Emerging importance of neuron-satellite glia interactions within trigeminal ganglia in craniofacial pain

Open Pain Journal

Volumn 3, Issue 1, 2010, Pages 3-13

  Durham, P L ^a   Garrett, F G ^a  

^a MISSOURI STATE UNIVERSITY   (United States)

Author keywords

Acute; Chronic; Comorbitity; Gap junctions connexins; Inflammation; Migraine; Neuron; Neuropathic; Peripheral sensitization; Rhinosinusitus; Satellite glia; Signaling; Tmj; Trigeminal

Indexed keywords

GAP JUNCTION PROTEIN;

ARTICLE; CELL INTERACTION; COMORBIDITY; CRANIOFACIAL PAIN; FACE PAIN; GAP JUNCTION; GLIA; HEADACHE; HUMAN; INFLAMMATION; MIGRAINE; NERVE CELL; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHINOSINUSITIS; TEMPOROMANDIBULAR JOINT DISORDER; TOOTH PAIN; TRIGEMINAL NERVE; TRIGEMINUS GANGLION; TRIGEMINUS NEURALGIA;

EID: 77953772783     PISSN: None     EISSN: 18763863     Source Type: Journal    
DOI: 10.2174/1876386301003010003     Document Type: Article

References (118)

1. Sessle B. The neurobiology of facial and dental pain: Present knowledge, future directions. J Dent Res 1987; 66: 962-981.
2. Lipton JA, Ship JA, Larach-Robinson D. Estimated prevalence and distribution of reported orofacial pain in the united states. J Am Dent Assoc 1993; 124: 115-121.
3. Carlsson G, LeResche L. Epidemiology of temporomandibular disorders. In: Sessle, Bryant PS, Dionne, RA (Eds). Temporoman-dibular disorders and related pain conditions. Progress in pain research and management, IASP Press, Seattle, 1995, pp. 211-226.
4. Shankland W. The trigeminal nerve. Part i: An over-view. Cranio 2000; 18: 238-248.
5. Lazarov N. Comparative analysis of the chemical neuroanatomy of the mammalian trigeminal ganglion and mesencephalic trigeminal nucleus. Prog Neurobiol 2002; 66: 19-59.
6. Devor M. Unexplained peculiarities of the dorsal root ganglion. Pain 1999; Suppl 6: S27-35.
7. Hanani M. Satellite glial cells in sensory ganglia: From form to function. Brain Res Rev 2005; 48: 457-476.
8. Garbay B, Heape A, Sarqueil F, et al. Myelin synthesis in the peripheral nervous system. Prog Neurobiol 2000; 61: 267-304.
9. Huang T, Belzer V, Hanani M. Gap junctions in dorsal root ganglia: Possible contribution to visceral pain. Eur J Pain 2010; 49: e1-11.
10. Hanani M, Huang T, Cherkas P, et al. Glial cell plasticity in sensory ganglia induced by nerve damage. Neuroscience 2002; 114: 279-283.
11. Cherkas P, Huang T, Pannicke T, et al. The effects of axotomy on neurons and satellite glial cells in mouse trigeminal ganglion. Pain 2004; 110: 290-298.
12. Dublin P, Hanani M. Satellite glial cells in sensory ganglia: Their possible contribution to inflammatory pain. Brain Behav Immun 2007; 21: 592-598.
13. Goldberg GS, Lampe PD, Nicholson BJ. Selective transfer of endogenous metabolites through gap junctions composed of different connexins. Nat Cell Biol 1999; 1: 457-459.
14. Goldberg G, Moreno A, Lampe P. Gap junctions between cells expressing connexin 43 or 32 show inverse permselectivity to adenosine and atp. J Bio Chem 2002; 277: 36725-36730.
15. White T, Bruzzone R. Multiple connexin proteins in single intercellular channels: Connexin compatibility and functional consequences. J Bioenerg Biomembr 1996; 28: 339-350.
16. Beyer E, Davis L, Saffitz J, et al. Cardiac intercellular communication: Consequences of connexin distribution and diversity. Braz J Med Biol Res 1995; 4: 415-425.
17. Laird D. Life cycle of connexins in health and disease. Biochem J 2006; 394: 527-543.
18. Fallon R, Goodenough D. Five-hour half-life of mouse liver gap-junction protein. J Cell Biol 1981; 90: 521-526.
19. Beardslee M, Laing J, Beyer E, et al. Rapid turnover of connexin43 in the adult rat heart. Circ Res 1998; 83: 629-635.
20. Bukauskas F, Jordan K, Bukauskiene A, et al. Clustering of connexin 43-enhanced green flourescent protein gap junction channels and functional coupling in living cells. Proc Natl Acad Sci USA 2000; 97: 2556-2561.
21. Nagy J, Dudek F, Rash J. Update on connexins and gap junctions in neurons and glia in the mammalian nervous system. Brain Res Rev 2004; 47: 191-215.
22. Ebihara L. New roles for connexons. News Physiol Sci 2003; 18: 100-103.
23. Goodenough D, Goliger J, Paul D. Connexins, connexons, and intercellular communication. Annu Rev Biochem 1996; 65: 475-502.
24. Saez J, Berthoud V, Branes M, et al. Plasma membrane channels formed by connexins: Their regulation and function. Physiol Rev 2003; 83: 1359-1400.
25. Rouach N, Avignone E, Meme W, et al. Gap junctions and connexin expression in the normal and pathological central nervous system. Biol Cell 2002; 94: 457-475.
26. Alvarez-Maubecin V, Garcia-Hernandez F, Williams J, et al. Functional coupling between neurons and glia. J Neurosci 2000; 20: 4091-4098.
27. Venance L, Prémont J, Glowinski J, et al. Gap junctional communication and pharmacological heterogeneity in astrocytes cultured from the rat striatum. J Physiol 1998; 510: 429-440.
28. Mobbs P, Brew H, Attwell D. A quantitative analysis of glial cell coupling in the retina of the axolotl (ambystoma mexicanum). Brain Res 1998; 460: 235-245.
29. Holthoff K, Witte O. Directed spatial potassium redistribution in rat neocortex. Glia 2000; 29: 288-292.
30. Rose C, Ransom B. Gap junctions equalize intracellular na+ concentration in astrocytes. Glia 1997; 20: 299-307.
31. Vit J, Jasmin L, Bhargava A, et al. Satellite glial cells in the trigeminal ganglion as a determinant of orofacial neuropathic pain. Neuron Glia Biol 2006; 2: 247-257.
32. Ohara P, Vit J, Bhargava A, et al. Evidence for a role of connexin 43 in trigeminal pain using rna interference in vivo. J Neurophys 2008; 100: 3064-3073.
33. Amir R, Devor M. Extra spike formation in sensory neurons and the disruption of afferent spike patterning. Biophys J 2003; 84: 2700-2708.
34. Amir R, Devor M. Electrical excitability of the soma of sensory neurons is required for spike invasion of the soma, but not for through-conduction. Biophys J 2003; 84: 2181-2191.
35. Robinson P, Boissonade F, Loescher A, et al. Peripheral mechanisms for the initiation of pain following trigeminal nerve injury. J Orofac Pain 2004; 18: 287-292.
36. Vit JP, Ohara PT, Bhargava A, et al. Silencing the kir4.1 potassium channel subunit in satellite glial cells of the rat trigeminal ganglion results in pain-like behavior in the absence of nerve injury. J Neurosci 2008; 28: 4161-4171.
37. Kucheryavykh Y, Kucheryavykh L, Nichols C, et al. Downregulation of kir4.1 inward rectifying potassium channel subunits by rnai impairs potassium transfer and glutamate uptake by cultured cortical astrocytes. Glia 2007; 55: 274-281.
38. Djukic B, Casper K, Philpot B, et al. Conditional knock-out of kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. J Neurosci 2007; 27: 11354-11365.
39. Olsen M, Sontheimer H. Functional implications for kir4.1 channels in glial biology: From k+ buffering to cell differentiation. J Neurochem 2008; 107: 589-601.
40. Vit J, Ohara P, Sundberg C, et al. Adenovector gad65 gene delivery into the rat trigeminal ganglion produces orofacial analgesia. Mol Pain 2009; 5: 42.
41. Naik A, Pathirathna S, Jevtovic-Todorovic V. Gabaa receptor modulation in dorsal root ganglia in vivo affects chronic pain after nerve injury. Neuroscience 2008; 154: 1539-1553.
42. Dodick D, Silberstein S. Central sensitization theory of migraine: Clinical implications. Headache 2006; 46: S182-191.
43. Watkins L, Milligan E. Maier S. Glial activation: A driving force for pathological pain. Trends Neurosci 2001; 24: 450-455.
44. 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.
45. Thalakoti S, Patil V, Damodaram S, et al. Neuron-glia signaling in trigeminal ganglion: Implications for migraine pathology. Headache 2007; 47: 1008-1023.
46. Caterina M, Schumacher M, Tominaga M, et al. The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature 1997; 389: 816-824.
47. Pietrobon D, Striessnig J. Neurobiology of migraine. Nat Rev Neurosci 2003; 4: 386-398.
48. Blomstrand F, Aberg N, Eriksson P, et al. Extent of intercellular calcium wave propagation is related to gap junction permeability and level of connexin-43 expression in astrocytes in primary cultures from four brain regions. Neuroscience 1999; 92: 255-265.
49. Garcia-Hirschfeld J, Lopez-Briones L, Belmonte C, et al. Intracellular free calcium responses to protons and capsaicin in cultured trigeminal neurons. Neuroscience 1995; 67: 235-243.
50. Donato R. S100: A multigenic family of calcium-modulated proteins of the ef-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 2001; 33: 637-668 Review.
51. Liu L, Li Y, Van Eldik LJ, et al. S100b-induced microglial and neuronal il-1 expression is mediated by cell type-specific transcription factors. J Neurochem 2005; 92: 546-553.
52. Lue LF, Walker DG, Brachova L, et al. Involvement of microglial receptor for advanced glycation endproducts (rage) in alzheimer's disease: Identification of a cellular activation mechanism. Exp Neurol 2001; 171: 29-45.
53. Marenholz I, Heizmann CW, Fritz G. S100 proteins in mouse and man: From evolution to function and pathology (including an update of the nomenclature). Biochem Biophys Res Commun 2004; 322: 1111-1122.
54. Cheng J, Ji R. Intracellular signaling in primary sensory neurons and persistent pain. Neurochem Res 2008; 33: 1970-1978.
55. Oh EJ, Weinreich D. Chemical communication between vagal afferent somata in nodose ganglia of the rat and the guinea pig in vitro. J Neurophysiol 2002; 87: 2801-2807.
56. Ulrich-Lai YM, Flores CM, Harding-Rose CA, et al. Capsaicin-evoked release of immunoreactive calcitonin gene-related peptide from rat trigeminal ganglion: Evidence for intraganglionic neurotransmission. Pain 2001 91: 219-226.
57. Amir R, Devor M. Chemically mediated cross-excitation in rat dorsal root ganglia. J Neurosci 1996; 16: 4733-4741.
58. Amir R, Devor M. Functional cross-excitation between afferent a-and c-neurons in dorsal root ganglia. Neuroscience 2000; 95: 189-195.
59. Ji RR. Peripheral and central mechanisms of inflammatory pain, with emphasis on map kinases. Curr Drug Targets Inflamm Allergy 2004; 3: 299-303.
60. Ji R. Mitogen-activated protein kinases as potential targets for pain killers. Curr Opin Investig Drugs 2004; 5: 71-75.
61. Hargreaves RJ, Shepheard SL. Pathophysiology of migraine-new insights. Can J Neurol Sci 1999; 26 Suppl 3: S12-19.
62. Buzzi M. Trigeminal pain pathway: Peripheral and central activation as experimental models of migraine. Func Neurol 2001; 16: 77-81.
63. Holmlund A, Ekblom A, Hansson P, et al. Concentration of neuropeptide substance - p, neurokinin a, calcitonin gene related peptide, neuropeptide y and vasoactive intestinal polypeptide in the synovial fluid of the -human temporomandibular joint. Int J Oral Maxillofac Surg 1991; 20: 228-231.
64. Appelgren A, Appelgren B, Kopp S, et al. Relation between intra-articular temperature of the arthritic temporomandibular joint and presence of calcitonin gene-related peptide in the joint fluid. A clinical study. Acta Odontol Scand 1993; 51: 285-291.
65. Zhang X, Chen Y, Wang C, et al. Neuronal somatic atp release triggers neuron-satellite glial cell communication in dorsal root ganglia. Proc Nat Acad Sci 2007; 104: 9864-9869.
66. Neubert JK, Maidment NT, Matsuka Y, et al. Inflammation-induced changes in primary afferent-evoked release of substance p within trigeminal ganglia in vivo. Brain Res 2000; 871: 181-191.
67. Li J, Vause C, Durham P. Calcitonin gene-related peptide stimulation of nitric oxide synthesis and release from trigeminal ganglion glial cells. Brain Res 2008; 1196: 22-32.
68. Zhang Z, Winborn C, Marquez de Prado B, et al. Sensitization of calcitonin gene-related peptide receptors by receptor activity-modifying protein-1 in the trigeminal ganglion. J Neurosci 2007; 27: 2693-2703.
69. Purkiss J, Welch M, Doward S, et al. Capsaicin-stimulated release of substance p from cultured dorsal root ganglion neurons: Involvement of two distinct mechanisms. Biochem Pharmacol 2000; 59: 1403-1406.
70. Durham P, Cady R, Cady R. Regulation of calcitonin gene-related peptide secretion from trigeminal nerve cells by botulinum toxin type a: Implications for migraine therapy. Headache 2004; 44: 35-42.
71. Rothwell N, Hopkins S. Cytokines and the nervous system ii: Actions and mechanisms of action. Trends Neurosci 1995; 18: 130-136.
72. Vitkovic L, Bockaert J, Jacque C. Inflammatory Cytokines: Neuromodulators in normal brain? J Neurochem 2000; 74: 457-471.
73. Capuano A, De Corato A, Lisi L, et al. Proinflammatory-activated trigeminal satellite cells promote neuronal sensitization: Relevance for migraine pathology. Mol Pain 2009; 5: 43.
74. Fabbretti E, D'Arco M, Fabbro A, et al. Delayed upregulation of atp p2x3 receptors of trigeminal sensory neurons by calcitonin gene-related peptide. J Neurosci 2006; 26: 6163-6171.
75. Suadicani S, Cherkas P, Zuckerman J, et al. Bidirectional calcium signaling between satellite glial cells and neurons in cultured mouse trigeminal ganglia. Neuron Glia Biol 2009; 6: 1-9.
76. Cady R, Schreiber C. Sinus headache or migraine? Considerations in making a differential diagnosis. Neurology 2002; 58: S10-14.
77. Schreiber C, Hutchinson S, Webster C, et al. Prevalence of migraine in patients with a history of self-reported or physician-diagnosed Sinus Headache. Arch Intern Med 2004; 164: 1769-1772.
78. Cady R, Schreiber C, Farmer K. Understanding the patient with migraine: The evolution from episodic headache to chronic neurologic disease. A proposed classification of patients with headache. Headache 2004; 44: 426-435.
79. Schreiber C, Hutchinson S, Webster C, et al. Prevalence of migraine in patients with a history of self-reported or physician-diagnosed Sinus Headache. Arch Intern Med 2004; 164: 1769-1772.
80. Ku M, Silverman B, Prifti N, et al. Prevalence of migraine headaches in patients with allergic rhinitis. Ann Allergy Asthma Immunol 2006; 97: 226-230.
81. Damodaram S, Thalakoti S, Freeman SE, et al. Tonabersat inhibits trigeminal ganglion neuronal-satellite glial cell signaling. Headache 2009; 49: 5-20.
82. Bensch G, Nelson H, Borish L. Evaluation of cytokines in nasal secretions after nasal antigen challenge: Lack of influence of antihistamines. Ann Allergy Asthma Immunol 2002; 88: 457-462.
83. Repka-Ramirez S, Naranch K, Park Y, et al. Cytokines in nasal lavage fluids from acute sinusitis, allergic rhinitis, and chronic fatigue syndrome subjects. Allergy Asthma Proc 2002; 23: 185-190.
84. Bachert C, Wagenmann M, Hauser U. Proinflammatory cytokines: Measurement in nasal secretion and induction of adhesion receptor expression. Int Arch Allergy Immunol 1995; 107: 106-108.
85. Bradding P, Mediwake R, Feather I, et al. Tnf alpha is localized to nasal mucosal mast cells and is released in acute allergic rhinitis. Clin Exp Allergy 1995; 25: 406-415.
86. Pietrobon D. Migraine: New molecular mechanisms. Neuroscientist 2005; 11: 373-386.
87. Morch C, Hu J, Arendt-Nielsen L, et al. Convergence of cutaneous, musculoskeletal, dural and visceral afferents onto nocicpetive neurons in the first cervical dorsal horn. Eur J Neurosci 2007; 26: 142-154.
88. Piovesan E, Kowacs P, Oshinsky M. Convergence of cervical and trigeminal sensory afferents. Curr Pain Headache Rep 2003; 7: 377-383.
89. Freeman S, Patil V, Durham P. Nitric oxide-proton stimulation of trigeminal ganglion neurons increases mitogen-activated protein kinase and phosphatase expression in neurons and satellite glial cells. Neuroscience 2008; 157: 542-555.
90. Arinci A, Ademoglu E, Aslan A, et al. Molecular correlates of temporomandibular joint disease. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2005; 99: 666-670.
91. Takahashi T, Kondoh T, Ohtani M, et al. Association between arthroscopic diagnosis of temporomandibular joint osteoarthritis and synovial fluid nitric oxide levels. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1999; 88: 129-136.
92. Ichikawa H, Sugimoto T. The co-expression of asic3 with calcitonin gene-related peptide and parvalbumin in the rat trigeminal ganglion. Brain Res 2002; 943: 287-291.
93. Tanimoto T, Takeda M, Nasu M, et al. Immunohistochemical co-expression of carbonic anhydrase ii with kv1.4 and trpv1 in rat small-diameter trigeminal ganglion neurons. Brain Res 2005; 1044: 262-265.
94. Bae Y, Oh J, Hwang S, et al. Expression of vanilloid receptor trpv1 in the rat trigeminal sensory nuclei. J Comp Neurol 2004; 478: 62-71.
95. Diogenes A, Patwardhan A, Jeske N, et al. Prolactin modulates trpv1 in female rat trigeminal sensory neurons. J Neurosci 2006; 26: 8126-8136.
96. Durham P, Russo A. Stimulation of the calcitonin gene-related peptide enhancer by mitogen-activated protein kinases and repression by an antimigraine drug in trigeminal ganglia neurons. J Neurosci 2003; 23: 807-815.
97. 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.
98. Kaminska B. Mapk signaling pathways as molecular targets for anti inflammatory therapy-from molecular mechanisms to therapeutic benefits. Biochem Biophsy Acta 2005; 1754: 253-262.
99. Schindler J, Monahan J, Smith W. P38 pathway kinases as anti-inflammatory drug targets. J Dent Res 2007; 86: 800-811.
100. Alstergren P. Cytokines in temporomandibular joint arthritis. Oral Dis 2000; 6: 331-334.
101. Nishimura M, Segami N, Keneyama K, et al. Proinflammatory cytokines and arthroscopic findings of patients with internal derangement and osteoarthritis of temporomandibular joint. Br J Oral Maxillofac Surg 2002; 40: 68-71.
102. Takeda M, Tanimoto T, Kadoi J, et al. Enhanced excitability of nociceptive trigeminal ganglion neurons by satellite glial cytokine following peripheral inflammation. Pain 2007; 129: 155-166.
103. Wang X, Liu Y. Regulation of innate immune response by map kinase phosphatase-1. Cell Signal 2007; 19: 1372-1382.
104. 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 2009; 1-12.
105. Suzuki I, Harada T, Asano M, et al. 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.
106. Thut P, Hermanstyne T, Flake N, et al. 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.
107. Wang S, Lim G, Mao J, et al. Regulation of the trigeminal nr1 subunit expression induced by inflammation of the temporoman-dibular joint region in rats. Pain 2008; 10: 1-7.
108. Xu Q, Garraway S, Weyerbacher A, et al. Activation of the neuronal extracellular signal-regulated kinase 2 in the spinal cord dorsal horn is required for complete freund's adjuvant-induced pain hypersensitivity. J Neurosci 2008; 28: 14087-14096.
109. Nakase T, Naus C. Gap junctions and neurological disorders of the central nervous system. Biochim Biophys Acta 2004; 1662: 149-158.
110. Schock S, Leblanc D, Hakim A, et al. Atp release by way of connexin 36 hemichannels mediates ischemic tolerance in vitro. Biochem Biophys Res Commun 2008; 368: 138-144.
111. Toma I, Bansal E, Meer EJ, et al. Connexin 40 and atp-dependent intercellular calcium wave in renal glomerular endothelial cells. Am J Physiol Regul Integr Comp Physiol 2008; 294: R1769-1776.
112. Cheriann P, Siller-Jackson A, Gu S, et al. Mechanical strain opens connexin 43 hemichannels in osteocytes: A novel mechanism for the release of prostaglandin. Mol Biol Cell 2005; 16: 3100-3106.
113. Bruzzone S, Guida L, Zocchi E, Franco L, De Flora A. Connexin 43 hemi channels mediate ca2+-regulated transmembrane nad+ fluxes in intact cells. FASEB J 2001; 15: 10-12.
114. Bennett M, Contreras JE, Bukauskas FF, Sáez JC. New roles for astrocytes: Gap junction hemichannels have something to communicate. Trends Neurosci 2003; 26: 610-617.
115. Ebihara L. New roles for connexins. News Physiol Sci 2003; 18: 100-103.
116. Ye Z, Wyeth MS, Baltan-Tekkok S, Ransom BR. Functional hemichannels in astrocytes: A novel mechanism of glutamate release. J Neurosci 2003; 23: 3588-3596.
117. Hucho T, Levine JD. Signaling pathways in sensitization: Toward a nociceptor cell biology. Neuron 2007; 55: 365-376.
118. Watkins L, Maier S. Beyond neurons: Evidence that immune and glial cells contribute to pathological pain states. Physiol Rev 2002; 82: 981-1011.