Decreased age-related cardiac dysfunction, myocardial nitrative stress, inflammatory gene expression, and apoptosis in mice lacking fatty acid amide hydrolase.

Recent studies have uncovered important cross talk between inflammation, generation of reactive oxygen and nitrogen species, and lipid metabolism in the pathogenesis of cardiovascular aging. Inhibition of the endocannabinoid anandamide metabolizing enzyme, the fatty acid amide hydrolase (FAAH), is emerging as a promising novel approach for the treatment of various inflammatory disorders. In this study, we have investigated the age-associated decline of cardiac function and changes in inflammatory gene expression, nitrative stress, and apoptosis in FAAH knockout (FAAH(-/-)) mice and their wild-type (FAAH(+/+)) littermates. Additionally, we have explored the effects of anandamide on TNF-alpha-induced ICAM-1 and VCAM-1 expression and monocyte-endothelial adhesion in human coronary artery endothelial cells (HCAECs). There was no difference in the cardiac function (measured by the pressure-volume conductance catheter system) between 2- to 3-mo-old (young) FAAH(-/-) and FAAH(+/+) mice. In contrast, the aging-associated decline in cardiac function and increased myocardial gene expression of TNF-alpha, gp91phox, matrix metalloproteinase (MMP)-2, MMP-9, caspase-3 and caspase-9, myocardial inducible nitric oxide synthase protein expression, nitrotyrosine formation, poly (ADP-ribose)polymerase cleavage and caspase-3/9 activity, observed in 28- to 31-mo-old (aging) FAAH(+/+) mice, were largely attenuated in knockouts. There was no difference in the myocardial cannabinoid CB(1) and CB(2) receptor gene expression between young and aging FAAH(-/-) and FAAH(+/+) mice. Anandamide dose dependently attenuated the TNF-alpha-induced ICAM-1 and VCAM-1 expression, NF-kappaB activation in HCAECs, and the adhesion of monocytes to HCAECs in a CB(1)- and CB(2)-dependent manner. These findings suggest that pharmacological inhibition of FAAH may represent a novel protective strategy against chronic inflammation, oxidative/nitrative stress, and apoptosis associated with cardiovascular aging and atherosclerosis.

[1]  Z. Ungvari,et al.  Vasculoprotective effects of anti-tumor necrosis factor-alpha treatment in aging. , 2007, The American journal of pathology.

[2]  A. Sanyal,et al.  Endocannabinoids acting at vascular CB1 receptors mediate the vasodilated state in advanced liver cirrhosis , 2001, Nature Medicine.

[3]  S. Gaetani,et al.  Oleoylethanolamide, an endogenous PPAR-α agonist, lowers body weight and hyperlipidemia in obese rats , 2005, Neuropharmacology.

[4]  R. Schwabe,et al.  Fatty Acid Amide Hydrolase Determines Anandamide-induced Cell Death in the Liver* , 2006, Journal of Biological Chemistry.

[5]  N. Ueda,et al.  Partial Purification and Characterization of the Porcine Brain Enzyme Hydrolyzing and Synthesizing Anandamide (*) , 1995, The Journal of Biological Chemistry.

[6]  F. Mach,et al.  Low dose oral cannabinoid therapy reduces progression of atherosclerosis in mice , 2005, Nature.

[7]  D. Kipmen-Korgun,et al.  Anandamide initiates Ca2+ signaling via CB2 receptor linked to phospholipase C in calf pulmonary endothelial cells , 2003 .

[8]  B. Cravatt,et al.  The endogenous cannabinoid system and its role in nociceptive behavior. , 2004, Journal of neurobiology.

[9]  K. Mackie,et al.  Endocannabinoids Acting at Cannabinoid-1 Receptors Regulate Cardiovascular Function in Hypertension , 2004, Circulation.

[10]  T. Hintze,et al.  NAD(P)H oxidase-generated superoxide anion accounts for reduced control of myocardial O2 consumption by NO in old Fischer 344 rats. , 2003, American journal of physiology. Heart and circulatory physiology.

[11]  R. Watson,et al.  Modulation of iNOS activity in age-related cardiac dysfunction. , 2004, Life sciences.

[12]  T. Bonner,et al.  Structure of a cannabinoid receptor and functional expression of the cloned cDNA , 1990, Nature.

[13]  D. Kipmen-Korgun,et al.  Anandamide initiates Ca(2+) signaling via CB2 receptor linked to phospholipase C in calf pulmonary endothelial cells. , 2003, British journal of pharmacology.

[14]  Alan Saghatelian,et al.  Functional disassociation of the central and peripheral fatty acid amide signaling systems. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[15]  C. Ni,et al.  ICAM-1 induction by TNFalpha and IL-6 is mediated by distinct pathways via Rac in endothelial cells. , 2005, Journal of biomedical science.

[16]  B. Cravatt,et al.  Fatty acid amide hydrolase: an emerging therapeutic target in the endocannabinoid system. , 2003, Current opinion in chemical biology.

[17]  Z. Vogel,et al.  Delta-9-tetrahydrocannabinol protects cardiac cells from hypoxia via CB2 receptor activation and nitric oxide production , 2006, Molecular and Cellular Biochemistry.

[18]  M. Valenti,et al.  The FASEB Journal express article 10.1096/fj.05-4943fje. Published online January 10, 2006. ©2006 FASEB , 2022 .

[19]  B. Cravatt,et al.  Hemodynamic profile, responsiveness to anandamide, and baroreflex sensitivity of mice lacking fatty acid amide hydrolase. , 2005, American journal of physiology. Heart and circulatory physiology.

[20]  H. Pan,et al.  Cannabinoid‐2 receptor mediates protection against hepatic ischemia/reperfusion injury , 2007, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[21]  D. Gibson,et al.  Isolation and structure of a brain constituent that binds to the cannabinoid receptor. , 1992, Science.

[22]  Z. Ungvari,et al.  Vasculoprotective effects of anti-tumor necrosis factor-alpha treatment in aging. , 2007, The American journal of pathology.

[23]  J. Groves,et al.  Potent Metalloporphyrin Peroxynitrite Decomposition Catalyst Protects Against the Development of Doxorubicin-Induced Cardiac Dysfunction , 2003, Circulation.

[24]  M. Valenti,et al.  Up‐regulation of anandamide levels as an endogenous mechanism and a pharmacological strategy to limit colon inflammation , 2006, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[25]  R. Alexander,et al.  Vascular cell adhesion molecule-1 (VCAM-1) gene transcription and expression are regulated through an antioxidant-sensitive mechanism in human vascular endothelial cells. , 1993, The Journal of clinical investigation.

[26]  Arya M. Sharma,et al.  Activation of the peripheral endocannabinoid system in human obesity. , 2005, Diabetes.

[27]  A. Planas,et al.  The FASEB Journal express article 10.1096/fj.02-0795fje. Published online January 2, 2003. Inhibition of tumor angiogenesis by cannabinoids , 2022 .

[28]  D. Piomelli,et al.  Oleylethanolamide activates Ras-Erk pathway and improves myocardial function in doxorubicin-induced heart failure. , 2006, Endocrinology.

[29]  R. Lerner,et al.  Chemical characterization of a family of brain lipids that induce sleep. , 1995, Science.

[30]  C. Szabó,et al.  Nitrosative stress and pharmacological modulation of heart failure. , 2005, Trends in pharmacological sciences.

[31]  C. Trautwein,et al.  CB1 cannabinoid receptor antagonism: A new strategy for the treatment of liver fibrosis , 2007, Hepatology.

[32]  G. Appendino,et al.  Anandamide inhibits nuclear factor-kappaB activation through a cannabinoid receptor-independent pathway. , 2003, Molecular pharmacology.

[33]  D. Lamontagne,et al.  The endogenous cardiac cannabinoid system: a new protective mechanism against myocardial ischemia. , 2006, Archives des maladies du coeur et des vaisseaux.

[34]  K. Mackie,et al.  Endocannabinoid activation at hepatic CB1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity. , 2005, The Journal of clinical investigation.

[35]  L. Petrocellis,et al.  The endocannabinoid system and its therapeutic exploitation , 2004, Nature Reviews Drug Discovery.

[36]  W. Campbell,et al.  Cannabinoid CB1 receptor of cat cerebral arterial muscle functions to inhibit L-type Ca2+ channel current. , 1999, The American journal of physiology.

[37]  Ken Mackie,et al.  Cannabinoid receptors as therapeutic targets. , 2006, Annual review of pharmacology and toxicology.

[38]  P. Pacher,et al.  The Endocannabinoid System as an Emerging Target of Pharmacotherapy , 2006, Pharmacological Reviews.

[39]  J. Falck,et al.  Endothelium-derived 2-arachidonylglycerol: an intermediate in vasodilatory eicosanoid release in bovine coronary arteries. , 2005, American journal of physiology. Heart and circulatory physiology.

[40]  L. Liaudet,et al.  Cannabidiol attenuates high glucose-induced endothelial cell inflammatory response and barrier disruption. , 2007, American journal of physiology. Heart and circulatory physiology.

[41]  W. Campbell,et al.  Characterization of the kinetics and distribution of N-arachidonylethanolamine (anandamide) hydrolysis by rat brain. , 1995, Biochimica et biophysica acta.

[42]  B. Cravatt,et al.  The endogenous cannabinoid system protects against colonic inflammation. , 2004, The Journal of clinical investigation.

[43]  S. Gaetani,et al.  Modulation of anxiety through blockade of anandamide hydrolysis , 2003, Nature Medicine.

[44]  M. Korabiowska,et al.  Inhibition of nuclear factor-κB attenuates atherosclerosis in apoE/LDLR - double knockout mice , 2005 .

[45]  C. Szabó,et al.  A New, Potent Poly(ADP-ribose) Polymerase Inhibitor Improves Cardiac and Vascular Dysfunction Associated with Advanced Aging , 2004, Journal of Pharmacology and Experimental Therapeutics.

[46]  B. Cravatt,et al.  Structure and function of fatty acid amide hydrolase. , 2005, Annual review of biochemistry.

[47]  M. Korabiowska,et al.  Inhibition of nuclear factor-kappaB attenuates artherosclerosis in apoE/LDLR - double knockout mice. , 2005, Journal of physiology and pharmacology : an official journal of the Polish Physiological Society.

[48]  R. Schwabe,et al.  Anandamide induces necrosis in primary hepatic stellate cells , 2005, Hepatology.

[49]  H. Nishimatsu,et al.  Blockade of Endogenous Cytokines Mitigates Neointimal Formation in Obese Zucker Rats , 2005, Circulation.

[50]  J. Liao,et al.  A functional role of I kappa B-epsilon in endothelial cell activation. , 2000, Journal of immunology.

[51]  Z. Ungvari,et al.  Aging‐induced proinflammatory shift in cytokine expression profile in rat coronary arteries , 2003, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[52]  J. Schwartz,et al.  Formation and inactivation of endogenous cannabinoid anandamide in central neurons , 1994, Nature.

[53]  Y. Izumi,et al.  Endocannabinoid, anandamide in gingival tissue regulates the periodontal inflammation through NF‐κB pathway inhibition , 2006, FEBS letters.

[54]  A. Makriyannis,et al.  Functional CB1 cannabinoid receptors in human vascular endothelial cells. , 2000, The Biochemical journal.

[55]  Stephen P. Mayfield,et al.  Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides , 1996, Nature.

[56]  Z. Ungvari,et al.  Role of oxidative and nitrosative stress, longevity genes and poly(ADP-ribose) polymerase in cardiovascular dysfunction associated with aging. , 2005, Current vascular pharmacology.

[57]  K. Mackie,et al.  Identification functional characterization of brainstem cannabinoid CB2 receptors. , 2022 .

[58]  D. Deutsch,et al.  Enzymatic synthesis and degradation of anandamide, a cannabinoid receptor agonist. , 1993, Biochemical pharmacology.

[59]  P. Pacher,et al.  Haemodynamic profile and responsiveness to anandamide of TRPV1 receptor knock‐out mice , 2004, The Journal of physiology.

[60]  Pál Pacher,et al.  Left ventricular pressure-volume relationship in a rat model of advanced aging-associated heart failure. , 2004, American journal of physiology. Heart and circulatory physiology.

[61]  R. Schulz Intracellular targets of matrix metalloproteinase-2 in cardiac disease: rationale and therapeutic approaches. , 2007, Annual review of pharmacology and toxicology.

[62]  E. Bertoli,et al.  Oleoylethanolamide Protects Human Sperm Cells from Oxidation Stress: Studies on Cases of Idiopathic Infertility1 , 2006, Biology of reproduction.

[63]  T. Klein Cannabinoid-based drugs as anti-inflammatory therapeutics , 2005, Nature Reviews Immunology.

[64]  L. Mestre,et al.  The synthetic cannabinoid WIN 55,212-2 increases COX-2 expression and PGE2 release in murine brain-derived endothelial cells following Theiler's virus infection. , 2006, Biochemical pharmacology.

[65]  P. Pacher,et al.  Cardiovascular pharmacology of cannabinoids. , 2005, Handbook of experimental pharmacology.

[66]  F. Lenz,et al.  Human brain endothelium: coexpression and function of vanilloid and endocannabinoid receptors. , 2004, Brain research. Molecular brain research.

[67]  Z. Ungvari,et al.  Aging-Induced Phenotypic Changes and Oxidative Stress Impair Coronary Arteriolar Function , 2002, Circulation research.

[68]  J. Liao,et al.  A Functional Role of IκB-ε in Endothelial Cell Activation1 , 2000, The Journal of Immunology.

[69]  B. Cravatt,et al.  Formation of prostamides from anandamide in FAAH knockout mice analyzed by HPLC with tandem mass spectrometry Published, JLR Papers in Press, January 16, 2004. DOI 10.1194/jlr.M300475-JLR200 , 2004, Journal of Lipid Research.

[70]  Z. Vogel,et al.  Anandamide Protects from Low Serum-induced Apoptosis via Its Degradation to Ethanolamine* , 2007, Journal of Biological Chemistry.

[71]  C. Fowler,et al.  Inhibition of fatty acid amide hydrolase, a key endocannabinoid metabolizing enzyme, by analogues of ibuprofen and indomethacin. , 2007, European journal of pharmacology.

[72]  L. Petrocellis,et al.  Prostaglandin Ethanolamides (Prostamides): In Vitro Pharmacology and Metabolism , 2004, Journal of Pharmacology and Experimental Therapeutics.

[73]  B. Cravatt,et al.  Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[74]  L. Hovgaard,et al.  Inhibition of Tumor Necrosis Factor-&agr; Reduces Atherosclerosis in Apolipoprotein E Knockout Mice , 2004, Arteriosclerosis, thrombosis, and vascular biology.

[75]  Peter Libby,et al.  The immune response in atherosclerosis: a double-edged sword , 2006, Nature Reviews Immunology.

[76]  L. Liaudet,et al.  Nitric oxide and peroxynitrite in health and disease. , 2007, Physiological reviews.