptors. J Pharmacol Exp Ther 2005; 314 (2): 868-75
53. Grimsey NL, Goodfellow CE, Dragunow M, Glass M. Cannabinoid receptor 2 undergoes Rab5-mediated internalization and recycles via a Rab11-dependent pathway. Biochim Biophys Acta 2011; 1813 (8): 1554-60
54. Atwood BK, Mackie K. CB2: a cannabinoid receptor with an identity crisis. Br J Pharmacol 2010; 160 (3): 467-79
55. Pazos MR, Mohammed N, Lafuente H, et al. Mechanisms of cannabidiol neuroprotection in hypoxic-ischemic newborn pigs: role of 5HT(1A) and CB2 receptors. Neuropharmacology 2013; 71: 282-91
56. Pazos MR, Cinquina V, Gomez A, et al. Cannabidiol administration after hypoxia-ischemia to newborn rats reduces long-term brain injury and restores neurobehavioral function. Neuropharmacology 2012; 63 (5): 776-83
57. Sun S, Chen X, Gao Y, et al. Mn-SOD upregulation by electroacupuncture attenuates ischemic oxidative damage via CB1R-mediated STAT3 phosphorylation. Mol Neurobiol 2014. [. Epub ahead of print]
58. Zhou H, Zhang Z, Wei H, et al. Activation of STAT3 is involved in neuroprotection by electroacupuncture pretreatment via cannabinoid CB1 receptors in rats. Brain Res 2013; 1529: 154-64
59. Ma L, Zhu Z, Zhao Y, et al. Cannabinoid receptor type 2 activation yields delayed tolerance to focal cerebral ischemia. Curr Neurovasc Res 2011; 8 (2): 145-52
60. Wei H, Yao X, Yang L, et al. Glycogen synthase kinase-3beta is involved in electroacupuncture pretreatment via the cannabinoid CB1 receptor in ischemic stroke. Mol Neurobiol 2014; 49 (1): 326-36
61. Kockeritz L, Doble B, Patel S, Woodgett JR. Glycogen synthase kinase-3-an overview of an over-achieving protein kinase. Curr Drug Targets 2006; 7 (11): 1377-88
62. Dash PK, Johnson D, Clark J, et al. Involvement of the glycogen synthase kinase-3 signaling pathway in TBI pathology and neurocognitive outcome. PLoS ONE 2011; 6 (9): e24648
63. Simao F, Matte A, Pagnussat AS, et al. Resveratrol prevents CA1 neurons against ischemic injury by parallel modulation of both GSK-3beta and CREB through PI3-K/Akt pathways. Eur J Neurosci 2012; 36 (7): 2899-905
64. Du J, Wang Q, Hu B, et al. Involvement of ERK 1/2 activation in electroacupuncture pretreatment via cannabinoid CB1 receptor in rats. Brain Res 2010; 1360: 1-7
65. Pinar-Sueiro S, Zorrilla Hurtado JA, Veiga-Crespo P, et al. Neuroprotective effects of topical CB1 agonist WIN 55212-2 on retinal ganglion cells after acute rise in intraocular pressure induced ischemia in rat. Exp Eye Res 2013; 110: 55-8
66. Viveros MP, Marco EM, Llorente R, Lamota L. The role of the hippocampus in mediating emotional responses to nicotine and cannabinoids: a possible neural substrate for functional interactions. Behav Pharmacol 2007; 18 (5-6): 375-89
67. Gamaleddin I, Wertheim C, Zhu AZ, et al. Cannabinoid receptor stimulation increases motivation for nicotine and nicotine seeking. Addict Biol 2012; 17 (1): 47-61
68. Chen Y, Nie H, Tian L, et al. Nicotine-induced neuroprotection against ischemic injury involves activation of endocannabinoid system in rats. Neurochem Res 2013; 38 (2): 364-70
69. Sun J, Fang Y, Chen T, et al. WIN55, 212-2 promotes differentiation of oligodendrocyte precursor cells and improve remyelination through regulation of the phosphorylation level of the ERK 1/2 via cannabinoid receptor 1 after stroke-induced demyelination. Brain Res 2013; 1491: 225-35
70. Hu B, Wang Q, Chen Y, et al. Neuroprotective effect of WIN 55,212-2 pretreatment against focal cerebral ischemia through activation of extracellular signal-regulated kinases in rats. Eur J Pharmacol 2010; 645 (1-3): 102-7
71. Zhang M, Mahadevan A, Amere M, et al. Unique effects of compounds active at both cannabinoid and serotonin receptors during stroke. Transl Stroke Res 2012; 3 (3): 348-56
72. Su B, Dong H, Ma R, et al. Cannabinoid 1 receptor mediation of spinal cord ischemic tolerance induced by limb remote ischemia preconditioning in rats. J Thorac Cardiovasc Surg 2009; 138 (6): 1409-16
73. Gasperi V, Evangelista D, Chiurchiu V, et al. 2-Arachidonoylglycerol modulates human endothelial cell/leukocyte interactions by controlling selectin expression through CB1 and CB2 receptors. Int J Biochem Cell Biol 2014; 51: 79-88
74. Heinel LA, Rubin S, Rosenwasser RH, et al. Leukocyte involvement in cerebral infarct generation after ischemia and reperfusion. Brain Res Bull 1994; 34 (2): 137-41
75. Shmist YA, Goncharov I, Eichler M, et al. Delta-9-tetrahydrocannabinol protects cardiac cells from hypoxia via CB2 receptor activation and nitric oxide production. Mol Cell Biochem 2006; 283 (1-2): 75-83
76. Gonzalez C, Herradon E, Abalo R, et al. Cannabinoid/agonist WIN 55,212-2 reduces cardiac ischaemia-reperfusion injury in Zucker diabetic fatty rats: role of CB2 receptors and iNOS/eNOS. Diabetes Metab Res Rev 2011; 27 (4): 331-40
77. Li Q, Wang F, Zhang YM, et al. Activation of cannabinoid type 2 receptor by JWH133 protects heart against ischemia/reperfusion-induced apoptosis. Cell Physiol Biochem 2013; 31 (4-5): 693-702
78. Li Q, Guo HC, Maslov LN, et al. Mitochondrial permeability transition pore plays a role in the cardioprotection of CB2 receptor against ischemia-reperfusion injury. Can J Physiol Pharmacol 2014; 92 (3): 205-14
79. Li Q, Cui N, Du Y, et al. Anandamide reduces intracellular Ca2+ concentration through suppression of Na+/Ca2+ exchanger current in rat cardiac myocytes. PLoS One 2013; 8 (5): e63386
80. Duerr GD, Heinemann JC, Suchan G, et al. The endocannabinoid-CB2 receptor axis protects the ischemic heart at the early stage of cardiomyopathy. Basic Res Cardiol 2014; 109 (4): 425
81. Li Q, Shi M, Li B. Anandamide enhances expression of heat shock protein 72 to protect against ischemia-reperfusion injury in rat heart. J Physiol Sci 2013; 63 (1): 47-53
82. Cappellano G, Uberti F, Caimmi PP, et al. Different expression and function of the endocannabinoid system in human epicardial adipose tissue in relation to heart disease. Can J Cardiol 2013; 29 (4): 499-509
83. Cao Z, Mulvihill MM, Mukhopadhyay P, et al. Monoacylglycerol lipase controls endocannabinoid and eicosanoid signaling and hepatic injury in mice. Gastroenterology 2013; 144 (4): 808-17; e15
84. Pacher P, Gao B. Endocannabinoids and liver disease. III. Endocannabinoid effects on immune cells: implications for Inflammatory liver diseases. Am J Physiol Gastrointest Liver Physiol 2008; 294 (4): G850-4
85. Lotersztajn S, Teixeira-Clerc F, Julien B, et al. CB2 receptors as new therapeutic targets for liver diseases. Br J Pharmacol 2008; 153 (2): 286-9
86. Teixeira-Clerc F, Belot MP, et al. Beneficial paracrine effects of cannabinoid receptor 2 on liver injury and regeneration. Hepatology 2010; 52 (3): 1046-59
87. Fouad AA, Jresat I. Therapeutic Potential of cannabidiol against ischemia/reperfusion liver injury in rats. Eur J Pharmacol 2011; 670 (1): 216-23
88. Mukhopadhyay P, Rajesh M, Horvath B, et al. Cannabidiol protects against hepatic ischemia/reperfusion injury by attenuating inflammatory signaling and response, oxidative/nitrative stress, and cell death. Free Radic Biol Med 2011; 50 (10): 1368-81
89. Caraceni P, Pertosa AM, Giannone F, et al. Antagonism of the cannabinoid CB-1 receptor protects rat liver against ischaemia-reperfusion injury complicated by endotoxaemia. Gut 2009; 58 (8): 1135-43
90. Rajesh M, Pan H, Mukhopadhyay P, et al. Cannabinoid-2 receptor agonist HU-308 protects against hepatic ischemia/reperfusion injury by attenuating oxidative stress, inflammatory response, and apoptosis. J Leukoc Biol 2007; 82 (6): 1382-9
91. Edelstein CL, Ling H, Schrier RW. The nature of renal cell injury. Kidney Int 1997; 51 (5): 1341-51
92. Feng L, Ke N, Cheng F, et al. The protective mechanism of ligustrazine against renal ischemia/reperfusion injury. J Surg Res 2011; 166 (2): 298-305
93. Hosseini F, Naseri MK, Badavi M, et al. Effect of beta carotene on lipid peroxidation and antioxidant status following renal ischemia/reperfusion injury in rat. Scand J Clin Lab Invest 2010; 70 (4): 259-63
94. Kizilgun M, Poyrazoglu Y, Oztas Y, et al. Beneficial effects of N-acetylcysteine and ebselen on renal ischemia/reperfusion injury. Ren Fail 2011; 33 (5): 512-17
95. Yamamoto S, Hagiwara S, Hidaka S, et al. The antioxidant EPC-K1 attenuates renal ischemia-reperfusion injury in a rat model. Am J Nephrol 2011; 33 (6): 485-90