Neonatal anandamide treatment results in prolonged mitochondrial damage in the vanilloid receptor type 1-immunoreactive B-type neurons of the rat trigeminal ganglion

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Abstract

Capsaicin acting on the vanilloid type 1 receptor (VR1) excites a subset of primary sensory neurons. Systemic capsaicin treatment of adult or neonatal rats results in selective damage of the B-type neurons in the rat sensory ganglia by causing a long-lasting mitochondrial lesion that has been described in detail in previous studies. The endocannabinoid, anandamide, exhibits an agonist effect on VR1 receptors. The physiological role of anandamide as a VR1 agonist is still uncertain. This study addresses whether high doses of anandamide induce similar ultrastructural changes to those described for capsaicin. The effect of neonatally administered anandamide (1 mg/kg) on neurons of the trigeminal ganglia and the hippocampal formation was examined in the light and electron microscope from the first day after injections to the 20th week after treatment. Anandamide was found to cause mitochondrial damage of the B-type neurons of trigeminal ganglia similar to what has been described for capsaicin. The time course of damage was also comparable. In addition to the cells of the trigeminal ganglia, B-type cells of dorsal root ganglia were also damaged. A-type neurons and satellite glial cells were not affected either in the trigeminal or in the dorsal root ganglia. In the hippocampal formation, where a subpopulation of local circuit neurons is known to contain cannabinoid type 1 (CB1) but not VR1 receptors, anandamide did not cause morphological changes of mitochondria either in the dentate gyrus or in Ammon's horn. At 3 weeks of age, all VR1-immunoreactive neurons in the trigeminal ganglia of animals treated neonatally with anandamide displayed swollen mitochondria. The results suggest that anandamide, at pharmacologically relevant doses, acts on the VR1 receptor and causes prolonged and selective mitochondrial damage of B-type sensory neurons, as has previously been described for capsaicin.

Original languageEnglish
Pages (from-to)805-814
Number of pages10
JournalNeuroscience
Volume115
Issue number3
DOIs
Publication statusPublished - Dec 9 2002

Fingerprint

Trigeminal Ganglion
Capsaicin
Neurons
Hippocampus
Spinal Ganglia
Sensory Receptor Cells
Therapeutics
Mitochondria
Sensory Ganglia
Endocannabinoids
Cannabinoids
anandamide
vanilloid receptor subtype 1
Dentate Gyrus
Neuroglia
B-Lymphocytes
Electrons
Light
Injections
TRPV1 receptor

Keywords

  • Analgesia
  • Cannabinoid
  • Electron microscopy
  • Sensory ganglia

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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title = "Neonatal anandamide treatment results in prolonged mitochondrial damage in the vanilloid receptor type 1-immunoreactive B-type neurons of the rat trigeminal ganglion",
abstract = "Capsaicin acting on the vanilloid type 1 receptor (VR1) excites a subset of primary sensory neurons. Systemic capsaicin treatment of adult or neonatal rats results in selective damage of the B-type neurons in the rat sensory ganglia by causing a long-lasting mitochondrial lesion that has been described in detail in previous studies. The endocannabinoid, anandamide, exhibits an agonist effect on VR1 receptors. The physiological role of anandamide as a VR1 agonist is still uncertain. This study addresses whether high doses of anandamide induce similar ultrastructural changes to those described for capsaicin. The effect of neonatally administered anandamide (1 mg/kg) on neurons of the trigeminal ganglia and the hippocampal formation was examined in the light and electron microscope from the first day after injections to the 20th week after treatment. Anandamide was found to cause mitochondrial damage of the B-type neurons of trigeminal ganglia similar to what has been described for capsaicin. The time course of damage was also comparable. In addition to the cells of the trigeminal ganglia, B-type cells of dorsal root ganglia were also damaged. A-type neurons and satellite glial cells were not affected either in the trigeminal or in the dorsal root ganglia. In the hippocampal formation, where a subpopulation of local circuit neurons is known to contain cannabinoid type 1 (CB1) but not VR1 receptors, anandamide did not cause morphological changes of mitochondria either in the dentate gyrus or in Ammon's horn. At 3 weeks of age, all VR1-immunoreactive neurons in the trigeminal ganglia of animals treated neonatally with anandamide displayed swollen mitochondria. The results suggest that anandamide, at pharmacologically relevant doses, acts on the VR1 receptor and causes prolonged and selective mitochondrial damage of B-type sensory neurons, as has previously been described for capsaicin.",
keywords = "Analgesia, Cannabinoid, Electron microscopy, Sensory ganglia",
author = "E. Sz{\"o}ke and G. Cz{\'e}h and J. Szolcs{\'a}nyi and L. S{\'e}ress",
year = "2002",
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doi = "10.1016/S0306-4522(02)00420-7",
language = "English",
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pages = "805--814",
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T1 - Neonatal anandamide treatment results in prolonged mitochondrial damage in the vanilloid receptor type 1-immunoreactive B-type neurons of the rat trigeminal ganglion

AU - Szöke, E.

AU - Czéh, G.

AU - Szolcsányi, J.

AU - Séress, L.

PY - 2002/12/9

Y1 - 2002/12/9

N2 - Capsaicin acting on the vanilloid type 1 receptor (VR1) excites a subset of primary sensory neurons. Systemic capsaicin treatment of adult or neonatal rats results in selective damage of the B-type neurons in the rat sensory ganglia by causing a long-lasting mitochondrial lesion that has been described in detail in previous studies. The endocannabinoid, anandamide, exhibits an agonist effect on VR1 receptors. The physiological role of anandamide as a VR1 agonist is still uncertain. This study addresses whether high doses of anandamide induce similar ultrastructural changes to those described for capsaicin. The effect of neonatally administered anandamide (1 mg/kg) on neurons of the trigeminal ganglia and the hippocampal formation was examined in the light and electron microscope from the first day after injections to the 20th week after treatment. Anandamide was found to cause mitochondrial damage of the B-type neurons of trigeminal ganglia similar to what has been described for capsaicin. The time course of damage was also comparable. In addition to the cells of the trigeminal ganglia, B-type cells of dorsal root ganglia were also damaged. A-type neurons and satellite glial cells were not affected either in the trigeminal or in the dorsal root ganglia. In the hippocampal formation, where a subpopulation of local circuit neurons is known to contain cannabinoid type 1 (CB1) but not VR1 receptors, anandamide did not cause morphological changes of mitochondria either in the dentate gyrus or in Ammon's horn. At 3 weeks of age, all VR1-immunoreactive neurons in the trigeminal ganglia of animals treated neonatally with anandamide displayed swollen mitochondria. The results suggest that anandamide, at pharmacologically relevant doses, acts on the VR1 receptor and causes prolonged and selective mitochondrial damage of B-type sensory neurons, as has previously been described for capsaicin.

AB - Capsaicin acting on the vanilloid type 1 receptor (VR1) excites a subset of primary sensory neurons. Systemic capsaicin treatment of adult or neonatal rats results in selective damage of the B-type neurons in the rat sensory ganglia by causing a long-lasting mitochondrial lesion that has been described in detail in previous studies. The endocannabinoid, anandamide, exhibits an agonist effect on VR1 receptors. The physiological role of anandamide as a VR1 agonist is still uncertain. This study addresses whether high doses of anandamide induce similar ultrastructural changes to those described for capsaicin. The effect of neonatally administered anandamide (1 mg/kg) on neurons of the trigeminal ganglia and the hippocampal formation was examined in the light and electron microscope from the first day after injections to the 20th week after treatment. Anandamide was found to cause mitochondrial damage of the B-type neurons of trigeminal ganglia similar to what has been described for capsaicin. The time course of damage was also comparable. In addition to the cells of the trigeminal ganglia, B-type cells of dorsal root ganglia were also damaged. A-type neurons and satellite glial cells were not affected either in the trigeminal or in the dorsal root ganglia. In the hippocampal formation, where a subpopulation of local circuit neurons is known to contain cannabinoid type 1 (CB1) but not VR1 receptors, anandamide did not cause morphological changes of mitochondria either in the dentate gyrus or in Ammon's horn. At 3 weeks of age, all VR1-immunoreactive neurons in the trigeminal ganglia of animals treated neonatally with anandamide displayed swollen mitochondria. The results suggest that anandamide, at pharmacologically relevant doses, acts on the VR1 receptor and causes prolonged and selective mitochondrial damage of B-type sensory neurons, as has previously been described for capsaicin.

KW - Analgesia

KW - Cannabinoid

KW - Electron microscopy

KW - Sensory ganglia

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