期刊论文详细信息
Molecular Pain
The effect of minocycline on the masticatory movements following the inferior alveolar nerve transection in freely moving rats
Junichi Kitagawa1  Barry J Sessle3  Koichi Iwata2  Kensuke Yamamura1  Yoshiaki Yamada1  Hossain Md Zakir1  Rahman Md Mostafeezur1 
[1] Division of Oral Physiology, Department of Oral Biological Science, Niigata University Graduate School of Medical and Dental Sciences, 2-5274, Gakkocho-dori, Niigata, 951-8514, Japan;Department of Physiology, Nihon University School of Dentistry, 1-8-13 Kandasurugadai, Chiyoda-ku, Tokyo, 101-8310, Japan;Faculty of Dentistry, University of Toronto, 124 Edward Street, Toronto, ON, M5G 1G6, Canada
关键词: modulation;    mastication;    trigeminal principal sensory nucleus;    trigeminal motor nucleus;    trigeminal neuropathic pain;    microglia;    Minocycline;   
Others  :  863874
DOI  :  10.1186/1744-8069-8-27
 received in 2012-01-17, accepted in 2012-04-20,  发布年份 2012
PDF
【 摘 要 】

Background

To determine the effects of inferior alveolar nerve transection (IAN-X) on masticatory movements in freely moving rats and to test if microglial cells in the trigeminal principal sensory nucleus (prV) or motor nucleus (motV) may be involved in modulation of mastication, the effects of microglial cell inhibitor minocycline (MC) on masticatory jaw movements, microglia (Iba1) immunohistochemistry and the masticatory jaw movements and related masticatory muscle EMG activities were studied in IAN-X rats.

Results

The number of Iba1-immunoreactive (IR) cells both in prV and motV was significantly larger in IAN-X rats compared with sham rats on day 3 after IAN-X. The intraperitoneal (i.p.) administration of MC caused a significant reduction of the number of Iba1-IR cells both in prV and motV that was evident on day 14 after IAN-X. Furthermore, a significant reduction of the number of Iba1-IR cells could be observed in motV but not in prV after microinjection (m.i.) of MC into the motV of IAN-X rats. The rats also exhibited a significant decrease in the head-withdrawal threshold on the side ipsilateral to the IAN-X compared to the threshold before IAN-X and it lasted to day 14. In addition, IAN-X markedly affected the ability to rat to carry out mastication. The number of complete masticatory sequences was significantly decreased. Furthermore, the total masticatory sequence time and food preparatory (PP) period duration was significantly elongated in compared to sham rats. Although IAN-X significantly affected the total number of chewing cycles within the RC period of a masticatory sequence, it had no effect on the duration of the chewing cycles. On the other hand, systemic administration of MC (both i.p. and m.i.) in IAN-X rats significantly improved decreased head-withdrawal threshold and the impaired masticatory jaw movements.

Conclusions

The present findings reveal that the strong modulation of masticatory jaw movements occurs following microglial cell activation after IAN-X, and the modulation recovers after inhibition of the microglial cell activation by MC, suggesting that microglial cell activation in the motV as well as in the prV has a pivotal role in modulating mastication following trigeminal nerve injury associated with orofacial neuropathic pain.

【 授权许可】

   
2012 Mostafeezur et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20140725065932640.pdf 1973KB PDF download
48KB Image download
58KB Image download
43KB Image download
140KB Image download
89KB Image download
220KB Image download
【 图 表 】

【 参考文献 】
  • [1]Dubner R: Sessle BJ: The Neural Basis of Oral and Facial Function. Plenum Press, New York; 1978.
  • [2]Lund JP: Mastication and its control by the brain stem. Crit Rev Oral Biol Med 1991, 2:33-64.
  • [3]Nakamura Y, Katakura N: Generation of masticatory rhythm in the brainstem. Neurosci Res 1995, 23:1-19.
  • [4]Yamada Y, Yamamura K, Inoue M: Coordination of cranial motoneurons during mastication. Respir Physiol Neurobiol 2005, 147:177-189.
  • [5]Lund JP, Donga R, Widmer CG, Stohler CS: The pain-adaptation model: a discussion of the relationship between chronic musculoskeletal pain and motor activity. Can J Physiol Pharmacol 1991, 69:683-694.
  • [6]Svensson P, Houe L, Arendt-Nielsen L: Bilateral experimental muscle pain changes electromyographic activity of human jaw-closing muscles during mastication. Exp Brain Res 1997, 116:182-185.
  • [7]Svensson P, Graven-Nielsen T: Craniofacial muscle pain: review of mechanisms and clinical manifestations. J Orofac Pain 2001, 15:117-145.
  • [8]Sae-Lee D, Whittle T, Forte AR, Peck CC, Byth K, Sessle BJ, Murray GM: Effects of experimental pain on jaw muscle activity during goal-directed jaw movements in humans. Exp Brain Res 2008, 189:451-462.
  • [9]Murray GM, Peck CC: Orofacial pain and jaw muscle activity: a new model. J Orofac Pain 2007, 21:263-278. discussion 279–288
  • [10]Svensson P, Arendt-Nielsen L, Houe L: Muscle pain modulates mastication: an experimental study in humans. J Orofac Pain 1998, 12:7-16.
  • [11]Yu XM, Sessle BJ, Vernon H, Hu JW: Effects of inflammatory irritant application to the rat temporomandibular joint on jaw and neck muscle activity. Pain 1995, 60:143-149.
  • [12]Iwata K, Tsuboi Y, Shima A, Harada T, Ren K, Kanda K, Kitagawa J: Central neuronal changes after nerve injury: neuroplastic influences of injury and aging. J Orofac Pain 2004, 18:293-298.
  • [13]Iwata K, Imai T, Tsuboi Y, Tashiro A, Ogawa A, Morimoto T, Masuda Y, Tachibana Y, Hu J: Alteration of medullary dorsal horn neuronal activity following inferior alveolar nerve transection in rats. J Neurophysiol 2001, 86:2868-2877.
  • [14]Okada-Ogawa A, Suzuki I, Sessle BJ, Chiang CY, Salter MW, Dostrovsky JO, Tsuboi Y, Kondo M, Kitagawa J, Kobayashi A, et al.: Astroglia in medullary dorsal horn (trigeminal spinal subnucleus caudalis) are involved in trigeminal neuropathic pain mechanisms. J Neurosci 2009, 29:11161-11171.
  • [15]Nakagawa K, Takeda M, Tsuboi Y, Kondo M, Kitagawa J, Matsumoto S, Kobayashi A, Sessle BJ, Shinoda M, Iwata K: Alteration of primary afferent activity following inferior alveolar nerve transection in rats. Mol Pain 2010, 6:9. BioMed Central Full Text
  • [16]Chiang CY, Wang J, Xie YF, Zhang S, Hu JW, Dostrovsky JO, Sessle BJ: Astroglial glutamate-glutamine shuttle is involved in central sensitization of nociceptive neurons in rat medullary dorsal horn. J Neurosci 2007, 27:9068-9076.
  • [17]Xie YF, Zhang S, Chiang CY, Hu JW, Dostrovsky JO, Sessle BJ: Involvement of glia in central sensitization in trigeminal subnucleus caudalis (medullary dorsal horn). Brain Behav Immun 2007, 21:634-641.
  • [18]Piao ZG, Cho IH, Park CK, Hong JP, Choi SY, Lee SJ, Lee S, Park K, Kim JS, Oh SB: Activation of glia and microglial p38 MAPK in medullary dorsal horn contributes to tactile hypersensitivity following trigeminal sensory nerve injury. Pain 2006, 121:219-231.
  • [19]Lee S, Zhao YQ, Ribeiro-da-Silva A, Zhang J: Distinctive response of CNS glial cells in oro-facial pain associated with injury, infection and inflammation. Mol Pain 2010, 6:79. BioMed Central Full Text
  • [20]Zhu L, Lu J, Tay SS, Jiang H, He BP: Induced NG2 expressing microglia in the facial motor nucleus after facial nerve axotomy. Neuroscience 2010, 166:842-851.
  • [21]Erazi H, Sansar W, Ahboucha S, Gamrani H: Aluminum affects glial system and behavior of rats. C R Biol 2010, 333:23-27.
  • [22]Huxtable AG, Zwicker JD, Alvares TS, Ruangkittisakul A, Fang X, Hahn LB, Posse de Chaves E, Baker GB, Ballanyi K, Funk GD: Glia contribute to the purinergic modulation of inspiratory rhythm-generating networks. J Neurosci 2010, 30:3947-3958.
  • [23]Sribnick EA, Samantaray S, Das A, Smith J, Matzelle DD, Ray SK, Banik NL: Postinjury estrogen treatment of chronic spinal cord injury improves locomotor function in rats. J Neurosci Res 2010, 88:1738-1750.
  • [24]Cui Y, Liao XX, Liu W, Guo RX, Wu ZZ, Zhao CM, Chen PX, Feng JQ: A novel role of minocycline: attenuating morphine antinociceptive tolerance by inhibition of p38 MAPK in the activated spinal microglia. Brain Behav Immun 2008, 22:114-123.
  • [25]Guasti L, Richardson D, Jhaveri M, Eldeeb K, Barrett D, Elphick MR, Alexander SP, Kendall D, Michael GJ, Chapman V: Minocycline treatment inhibits microglial activation and alters spinal levels of endocannabinoids in a rat model of neuropathic pain. Mol Pain 2009, 5:35. BioMed Central Full Text
  • [26]Hains BC, Waxman SG: Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J Neurosci 2006, 26:4308-4317.
  • [27]Ledeboer A, Sloane EM, Milligan ED, Frank MG, Mahony JH, Maier SF, Watkins LR: Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation. Pain 2005, 115:71-83.
  • [28]Mika J, Osikowicz M, Makuch W, Przewlocka B: Minocycline and pentoxifylline attenuate allodynia and hyperalgesia and potentiate the effects of morphine in rat and mouse models of neuropathic pain. Eur J Pharmacol 2007, 560:142-149.
  • [29]Mika J, Rojewska E, Makuch W, Przewlocka B: Minocycline reduces the injury-induced expression of prodynorphin and pronociceptin in the dorsal root ganglion in a rat model of neuropathic pain. Neuroscience 2010, 165:1420-1428.
  • [30]Owolabi SA, Saab CY: Fractalkine and minocycline alter neuronal activity in the spinal cord dorsal horn. FEBS Lett 2006, 580:4306-4310.
  • [31]Raghavendra V, Tanga F, DeLeo JA: Inhibition of microglial activation attenuates the development but not existing hypersensitivity in a rat model of neuropathy. J Pharmacol Exp Ther 2003, 306:624-630.
  • [32]Zanjani TM, Sabetkasaei M, Mosaffa N, Manaheji H, Labibi F, Farokhi B: Suppression of interleukin-6 by minocycline in a rat model of neuropathic pain. Eur J Pharmacol 2006, 538:66-72.
  • [33]Zhao P, Waxman SG, Hains BC: Extracellular signal-regulated kinase-regulated microglia-neuron signaling by prostaglandin E2 contributes to pain after spinal cord injury. J Neurosci 2007, 27:2357-2368.
  • [34]Nie H, Zhang H, Weng HR: Minocycline prevents impaired glial glutamate uptake in the spinal sensory synapses of neuropathic rats. Neuroscience 2010, 170:901-912.
  • [35]Saito K, Hitomi S, Suzuki I, Masuda Y, Kitagawa J, Tsuboi Y, Kondo M, Sessle BJ, Iwata K: Modulation of trigeminal spinal subnucleus caudalis neuronal activity following regeneration of transected inferior alveolar nerve in rats. J Neurophysiol 2008, 99:2251-2263.
  • [36]Cain P, Frank ME, Barry MA: Recovery of chorda tympani nerve function following injury. Exp Neurol 1996, 141:337-346.
  • [37]Lago N, Udina E, Ramachandran A, Navarro X: Neurobiological assessment of regenerative electrodes for bidirectional interfacing injured peripheral nerves. IEEE Trans Biomed Eng 2007, 54:1129-1137.
  • [38]Lee YS, Lin CY, Robertson RT, Hsiao I, Lin VW: Motor recovery and anatomical evidence of axonal regrowth in spinal cord-repaired adult rats. J Neuropathol Exp Neurol 2004, 63:233-245.
  • [39]Dellow PG, Lund JP: Evidence for central timing of rhythmical mastication. J Physiol 1971, 215:1-13.
  • [40]Tanaka S, Kogo M, Chandler SH, Matsuya T: Localization of oral-motor rhythmogenic circuits in the isolated rat brainstem preparation. Brain Res 1999, 821:190-199.
  • [41]Tsuboi A, Kolta A, Chen CC, Lund JP: Neurons of the trigeminal main sensory nucleus participate in the generation of rhythmic motor patterns. Eur J Neurosci 2003, 17:229-238.
  • [42]Kolta A, Brocard F, Verdier D, Lund JP: A review of burst generation by trigeminal main sensory neurons. Arch Oral Biol 2007, 52:325-328.
  • [43]Olsson KA, Sasamoto K, Lund JP: Modulation of transmission in rostral trigeminal sensory nuclei during chewing. J Neurophysiol 1986, 55:56-75.
  • [44]Mostafeezur R, Yamamura K, Kurose M, Yamada Y: Mastication-induced modulation of the jaw-opening reflex during different periods of mastication in awake rabbits. Brain Res 2009, 1254:28-37.
  • [45]Yamamura K: Mastication-induced modulation of orofacial sensory inputs as seen in the jaw reflex and single neuronal activities in the face primary somatosensory cortex of the rabbit. Arch Oral Biol 2007, 52:329-333.
  • [46]Stohler CS: Craniofacial pain and motor function: pathogenesis, clinical correlates, and implications. Crit Rev Oral Biol Med 1999, 10:504-518.
  • [47]Stohler CS, Ashton-Miller JA, Carlson DS: The effects of pain from the mandibular joint and muscles on masticatory motor behaviour in man. Arch Oral Biol 1988, 33:175-182.
  • [48]Moller E, Sheikholeslam A, Lous I: Response of elevator activity during mastication to treatment of functional disorders. Scand J Dent Res 1984, 92:64-83.
  • [49]Sohn MK, Graven-Nielsen T, Arendt-Nielsen L, Svensson P: Effects of experimental muscle pain on mechanical properties of single motor units in human masseter. Clin Neurophysiol 2004, 115:76-84.
  • [50]Cairns BE, Sessle BJ, Hu JW: Evidence that excitatory amino acid receptors within the temporomandibular joint region are involved in the reflex activation of the jaw muscles. J Neurosci 1998, 18:8056-8064.
  • [51]Sessle BJ: Acute and chronic craniofacial pain: brainstem mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates. Crit Rev Oral Biol Med 2000, 11:57-91.
  • [52]Ro JY, Svensson P, Capra N: Effects of experimental muscle pain on electromyographic activity of masticatory muscles in the rat. Muscle Nerve 2002, 25:576-584.
  • [53]Ji RR, Baba H, Brenner GJ, Woolf CJ: Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci 1999, 2:1114-1119.
  • [54]Ji RR, Strichartz G: Cell signaling and the genesis of neuropathic pain. Sci STKE 2004, 2004:reE14.
  • [55]Tsuda M, Inoue K, Salter MW: Neuropathic pain and spinal microglia: a big problem from molecules in "small" glia. Trends Neurosci 2005, 28:101-107.
  • [56]Watkins LR, Maier SF: Glia: a novel drug discovery target for clinical pain. Nat Rev Drug Discov 2003, 2:973-985.
  • [57]Wei F, Guo W, Zou S, Ren K, Dubner R: Supraspinal glial-neuronal interactions contribute to descending pain facilitation. J Neurosci 2008, 28:10482-10495.
  • [58]Milligan ED, Watkins LR: Pathological and protective roles of glia in chronic pain. Nat Rev Neurosci 2009, 10:23-36.
  • [59]Chiang CY, Dostrovsky JO, Iwata K, Sessle BJ: Role of glia in orofacial pain. Neuroscientist 2011, 17:303-320.
  • [60]Newman EA: New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci 2003, 26:536-542.
  • [61]Perea G, Araque A: Synaptic information processing by astrocytes. J Physiol Paris 2006, 99:92-97.
  • [62]Aronson AL: Pharmacotherapeutics of the newer tetracyclines. J Am Vet Med Assoc 1980, 176:1061-1068.
  • [63]Colovic M, Caccia S: Liquid chromatographic determination of minocycline in brain-to-plasma distribution studies in the rat. J Chromatogr B Analyt Technol Biomed Life Sci 2003, 791:337-343.
  • [64]Wu DC, Jackson-Lewis V, Vila M, Tieu K, Teismann P, Vadseth C, Choi DK, Ischiropoulos H, Przedborski S: Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J Neurosci 2002, 22:1763-1771.
  • [65]Hua XY, Svensson CI, Matsui T, Fitzsimmons B, Yaksh TL, Webb M: Intrathecal minocycline attenuates peripheral inflammation-induced hyperalgesia by inhibiting p38 MAPK in spinal microglia. Eur J Neurosci 2005, 22:2431-2440.
  • [66]Cho DC, Cheong JH, Yang MS, Hwang SJ, Kim JM, Kim CH: The effect of minocycline on motor neuron recovery and neuropathic pain in a rat model of spinal cord injury. J Korean Neurosurg Soc 2011, 49:83-91.
  • [67]Zimmermann M: Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.
  • [68]Naftel JP, Richards LP, Pan M, Bernanke JM: Course and composition of the nerves that supply the mandibular teeth of the rat. Anat Rec 1999, 256:433-447.
  • [69]Stein P, Brueckner J, Milliner M: Sensory innervation of mandibular teeth by the nerve to the mylohyoid: implications in local anesthesia. Clin Anat 2007, 20:591-595.
  • [70]Chudler EH, Anderson LC, Byers MR: Trigeminal ganglion neuronal activity and glial fibrillary acidic protein immunoreactivity after inferior alveolar nerve crush in the adult rat. Pain 1997, 73:141-149.
  • [71]Koga Y, Yoshida N, Kobayashi K, Ichiro O, Yamada Y: Development of a three-dimensional jaw-tracking system implanted in the freely moving mouse. Med Eng Phys 2001, 23:201-206.
  文献评价指标  
  下载次数:0次 浏览次数:4次