CB1 cannabinoid receptors promote oxidative/nitrosative stress, inflammation and cell death in a murine nephropathy model

Br J Pharmacol. 2010 Jun;160(3):657-68. doi: 10.1111/j.1476-5381.2010.00769.x.

Abstract

Background and purpose: Accumulating recent evidence suggests that cannabinoid-1 (CB(1)) receptor activation may promote inflammation and cell death and its pharmacological inhibition is associated with anti-inflammatory and tissue-protective effects in various preclinical disease models, as well as in humans.

Experimental approach: In this study, using molecular biology and biochemistry methods, we have investigated the effects of genetic deletion or pharmacological inhibition of CB(1) receptors on inflammation, oxidative/nitrosative stress and cell death pathways associated with a clinically relevant model of nephropathy, induced by an important chemotherapeutic drug cisplatin.

Results: Cisplatin significantly increased endocannabinoid anandamide content, activation of p38 and JNK mitogen-activated protein kinases (MAPKs), apoptotic and poly (ADP-ribose)polymerase-dependent cell death, enhanced inflammation (leucocyte infiltration, tumour necrosis factor-alpha and interleukin-1beta) and promoted oxidative/nitrosative stress [increased expressions of superoxide-generating enzymes (NOX2(gp91phox), NOX4), inducible nitric oxide synthase and tissue 4-hydroxynonenal and nitrotyrosine levels] in the kidneys of mice, accompanied by marked histopathological damage and impaired renal function (elevated creatinine and serum blood urea nitrogen) 3 days following its administration. Both genetic deletion and pharmacological inhibition of CB(1) receptors with AM281 or SR141716 markedly attenuated the cisplatin-induced renal dysfunction and interrelated oxidative/nitrosative stress, p38 and JNK MAPK activation, cell death and inflammatory response in the kidney.

Conclusions and implications: The endocannabinoid system through CB(1) receptors promotes cisplatin-induced tissue injury by amplifying MAPK activation, cell death and interrelated inflammation and oxidative/nitrosative stress. These results also suggest that inhibition of CB(1) receptors may exert beneficial effects in renal (and most likely other) diseases associated with enhanced inflammation, oxidative/nitrosative stress and cell death.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Arachidonic Acids / metabolism
  • Cell Death / genetics
  • Cell Death / physiology*
  • Cisplatin
  • Disease Models, Animal
  • Endocannabinoids
  • Glycerides / metabolism
  • Inflammation / physiopathology*
  • Kidney / drug effects
  • Kidney / metabolism
  • Kidney / pathology
  • Kidney / physiopathology
  • Male
  • Mice
  • Mice, Knockout
  • Morpholines / pharmacology
  • Nephritis / chemically induced*
  • Oxidative Stress / physiology*
  • Piperidines / pharmacology
  • Polyunsaturated Alkamides / metabolism
  • Pyrazoles / pharmacology
  • Receptor, Cannabinoid, CB1 / antagonists & inhibitors
  • Receptor, Cannabinoid, CB1 / genetics
  • Receptor, Cannabinoid, CB1 / physiology*
  • Rimonabant
  • Signal Transduction / drug effects
  • Signal Transduction / physiology

Substances

  • Arachidonic Acids
  • Endocannabinoids
  • Glycerides
  • Morpholines
  • Piperidines
  • Polyunsaturated Alkamides
  • Pyrazoles
  • Receptor, Cannabinoid, CB1
  • glyceryl 2-arachidonate
  • Cisplatin
  • Rimonabant
  • AM 281
  • anandamide