Involvement of AMPA receptor Glur2 and Glur3 trafficking in trigeminal spinal subnucleus caudalis and C1/C2 neurons in acute-facial inflammatory pain

Makiko Miyamoto, Yoshiyuki Tsuboi, Kuniya Honda, Masayuki Kobayashi, Kogo Takamiya, Richard L Huganir, Masahiro Kondo, Masamichi Shinoda, Barry J. Sessle, Ayano Katagiri, Daiju Kita, Ikuko Suzuki, Yoshiyuki Oi, Koichi Iwata

Research output: Contribution to journalArticle

Abstract

To evaluate the involvement of trafficking of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR) GluR2 and GluR3 subunits in an acute inflammatory orofacial pain, we analyzed nocifensive behavior, phosphorylated extracellular signal-regulated kinase (pERK) and Fos expression in Vi/Vc, Vc and C1/C2 in GluR2 delta7 knock-in (KI), GluR3 delta7 KI mice and wild-type mice. We also studied Vc neuronal activity to address the hypothesis that trafficking of GluR2 and GluR3 subunits plays an important role in Vi/Vc, Vc and C1/C2 neuronal activity associated with orofacial inflammation in these mice. Late nocifensive behavior was significantly depressed in GluR2 delta7 KI and GluR3 delta7 KI mice. In addition, the number of pERK-immunoreactive (IR) cells was significantly decreased bilaterally in the Vi/Vc, Vc and C1/C2 in GluR2 delta7 KI and GluR3 delta7 KI mice compared to wild-type mice at 40 min after formalin injection, and was also significantly smaller in GluR3 delta7 KI compared to GluR2 delta7 KI mice. The number of Fos protein-IR cells in the ipsilateral Vi/Vc, Vc and C1/C2 was also significantly smaller in GluR2 delta7 KI and GluR3 delta7 KI mice compared to wild-type mice 40 min after formalin injection. Nociceptive neurons functionally identified as wide dynamic range neurons in the Vc, where pERK- and Fos protein-IR cell expression was prominent, showed significantly lower spontaneous activity in GluR2 delta7 KI and GluR3 delta7 KI mice than wild-type mice following formalin injection. These findings suggest that GluR2 and GluR3 trafficking is involved in the enhancement of Vi/Vc, Vc and C1/C2 nociceptive neuronal excitabilities at 16-60 min following formalin injection, resulting in orofacial inflammatory pain.

Original languageEnglish (US)
Article numbere44055
JournalPLoS One
Volume7
Issue number8
DOIs
StatePublished - Aug 24 2012

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Facial Pain
AMPA Receptors
Formaldehyde
Neurons
pain
Extracellular Signal-Regulated MAP Kinases
neurons
receptors
mice
formalin
alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid
mitogen-activated protein kinase
injection
Injections
Proteins
Nociceptors
cells
proteins
inflammation

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Involvement of AMPA receptor Glur2 and Glur3 trafficking in trigeminal spinal subnucleus caudalis and C1/C2 neurons in acute-facial inflammatory pain. / Miyamoto, Makiko; Tsuboi, Yoshiyuki; Honda, Kuniya; Kobayashi, Masayuki; Takamiya, Kogo; Huganir, Richard L; Kondo, Masahiro; Shinoda, Masamichi; Sessle, Barry J.; Katagiri, Ayano; Kita, Daiju; Suzuki, Ikuko; Oi, Yoshiyuki; Iwata, Koichi.

In: PLoS One, Vol. 7, No. 8, e44055, 24.08.2012.

Research output: Contribution to journalArticle

Miyamoto, M, Tsuboi, Y, Honda, K, Kobayashi, M, Takamiya, K, Huganir, RL, Kondo, M, Shinoda, M, Sessle, BJ, Katagiri, A, Kita, D, Suzuki, I, Oi, Y & Iwata, K 2012, 'Involvement of AMPA receptor Glur2 and Glur3 trafficking in trigeminal spinal subnucleus caudalis and C1/C2 neurons in acute-facial inflammatory pain', PLoS One, vol. 7, no. 8, e44055. https://doi.org/10.1371/journal.pone.0044055
Miyamoto, Makiko ; Tsuboi, Yoshiyuki ; Honda, Kuniya ; Kobayashi, Masayuki ; Takamiya, Kogo ; Huganir, Richard L ; Kondo, Masahiro ; Shinoda, Masamichi ; Sessle, Barry J. ; Katagiri, Ayano ; Kita, Daiju ; Suzuki, Ikuko ; Oi, Yoshiyuki ; Iwata, Koichi. / Involvement of AMPA receptor Glur2 and Glur3 trafficking in trigeminal spinal subnucleus caudalis and C1/C2 neurons in acute-facial inflammatory pain. In: PLoS One. 2012 ; Vol. 7, No. 8.
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abstract = "To evaluate the involvement of trafficking of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR) GluR2 and GluR3 subunits in an acute inflammatory orofacial pain, we analyzed nocifensive behavior, phosphorylated extracellular signal-regulated kinase (pERK) and Fos expression in Vi/Vc, Vc and C1/C2 in GluR2 delta7 knock-in (KI), GluR3 delta7 KI mice and wild-type mice. We also studied Vc neuronal activity to address the hypothesis that trafficking of GluR2 and GluR3 subunits plays an important role in Vi/Vc, Vc and C1/C2 neuronal activity associated with orofacial inflammation in these mice. Late nocifensive behavior was significantly depressed in GluR2 delta7 KI and GluR3 delta7 KI mice. In addition, the number of pERK-immunoreactive (IR) cells was significantly decreased bilaterally in the Vi/Vc, Vc and C1/C2 in GluR2 delta7 KI and GluR3 delta7 KI mice compared to wild-type mice at 40 min after formalin injection, and was also significantly smaller in GluR3 delta7 KI compared to GluR2 delta7 KI mice. The number of Fos protein-IR cells in the ipsilateral Vi/Vc, Vc and C1/C2 was also significantly smaller in GluR2 delta7 KI and GluR3 delta7 KI mice compared to wild-type mice 40 min after formalin injection. Nociceptive neurons functionally identified as wide dynamic range neurons in the Vc, where pERK- and Fos protein-IR cell expression was prominent, showed significantly lower spontaneous activity in GluR2 delta7 KI and GluR3 delta7 KI mice than wild-type mice following formalin injection. These findings suggest that GluR2 and GluR3 trafficking is involved in the enhancement of Vi/Vc, Vc and C1/C2 nociceptive neuronal excitabilities at 16-60 min following formalin injection, resulting in orofacial inflammatory pain.",
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