Involvement of the endocannabinoid system in retinal damage after high intraocular pressure-induced ischemia in rats

Invest Ophthalmol Vis Sci. 2007 Jul;48(7):2997-3004. doi: 10.1167/iovs.06-1355.

Abstract

Purpose: To evaluate whether high intraocular pressure (IOP)-induced ischemia is associated with modifications in the retinal endocannabinoid metabolism and to ascertain whether drugs that interfere with the endocannabinoid system may prevent retinal damage due to ischemic insult.

Methods: Anandamide (AEA) synthesis, transport, hydrolysis, and AEA endogenous levels were assessed by means of high-performance liquid chromatography in the retinas of rats undergoing 45 minutes of ischemia followed by 12 hours of reperfusion. Under these experimental conditions, binding to cannabinoid (CB1R) and vanilloid (TRPV1) receptor was assessed with rapid-filtration assays. AEA-hydrolase (FAAH, fatty acid amide hydrolase), CB1R and TRPV1 protein content was determined by enzyme-linked immunosorbent assay. Finally, to characterize the neuroprotective profile of drugs that interfere with the endocannabinoid system, cell counting in the retinal ganglion cell (RGC) layer and real-time polymerase chain reactions for Thy-1 mRNA expression were used.

Results: In rat retina, ischemic insult followed by reperfusion resulted in enhanced FAAH activity and protein expression paralleled by a significant decrease in the endogenous AEA tone, whereas the AEA-membrane transporter or the AEA-synthase NAPE-PLD (N-acyl-phosphatidylethanolamine-hydrolyzing-phospholipase-d) were not affected. Retinal ischemia-reperfusion decreased the expression of cannabinoid (CB1) and vanilloid (TRPV1) receptors. Systemic administration of a specific FAAH inhibitor (e.g., URB597) reduced enzyme activity and minimized the retinal damage observed in ischemic-reperfused samples. Similarly, intravitreal injection of the AEA stable analogue, R(+)-methanandamide, reduced cell loss in the RGC layer, and this was prevented by systemic administration of a CB1 or TRPV1 selective antagonist (e.g., SR141716 and capsazepine, respectively).

Conclusions: The original observation that retinal ischemia-reperfusion reduces endogenous AEA via enhanced expression of FAAH supports the deduction that this is implicated in retinal cell loss caused by high IOP in the RGC layer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amidohydrolases / antagonists & inhibitors
  • Amidohydrolases / metabolism
  • Animals
  • Arachidonic Acids / metabolism
  • Benzamides / pharmacology
  • Cannabinoid Receptor Modulators / physiology*
  • Capsaicin / analogs & derivatives
  • Capsaicin / pharmacology
  • Carbamates / pharmacology
  • Cell Count
  • Chromatography, High Pressure Liquid
  • Endocannabinoids*
  • Enzyme Inhibitors / pharmacology
  • Enzyme-Linked Immunosorbent Assay
  • Hydrolysis
  • Intraocular Pressure*
  • Male
  • Ocular Hypertension / complications
  • Piperidines / pharmacology
  • Polyunsaturated Alkamides / metabolism
  • Pyrazoles / pharmacology
  • RNA, Messenger / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Cannabinoid, CB1 / antagonists & inhibitors
  • Receptor, Cannabinoid, CB1 / metabolism
  • Reperfusion Injury / etiology
  • Reperfusion Injury / metabolism*
  • Reperfusion Injury / pathology
  • Reperfusion Injury / prevention & control
  • Retinal Diseases / etiology
  • Retinal Diseases / metabolism*
  • Retinal Diseases / pathology
  • Retinal Diseases / prevention & control
  • Retinal Ganglion Cells / pathology
  • Retinal Vessels / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Rimonabant
  • TRPV Cation Channels / antagonists & inhibitors
  • TRPV Cation Channels / metabolism
  • Thy-1 Antigens / genetics

Substances

  • Arachidonic Acids
  • Benzamides
  • Cannabinoid Receptor Modulators
  • Carbamates
  • Endocannabinoids
  • Enzyme Inhibitors
  • Piperidines
  • Polyunsaturated Alkamides
  • Pyrazoles
  • RNA, Messenger
  • Receptor, Cannabinoid, CB1
  • TRPV Cation Channels
  • Thy-1 Antigens
  • Trpv1 protein, rat
  • cyclohexyl carbamic acid 3'-carbamoylbiphenyl-3-yl ester
  • Amidohydrolases
  • fatty-acid amide hydrolase
  • capsazepine
  • Rimonabant
  • Capsaicin
  • anandamide