DIFFERENTIAL CELLULAR LOCALIZATION OF ANTIOXIDANT ENZYMES IN THE TRIGEMINAL GANGLION

被引:51
作者
Sato, H. [1 ,2 ,5 ]
Shibata, M. [1 ]
Shimizu, T. [1 ]
Shibata, S. [3 ]
Toriumi, H. [1 ]
Ebine, T. [1 ]
Kuroi, T. [1 ]
Iwashita, T. [1 ]
Funakubo, M. [1 ]
Kayama, Y. [1 ]
Akazawa, C. [4 ]
Wajima, K. [2 ]
Nakagawa, T. [2 ]
Okano, H. [3 ]
Suzuki, N. [1 ]
机构
[1] Keio Univ, Sch Med, Dept Neurol, Shinjuku Ku, Tokyo 1608582, Japan
[2] Keio Univ, Dept Dent & Oral Surg, Sch Med, Shinjuku Ku, Tokyo 1608582, Japan
[3] Keio Univ, Dept Physiol, Sch Med, Shinjuku Ku, Tokyo 1608582, Japan
[4] Tokyo Med & Dent Univ, Grad Sch Hlth & Sci, Dept Biochem & Biophys, Bunkyo Ku, Tokyo 1138510, Japan
[5] Japan Soc Promot Sci, Chiyoda Ku, Tokyo 1028472, Japan
关键词
trigeminal ganglion; glutathione peroxidase; catalase; transient receptor potential vanilloid subfamily member 1; caspase; inflammatory pain; CAPSAICIN-INDUCED APOPTOSIS; GLUTATHIONE-S-TRANSFERASE; FREE-RADICAL SCAVENGER; NEUROPATHIC PAIN; REACTIVE OXYGEN; THERMAL HYPERALGESIA; OXIDATIVE STRESS; NERVOUS-SYSTEM; MICE LACKING; DIABETIC-NEUROPATHY;
D O I
10.1016/j.neuroscience.2013.06.010
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
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. (C) 2013 IBRO. Published by Elsevier Ltd. All rights reserved.
引用
收藏
页码:345 / 358
页数:14
相关论文
共 66 条
[1]   Prevalence and Characteristics of Painful Diabetic Neuropathy in a Large Community-Based Diabetic Population in the UK [J].
Abbott, Caroline A. ;
Malik, Rayaz A. ;
van Ross, Ernest R. E. ;
Kulkarni, Jai ;
Boulton, Andrew J. M. .
DIABETES CARE, 2011, 34 (10) :2220-2224
[2]   HIV-1 viral protein R causes peripheral nervous system injury associated with in vivo neuropathic pain [J].
Acharjee, Shaona ;
Noorbakhsh, Farshid ;
Stemkowski, Patrick L. ;
Olechowski, Camille ;
Cohen, Eric A. ;
Ballanyi, Klaus ;
Kerr, Bradley ;
Pardo, Carlos ;
Smith, Peter A. ;
Power, Christopher .
FASEB JOURNAL, 2010, 24 (11) :4343-4353
[3]   Capsaicin-induced apoptosis of glioma cells is mediated by TRPV1 vanilloid receptor and requires p38 MAPK activation [J].
Amantini, C. ;
Mosca, M. ;
Nabissi, M. ;
Lucciarini, R. ;
Caprodossi, S. ;
Arcella, A. ;
Giangaspero, F. ;
Santoni, G. .
JOURNAL OF NEUROCHEMISTRY, 2007, 102 (03) :977-990
[4]   CNS Peroxiredoxins and Their Regulation in Health and Disease [J].
Bell, Karen F. S. ;
Hardingham, Giles E. .
ANTIOXIDANTS & REDOX SIGNALING, 2011, 14 (08) :1467-1477
[5]   Neuronal activity regulates glutamate transporter dynamics in developing astrocytes [J].
Benediktsson, Adrienne M. ;
Marrs, Glen S. ;
Tu, Jian Cheng ;
Worley, Paul F. ;
Roth-Stein, Jeffrey D. ;
Bergles, Dwight E. ;
Dailey, Michael E. .
GLIA, 2012, 60 (02) :175-188
[6]   The transcription factor Sox10 is a key regulator of peripheral glial development [J].
Britsch, S ;
Goerich, DE ;
Riethmacher, D ;
Peirano, RI ;
Rossner, M ;
Nave, KA ;
Birchmeier, C ;
Wegner, M .
GENES & DEVELOPMENT, 2001, 15 (01) :66-78
[7]   Dorsal Root Ganglia Damage in SIV-Infected Rhesus Macaques An Animal Model of HIV-Induced Sensory Neuropathy [J].
Burdo, Tricia H. ;
Orzechowski, Krystyna ;
Knight, Heather L. ;
Miller, Andrew D. ;
Williams, Kenneth .
AMERICAN JOURNAL OF PATHOLOGY, 2012, 180 (04) :1362-1369
[8]   Diabetic neuropathy: clinical manifestations and current treatments [J].
Callaghan, Brian C. ;
Cheng, Hsinlin T. ;
Stables, Catherine L. ;
Smith, Andrea L. ;
Feldman, Eva L. .
LANCET NEUROLOGY, 2012, 11 (06) :521-534
[9]   Differential contribution of SNARE-dependent exocytosis to inflammatory potentiation of TRPV1 in nociceptors [J].
Camprubi-Robles, M. ;
Planells-Cases, R. ;
Ferrer-Montiel, A. .
FASEB JOURNAL, 2009, 23 (11) :3722-3733
[10]   Impaired nociception and pain sensation in mice lacking the capsaicin receptor [J].
Caterina, MJ ;
Leffler, A ;
Malmberg, AB ;
Martin, WJ ;
Trafton, J ;
Petersen-Zeitz, KR ;
Koltzenburg, M ;
Basbaum, AI ;
Julius, D .
SCIENCE, 2000, 288 (5464) :306-313