Differential cellular localization of antioxidant enzymes in the trigeminal ganglion

H. Sato, Mamoru Shibata, Toshihiko Shimizu, Shinsuke Shibata, H. Toriumi, T. Ebine, T. Kuroi, T. Iwashita, M. Funakubo, Y. Kayama, C. Akazawa, K. Wajima, Taneaki Nakagawa, Hideyuki Okano, N. Suzuki

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

Because of its high oxygen demands, neural tissue is predisposed to oxidative stress. Here, our aim was to clarify the cellular localization of antioxidant enzymes in the trigeminal ganglion. We found that the transcriptional factor Sox10 is localized exclusively in satellite glial cells (SGCs) in the adult trigeminal ganglion. The use of transgenic mice that express the fluorescent protein Venus under the Sox10 promoter enabled us to distinguish between neurons and SGCs. Although both superoxide dismutases 1 and 2 were present in the neurons, only superoxide dismutase 1 was identified in SGCs. The enzymes relevant to hydrogen peroxide degradation displayed differential cellular localization, such that neurons were endowed with glutathione peroxidase 1 and thioredoxin 2, and catalase and thioredoxin 2 were present in SGCs. Our immunohistochemical finding showed that only SGCs were labeled by the oxidative damage marker 8-hydroxy-2'-deoxyguanosine, which indicates that the antioxidant systems of SGCs were less potent. The transient receptor potential vanilloid subfamily member 1 (TRPV1), the capsaicin receptor, is implicated in inflammatory hyperalgesia, and we demonstrated that topical capsaicin application causes short-lasting mechanical hyperalgesia in the face. Our cell-based assay revealed that TRPV1 agonist stimulation in the presence of TRPV1 overexpression caused reactive oxygen species-mediated caspase-3 activation. Moreover, capsaicin induced the cellular demise of primary TRPV1-positive trigeminal ganglion neurons in a dose-dependent manner, and this effect was inhibited by a free radical scavenger and a pancaspase inhibitor. This study delineates the localization of antioxidative stress-related enzymes in the trigeminal ganglion and reveals the importance of the pivotal role of reactive oxygen species in the TRPV1-mediated caspase-dependent cell death of trigeminal ganglion neurons. Therapeutic measures for antioxidative stress should be taken to prevent damage to trigeminal primary sensory neurons in inflammatory pain disorders.

Original languageEnglish
Pages (from-to)345-358
Number of pages14
JournalNeuroscience
Volume248
DOIs
Publication statusPublished - 2013 Sep 17

Fingerprint

TRPV Cation Channels
Trigeminal Ganglion
Neuroglia
Antioxidants
Neurons
Enzymes
Thioredoxins
Capsaicin
Hyperalgesia
Reactive Oxygen Species
Venus
Free Radical Scavengers
Somatoform Disorders
Sensory Receptor Cells
Caspase 3
Catalase
Hydrogen Peroxide
Transgenic Mice
Oxidative Stress
Oxygen

Keywords

  • Catalase
  • Glutathione peroxidase
  • Inflammatory pain
  • Transient receptor potential vanilloid subfamily member 1, caspase
  • Trigeminal ganglion

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Differential cellular localization of antioxidant enzymes in the trigeminal ganglion. / Sato, H.; Shibata, Mamoru; Shimizu, Toshihiko; Shibata, Shinsuke; Toriumi, H.; Ebine, T.; Kuroi, T.; Iwashita, T.; Funakubo, M.; Kayama, Y.; Akazawa, C.; Wajima, K.; Nakagawa, Taneaki; Okano, Hideyuki; Suzuki, N.

In: Neuroscience, Vol. 248, 17.09.2013, p. 345-358.

Research output: Contribution to journalArticle

Sato, H, Shibata, M, Shimizu, T, Shibata, S, Toriumi, H, Ebine, T, Kuroi, T, Iwashita, T, Funakubo, M, Kayama, Y, Akazawa, C, Wajima, K, Nakagawa, T, Okano, H & Suzuki, N 2013, 'Differential cellular localization of antioxidant enzymes in the trigeminal ganglion', Neuroscience, vol. 248, pp. 345-358. https://doi.org/10.1016/j.neuroscience.2013.06.010
Sato, H. ; Shibata, Mamoru ; Shimizu, Toshihiko ; Shibata, Shinsuke ; Toriumi, H. ; Ebine, T. ; Kuroi, T. ; Iwashita, T. ; Funakubo, M. ; Kayama, Y. ; Akazawa, C. ; Wajima, K. ; Nakagawa, Taneaki ; Okano, Hideyuki ; Suzuki, N. / Differential cellular localization of antioxidant enzymes in the trigeminal ganglion. In: Neuroscience. 2013 ; Vol. 248. pp. 345-358.
@article{fe1033b28c7348cb8421c3c92283c6f6,
title = "Differential cellular localization of antioxidant enzymes in the trigeminal ganglion",
abstract = "Because of its high oxygen demands, neural tissue is predisposed to oxidative stress. Here, our aim was to clarify the cellular localization of antioxidant enzymes in the trigeminal ganglion. We found that the transcriptional factor Sox10 is localized exclusively in satellite glial cells (SGCs) in the adult trigeminal ganglion. The use of transgenic mice that express the fluorescent protein Venus under the Sox10 promoter enabled us to distinguish between neurons and SGCs. Although both superoxide dismutases 1 and 2 were present in the neurons, only superoxide dismutase 1 was identified in SGCs. The enzymes relevant to hydrogen peroxide degradation displayed differential cellular localization, such that neurons were endowed with glutathione peroxidase 1 and thioredoxin 2, and catalase and thioredoxin 2 were present in SGCs. Our immunohistochemical finding showed that only SGCs were labeled by the oxidative damage marker 8-hydroxy-2'-deoxyguanosine, which indicates that the antioxidant systems of SGCs were less potent. The transient receptor potential vanilloid subfamily member 1 (TRPV1), the capsaicin receptor, is implicated in inflammatory hyperalgesia, and we demonstrated that topical capsaicin application causes short-lasting mechanical hyperalgesia in the face. Our cell-based assay revealed that TRPV1 agonist stimulation in the presence of TRPV1 overexpression caused reactive oxygen species-mediated caspase-3 activation. Moreover, capsaicin induced the cellular demise of primary TRPV1-positive trigeminal ganglion neurons in a dose-dependent manner, and this effect was inhibited by a free radical scavenger and a pancaspase inhibitor. This study delineates the localization of antioxidative stress-related enzymes in the trigeminal ganglion and reveals the importance of the pivotal role of reactive oxygen species in the TRPV1-mediated caspase-dependent cell death of trigeminal ganglion neurons. Therapeutic measures for antioxidative stress should be taken to prevent damage to trigeminal primary sensory neurons in inflammatory pain disorders.",
keywords = "Catalase, Glutathione peroxidase, Inflammatory pain, Transient receptor potential vanilloid subfamily member 1, caspase, Trigeminal ganglion",
author = "H. Sato and Mamoru Shibata and Toshihiko Shimizu and Shinsuke Shibata and H. Toriumi and T. Ebine and T. Kuroi and T. Iwashita and M. Funakubo and Y. Kayama and C. Akazawa and K. Wajima and Taneaki Nakagawa and Hideyuki Okano and N. Suzuki",
year = "2013",
month = "9",
day = "17",
doi = "10.1016/j.neuroscience.2013.06.010",
language = "English",
volume = "248",
pages = "345--358",
journal = "Neuroscience",
issn = "0306-4522",
publisher = "Elsevier Limited",

}

TY - JOUR

T1 - Differential cellular localization of antioxidant enzymes in the trigeminal ganglion

AU - Sato, H.

AU - Shibata, Mamoru

AU - Shimizu, Toshihiko

AU - Shibata, Shinsuke

AU - Toriumi, H.

AU - Ebine, T.

AU - Kuroi, T.

AU - Iwashita, T.

AU - Funakubo, M.

AU - Kayama, Y.

AU - Akazawa, C.

AU - Wajima, K.

AU - Nakagawa, Taneaki

AU - Okano, Hideyuki

AU - Suzuki, N.

PY - 2013/9/17

Y1 - 2013/9/17

N2 - Because of its high oxygen demands, neural tissue is predisposed to oxidative stress. Here, our aim was to clarify the cellular localization of antioxidant enzymes in the trigeminal ganglion. We found that the transcriptional factor Sox10 is localized exclusively in satellite glial cells (SGCs) in the adult trigeminal ganglion. The use of transgenic mice that express the fluorescent protein Venus under the Sox10 promoter enabled us to distinguish between neurons and SGCs. Although both superoxide dismutases 1 and 2 were present in the neurons, only superoxide dismutase 1 was identified in SGCs. The enzymes relevant to hydrogen peroxide degradation displayed differential cellular localization, such that neurons were endowed with glutathione peroxidase 1 and thioredoxin 2, and catalase and thioredoxin 2 were present in SGCs. Our immunohistochemical finding showed that only SGCs were labeled by the oxidative damage marker 8-hydroxy-2'-deoxyguanosine, which indicates that the antioxidant systems of SGCs were less potent. The transient receptor potential vanilloid subfamily member 1 (TRPV1), the capsaicin receptor, is implicated in inflammatory hyperalgesia, and we demonstrated that topical capsaicin application causes short-lasting mechanical hyperalgesia in the face. Our cell-based assay revealed that TRPV1 agonist stimulation in the presence of TRPV1 overexpression caused reactive oxygen species-mediated caspase-3 activation. Moreover, capsaicin induced the cellular demise of primary TRPV1-positive trigeminal ganglion neurons in a dose-dependent manner, and this effect was inhibited by a free radical scavenger and a pancaspase inhibitor. This study delineates the localization of antioxidative stress-related enzymes in the trigeminal ganglion and reveals the importance of the pivotal role of reactive oxygen species in the TRPV1-mediated caspase-dependent cell death of trigeminal ganglion neurons. Therapeutic measures for antioxidative stress should be taken to prevent damage to trigeminal primary sensory neurons in inflammatory pain disorders.

AB - Because of its high oxygen demands, neural tissue is predisposed to oxidative stress. Here, our aim was to clarify the cellular localization of antioxidant enzymes in the trigeminal ganglion. We found that the transcriptional factor Sox10 is localized exclusively in satellite glial cells (SGCs) in the adult trigeminal ganglion. The use of transgenic mice that express the fluorescent protein Venus under the Sox10 promoter enabled us to distinguish between neurons and SGCs. Although both superoxide dismutases 1 and 2 were present in the neurons, only superoxide dismutase 1 was identified in SGCs. The enzymes relevant to hydrogen peroxide degradation displayed differential cellular localization, such that neurons were endowed with glutathione peroxidase 1 and thioredoxin 2, and catalase and thioredoxin 2 were present in SGCs. Our immunohistochemical finding showed that only SGCs were labeled by the oxidative damage marker 8-hydroxy-2'-deoxyguanosine, which indicates that the antioxidant systems of SGCs were less potent. The transient receptor potential vanilloid subfamily member 1 (TRPV1), the capsaicin receptor, is implicated in inflammatory hyperalgesia, and we demonstrated that topical capsaicin application causes short-lasting mechanical hyperalgesia in the face. Our cell-based assay revealed that TRPV1 agonist stimulation in the presence of TRPV1 overexpression caused reactive oxygen species-mediated caspase-3 activation. Moreover, capsaicin induced the cellular demise of primary TRPV1-positive trigeminal ganglion neurons in a dose-dependent manner, and this effect was inhibited by a free radical scavenger and a pancaspase inhibitor. This study delineates the localization of antioxidative stress-related enzymes in the trigeminal ganglion and reveals the importance of the pivotal role of reactive oxygen species in the TRPV1-mediated caspase-dependent cell death of trigeminal ganglion neurons. Therapeutic measures for antioxidative stress should be taken to prevent damage to trigeminal primary sensory neurons in inflammatory pain disorders.

KW - Catalase

KW - Glutathione peroxidase

KW - Inflammatory pain

KW - Transient receptor potential vanilloid subfamily member 1, caspase

KW - Trigeminal ganglion

UR - http://www.scopus.com/inward/record.url?scp=84880613255&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84880613255&partnerID=8YFLogxK

U2 - 10.1016/j.neuroscience.2013.06.010

DO - 10.1016/j.neuroscience.2013.06.010

M3 - Article

VL - 248

SP - 345

EP - 358

JO - Neuroscience

JF - Neuroscience

SN - 0306-4522

ER -