Dietary grape seed polyphenols repress neuron and glia activation in trigeminal ganglion and trigeminal nucleus caudalis
Tóm tắt
Inflammation and pain associated with temporomandibular joint disorder, a chronic disease that affects 15% of the adult population, involves activation of trigeminal ganglion nerves and development of peripheral and central sensitization. Natural products represent an underutilized resource in the pursuit of safe and effective ways to treat chronic inflammatory diseases. The goal of this study was to investigate effects of grape seed extract on neurons and glia in trigeminal ganglia and trigeminal nucleus caudalis in response to persistent temporomandibular joint inflammation. Sprague Dawley rats were pretreated with 200 mg/kg/d MegaNatural-BP grape seed extract for 14 days prior to bilateral injections of complete Freund's adjuvant into the temporomandibular joint capsule. In response to grape seed extract, basal expression of mitogen-activated protein kinase phosphatase 1 was elevated in neurons and glia in trigeminal ganglia and trigeminal nucleus caudalis, and expression of the glutamate aspartate transporter was increased in spinal glia. Rats on a normal diet injected with adjuvant exhibited greater basal levels of phosphorylated-p38 in trigeminal ganglia neurons and spinal neurons and microglia. Similarly, immunoreactive levels of OX-42 in microglia and glial fibrillary acidic protein in astrocytes were greatly increased in response to adjuvant. However, adjuvant-stimulated levels of phosphorylated-p38, OX-42, and glial fibrillary acidic protein were significantly repressed in extract treated animals. Furthermore, grape seed extract suppressed basal expression of the neuropeptide calcitonin gene-related peptide in spinal neurons. Results from our study provide evidence that grape seed extract may be beneficial as a natural therapeutic option for temporomandibular joint disorders by suppressing development of peripheral and central sensitization.
Tài liệu tham khảo
Al-Jundi MA, John MT, Setz JM, Szentpetery A, Kuss O: Meta-analysis of treatment need for temporomandibular disorders in adult nonpatients. J Orofac Pain 2008, 22: 97–107.
Herb K, Cho S, Stiles MA: Temporomandibular joint pain and dysfunction. Curr Pain Headache Rep 2006, 10: 408–414. 10.1007/s11916-006-0070-7
Bonjardim LR, Lopes-Filho RJ, Amado G, Albuquerque RL, Goncalves SR: Association between symptoms of temporomandibular disorders and gender, morphological occlusion, and psychological factors in a group of university students. Indian J Dent Res 2009, 20: 190–194. 10.4103/0970-9290.52901
Bereiter DA, Okamoto K, Bereiter DF: Effect of persistent monoarthritis of the temporomandibular joint region on acute mustard oil-induced excitation of trigeminal subnucleus caudalis neurons in male and female rats. Pain 2005, 117: 58–67. 10.1016/j.pain.2005.05.013
Shimizu K, Guo W, Wang H, Zou S, LaGraize SC, Iwata K, Wei F, Dubner R, Ren K: Differential involvement of trigeminal transition zone and laminated subnucleus caudalis in orofacial deep and cutaneous hyperalgesia: the effects of interleukin-10 and glial inhibitors. Mol Pain 2009, 5: 75. 10.1186/1744-8069-5-75
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. 10.1016/j.bbi.2006.07.008
Damodaram S, Thalakoti S, Freeman SE, Garrett FG, Durham PL: Tonabersat inhibits trigeminal ganglion neuronal-satellite glial cell signaling. Headache 2009, 49: 5–20. 10.1111/j.1526-4610.2008.01262.x
Ren K: Emerging role of astroglia in pain hypersensitivity. Jpn Dent Sci Rev 2010, 46: 86–92. 10.1016/j.jdsr.2009.10.005
Guo W, Wang H, Watanabe M, Shimizo K, Zou S, LaGraize S, Wei F, Dubner R, Ren K: Glial-Cytokine-Neuronal Interactions Underlying the Mechanisms of Persistent Pain. J of Neuroscience 2007, 27: 6006–6018. 10.1523/JNEUROSCI.0176-07.2007
Garry EM, Delaney A, Blackburn-Munro G, Dickinson T, Moss A, Nakalembe I, Robertson DC, Rosie R, Robberecht P, Mitchell R, Fleetwood-Walker SM: Activation of p38 and p42/44 MAP kinase in neuropathic pain: involvement of VPAC2 and NK2 receptors and mediation by spinal glia. Mol Cell Neurosci 2005, 30: 523–537. 10.1016/j.mcn.2005.08.016
Hanani M: Satellite glial cells in sensory ganglia: from form to function. Brain Res Rev 2005, 48: 457–476. 10.1016/j.brainresrev.2004.09.001
Chiang CY, Li Z, Dostrovsky JO, Sessle BJ: Central sensitization in medullary dorsal horn involves gap junctions and hemichannels. Neuroreport 2010, 21: 233–237. 10.1097/WNR.0b013e328336eecb
Cheng JK, Ji RR: Intracellular signaling in primary sensory neurons and persistent pain. Neurochem Res 2008, 33: 1970–1978. 10.1007/s11064-008-9711-z
Takeda M, Takahashi M, Matsumoto S: Contribution of the activation of satellite glia in sensory ganglia to pathological pain. Neurosci Biobehav Rev 2009, 33: 784–792. 10.1016/j.neubiorev.2008.12.005
Ji RR, Gereau RWt, Malcangio M, Strichartz GR: MAP kinase and pain. Brain Res Rev 2009, 60: 135–148. 10.1016/j.brainresrev.2008.12.011
Ji RR: Peripheral and central mechanisms of inflammatory pain, with emphasis on MAP kinases. Curr Drug Targets Inflamm Allergy 2004, 3: 299–303. 10.2174/1568010043343804
Crown ED, Ye Z, Johnson KM, Xu GY, McAdoo DJ, Hulsebosch CE: Increases in the activated forms of ERK 1/2, p38 MAPK, and CREB are correlated with the expression of at-level mechanical allodynia following spinal cord injury. Exp Neurol 2006, 199: 397–407. 10.1016/j.expneurol.2006.01.003
Kopp S: Neuroendocrine, immune, and local responses related to temporomandibular disorders. J Orofac Pain 2001, 15: 9–28.
Thalakoti S, Patil V, Damodaram S, Vause C, Langford L, Freeman S, Durham P: Neuron-Glia signaling in trigeminal ganglion: Implications for migraine pathology. Headache 2007, 47: 1008–1023. 10.1111/j.1526-4610.2007.00854.x
Vause CV, Durham PL: Calcitonin gene-related peptide differentially regulates gene and protein expression in trigeminal glia cells: findings from array analysis. Neurosci Lett 2010, 473: 163–167. 10.1016/j.neulet.2010.01.074
Woolf C, Salter M: Neuronal plasticity: increasing the gain in pain. Science 2000, 288: 1765–1768. 10.1126/science.288.5472.1765
Li J, Vause C, Durham P: Calcitonin gene-related peptide stimulation of nitric oxide synthesis and release from trigeminal ganglion glial cells. Brain Research 2008, 1196: 22–32. 10.1016/j.brainres.2007.12.028
Vause C, Durham P: CGRP stimulation of iNOS and NO release from trigeminal ganglion glial cells involves mitogen-activated protein kinase pathways. J Neurochem 2009, 110: 811–821. 10.1111/j.1471-4159.2009.06154.x
Anderson LE, Seybold VS: Calcitonin gene-related peptide regulates gene transcription in primary afferent neurons. J Neurochem 2004, 91: 1417–1429. 10.1111/j.1471-4159.2004.02833.x
Latremoliere A, Woolf CJ: Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 2009, 10: 895–926. 10.1016/j.jpain.2009.06.012
Hargreaves R: New migraine and pain research. Headache 2007,47(Suppl 1):S26–43. 10.1111/j.1526-4610.2006.00675.x
Seger R, Krebs E: The MAPK signaling cascade. FASEB J 1995, 9: 726–735.
Shanley TP: Phosphatases: Counterregulatory role in inflammatory cell signaling. Crit Care Med 2002, 30: S80-S88. 10.1097/00003246-200201001-00011
Wang X, Liu Y: Regulation of innate immune response by MAP kinase phosphatase-1. Cell Signal 2007, 19: 1372–1382. 10.1016/j.cellsig.2007.03.013
Wu J, Roth R, Anderson E, Hong E, Lee M, Choi C, Neufer P, Shulman G, Kim J, Bennett A: Mice lacking MAP kinase phophatase-1 have enhanced MAP kinase activity and resistance to diet-induced obesity. Cell Metab 2006, 4: 61–73. 10.1016/j.cmet.2006.05.010
Wang X, Zhao Q, Matta R, Meng X, Liu X, Liu CG, Nelin LD, Liu Y: Inducible nitric-oxide synthase expression is regulated by mitogen-activated protein kinase phosphatase-1. J Biol Chem 2009, 284: 27123–27134. 10.1074/jbc.M109.051235
Zhao Q, Wang X, Nelin LD, Yao Y, Matta R, Manson ME, Baliga RS, Meng X, Smith CV, Bauer JA, et al.: MAP kinase phosphatase 1 controls innate immune responses and suppresses endotoxic shock. J Exp Med 2006, 203: 131–140. 10.1084/jem.20051794
Li L, Chen SF, Liu Y: MAP kinase phosphatase-1, a critical negative regulator of the innate immune response. Int J Clin Exp Med 2009, 2: 48–67.
Newman DJ, Cragg GM: Natural products as sources of new drugs over the last 25 years. J Nat Prod 2007, 70: 461–477. 10.1021/np068054v
Vuorelaa P, Leinonenb M, Saikkuc P, Tammelaa P, Rauhad JP, Wennberge T, Vuorela H: Natural products in the process of finding new drug candidates. Curr Med Chem 2004, 11: 1375–1389.
Wang J, Ho L, Zhao W, Ono K, Rosensweig C, Chen L, Humala N, Teplow DB, Pasinetti GM: Grape-derived polyphenolics prevent Abeta oligomerization and attenuate cognitive deterioration in a mouse model of Alzheimer's disease. J Neurosci 2008, 28: 6388–6392. 10.1523/JNEUROSCI.0364-08.2008
Milligan ED, Twining C, Chacur M, Biedenkapp J, O'Connor K, Poole S, Tracey K, Martin D, Maier SF, Watkins LR: Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats. J Neurosci 2003, 23: 1026–1040.
Tsuda M, Mizokoshi A, Shigemoto-Mogami Y, Koizumi S, Inoue K: Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 2004, 45: 89–95. 10.1002/glia.10308
Cady RJ, Durham PL: Cocoa-enriched diets enhance expression of phosphatases and decrease expression of inflammatory molecules in trigeminal ganglion neurons. Brain Res 2010, 6: 1323. 18–32
Clark A: MAP kinase phosphatase 1: a novel mediator of biological effects of glucocorticoids. J Endocrinol 2003, 178: 5–12. 10.1677/joe.0.1780005
Eljaschewitsch E, Witting A, Mawrin C, Lee T, Schmidt PM, Wolf S, Hoertnagl H, Raine CS, Schneider-Stock R, Nitsch R, Ullrich O: The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells. Neuron 2006, 49: 67–79. 10.1016/j.neuron.2005.11.027
Reddington M, Priller J, Treichel J, Haas C, Kreutzberg GW: Astrocytes and microglia as potential targets for calcitonin gene related peptide in the central nervous system. Can J Physiol Pharmacol 1995, 73: 1047–1049.
Seybold VS: The role of peptides in central sensitization. Handb Exp Pharmacol 2009, 194: 451–491. full_text
Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R: PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 2003, 6: 136–143. 10.1038/nn997
Le Greves P, Nyberg F, Terenius L, Hokfelt T: Calcitonin gene-related peptide is a potent inhibitor of substance P degradation. Eur J Pharmacol 1985, 115: 309–311. 10.1016/0014-2999(85)90706-X
Simonetti M, Giniatullin R, Fabbretti E: Mechanisms mediating the enhanced gene transcription of P2X3 receptor by calcitonin gene-related peptide in trigeminal sensory neurons. J Biol Chem 2008, 283: 18743–18752. 10.1074/jbc.M800296200
Burnstock G: Purinergic receptors and pain. Curr Pharm Des 2009, 15: 1717–1735. 10.2174/138161209788186335
Xin WJ, Weng HR, Dougherty PM: Plasticity in expression of the glutamate transporters GLT-1 and GLAST in spinal dorsal horn glial cells following partial sciatic nerve ligation. Mol Pain 2009, 5: 15. 10.1186/1744-8069-5-15
Gao YJ, Ji RR: Chemokines, neuronal-glial interactions, and central processing of neuropathic pain. Pharmacol Ther 2010, 126: 56–68. 10.1016/j.pharmthera.2010.01.002
Ji RR, Suter MR: p38 MAPK, microglial signaling, and neuropathic pain. Mol Pain 2007, 3: 33. 10.1186/1744-8069-3-33
Suzuki I, Harada T, Asano M, Tsuboi Y, Kondo M, Gionhaku N, Kitagawa J, Kusama T, Iwata K: Phosphorylation of ERK in trigeminal spinal nucleus neurons following passive jaw movement in rats with chronic temporomandibular joint inflammation. J Orofac Pain 2007, 21: 225–231.
Thut P, Hermanstyne T, Flake N, Gold M: An operant conditioning model to assess changes in feeding behavior associated with temporomandibular joint inflammation in the rat. J Orofacial Pain 2007, 21: 7–18.
Raghavendra V, Tanga FY, DeLeo JA: Complete Freunds adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS. Eur J Neurosci 2004, 20: 467–473. 10.1111/j.1460-9568.2004.03514.x
Ren K, Dubner R: Neuron-glia gets serious: role in pain hypersensitivity. Curr Op in Anaesthesiology 2008, 21: 570–579. 10.1097/ACO.0b013e32830edbdf
Aloisi F: The role of microglia and astrocytes in CNS immune surveillance and immunopathology. Adv Exp Med Biol 1999, 468: 123–133.
Miller RJ, Jung H, Bhangoo SK, White FA: Cytokine and chemokine regulation of sensory neuron function. Handb Exp Pharmacol 2009, 194: 417–449. full_text
Eliasson C, Sahlgren C, Berthold CH, Stakeberg J, Celis JE, Betsholtz C, Eriksson JE, Pekny M: Intermediate filament protein partnership in astrocytes. J Biol Chem 1999, 274: 23996–24006. 10.1074/jbc.274.34.23996
Lynch MA: The multifaceted profile of activated microglia. Mol Neurobiol 2009, 40: 139–156. 10.1007/s12035-009-8077-9
Davies AJ, Kim YH, Oh SB: Painful Neuron-Microglia Interactions in the Trigeminal Sensory System. The Open Pain Journal 2010, 3: 14–28. 10.2174/1876386301003020014
Yamazaki Y, Ren K, Shimada M, Iwata K: Modulation of paratrigeminal nociceptive neurons following temporomandibular joint inflammation in rats. Exp Neurol 2008, 214: 209–218. 10.1016/j.expneurol.2008.08.005
Ambalavanar R, Yallampalli C, Yallampalli U, Dessem D: Injection of adjuvant but not acidic saline into craniofacial muscle evokes nociceptive behaviors and neuropeptide expression. Neuroscience 2007, 149: 650–659. 10.1016/j.neuroscience.2007.07.058
Durham PL, Garrett FG: Neurological mechanisms of migraine: potential of the gap-junction modulator tonabersat in prevention of migraine. Cephalalgia 2009,29(Suppl 2):1–6. 10.1111/j.1468-2982.2009.01976.x
Garrett FG, Durham PL: Differential expression of connexins in trigeminal ganglion neurons and satellite glial cells in response to chronic or acute joint inflammation. Neuron Glia Biol 2008, 4: 295–306. 10.1017/S1740925X09990093