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Differential expression of connexins in trigeminal ganglion neurons and satellite glial cells in response to chronic or acute joint inflammation

Published online by Cambridge University Press:  13 August 2009

Filip G. Garrett  and
Paul L. Durham
Filip G. Garrett
Affiliation:
Department of Biology, Missouri State University, Springfield, MO 65897, USA
Paul L. Durham*
Affiliation:
Department of Biology, Missouri State University, Springfield, MO 65897, USA
*
Correspondence should be addressed to: Paul L. Durham, Ph.D., Department of Biology, Missouri State University, Springfield, MO 65897, USA phone: (417) 836-4869 email: pauldurham@missouristate.edu
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Abstract

Trigeminal nerve activation in response to inflammatory stimuli has been shown to increase neuron–glia communication via gap junctions in trigeminal ganglion. The goal of this study was to identify changes in the expression of gap junction proteins, connexins (Cxs), in trigeminal ganglia in response to acute or chronic joint inflammation. Although mRNA for Cxs 26, 36, 40 and 43 was detected under basal conditions, protein expression of only Cxs 26, 36 and 40 increased following capsaicin or complete Freund's adjuvant (CFA) injection into the temporomandibular joint (TMJ). While Cx26 plaque formation between neurons and satellite glia was transiently increased following capsaicin injections, Cx26 plaque formation between neurons and satellite glia was sustained in response to CFA. Interestingly, levels of Cx36 and Cx40 were only elevated in neurons following capsaicin or CFA injections, but the temporal response was similar to that observed for Cx26. In contrast, Cx43 expression was not increased in neurons or satellite glial cells in response to CFA or capsaicin. Thus, trigeminal ganglion neurons and satellite glia can differentially regulate Cx expression in response to the type and duration of inflammatory stimuli, which likely facilitates increased neuron–glia communication during acute and chronic inflammation and pain in the TMJ.

Keywords

Capsaicincomplete Freund's adjuvantgap junctionshemichannelstemporomandibular joint disorders
Type
Research Article
Information
Neuron Glia Biology , Volume 4 , Issue 4 , November 2008 , pp. 295 - 306
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Beardslee, M., Laing, J., Beyer, E. and Saffitz, J. (1998) Rapid turnover of connexin43 in the adult rat heart. Circulation Research 83, 629–635.CrossRefGoogle ScholarPubMed
Bennett, M., Contreras, J., Bukauskas, F. and Sáez, J. (2003) New roles for astrocytes: gap junction hemichannels have something to communicate. Trends in Neuroscience 26, 610–617.CrossRefGoogle ScholarPubMed
Beyer, E., Davis, L., Saffitz, J. and Veenstra, R. (1995) Cardiac intercellular communication: consequences of connexin distribution and diversity. Brazilian Journal of Medical and Biological Research 4, 415–425.Google Scholar
Bruzzone, S., Guida, L., Zocchi, E., Franco, L. and DeFlora, A. (2001) Connexin 43 hemi channels mediate Ca2+-regulated transmembrane NAD+ fluxes in intact cells. FASEB Journal 15, 10–12.CrossRefGoogle ScholarPubMed
Bukauskas, F., Jordan, K., Bukauskiene, A., Bennett, M., Lampe, P., Laird, D. et al. (2000) Clustering of connexin 43-enhanced green fluorescent protein gap junction channels and functional coupling in living cells. Proceedings of the National Academy of Sciences 97, 2556–2561.CrossRefGoogle ScholarPubMed
Carleson, J., Kogner, P., Bileviciute, I., Theodorsson, E., Appelgren, A., Appelgren, B. et al. (1997) Effects of capsaicin in temporomandibular joint arthritis in rats. Archives of Oral Biology 42, 869–876.CrossRefGoogle ScholarPubMed
Carlsson, G. and LeResche, L. (1995) Epidemiology of temporomandibular disorders. In Sessle, B., Bryant, P. and Dionne, R. (eds) Temporomandibular disorders and related pain conditions. Progress in pain research and management. IASP Press, pp. 211–226.Google Scholar
Caterina, M., Schumacher, M., Tominaga, M., Rosen, T. and Julius, D. (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816–824.CrossRefGoogle ScholarPubMed
Chang, Q., Gonzales, M., Pinter, M. and Balice-Gordon, R. (1999) Gap junctional coupling and petterns of connexin expression among neonatal rat lumbar spinal motor neurons. Journal of Neuroscience 19, 10813–10828.CrossRefGoogle ScholarPubMed
Cheriann, P., Siller-Jackson, A., Gu, S., Wang, X., Bonewald, L., Sprague, E. et al. (2005) Mechanical strain opens connexin 43 hemichannels in osteocytes: a novel mechanism for the release of prostaglandin. Molecular Biology of the Cell 16, 3100–3106.CrossRefGoogle Scholar
Condorelli, D., Parenti, R., Spinella, F., Trovato, S., Belluardo, N., Cardile, V. et al. (1998) Cloning of a new gap junction gene (Cx36) highly expressed in mammalian brain neurons. European Journal of Neuroscience 10, 1202–1208.CrossRefGoogle ScholarPubMed
Damodaram, S., Thalakoti, S., Freeman, S.E., Garrett, F.G. and Durham, P.L. (2009) Tonabersat inhibits trigeminal ganglion neuronal–satellite glial cell signaling. Headache 49, 5–20.CrossRefGoogle ScholarPubMed
Dermietzel, R., Gao, Y., Scemes, E., Vieira, D., Urban, M., Kremer, M. et al. (2000) Connexin43 null mice reveal that astrocytes express multiple connexins. Brain Research Brain Research Reviews 32, 45–56.CrossRefGoogle ScholarPubMed
Dodick, D. and Silberstein, S. (2006) Central sensitization theory of migraine: clinical implications. Headache 46, S182–S191.CrossRefGoogle ScholarPubMed
Ebihara, L. (2003) New roles for connexons. News in Physiological Sciences 18, 100–103.Google ScholarPubMed
Fallon, R. and Goodenough, D. (1981) Five-hour half-life of mouse liver gap-junction protein. Journal of Cell Biology 90, 521–526.CrossRefGoogle ScholarPubMed
Goldberg, G., Lampe, P.D. and Nicholson, B.J. (1999) Selective transfer of endogenous metabolites through gap junctions composed of different connexins. Nature Cell Biology 1, 457–459.CrossRefGoogle ScholarPubMed
Goldberg, G., Moreno, A.P. and Lampe, P.D. (2002) Gap junctions between cells expressing connexin 43 or 32 show inverse permselectivity to adenosine and ATP. Journal of Biological Chemistry 277, 36725–36730.CrossRefGoogle ScholarPubMed
Goodenough, D., Goliger, J. and Paul, D. (1996) Connexins, connexons, and intercellular communication. Annual Review of Biochemistry 65, 475–502.CrossRefGoogle ScholarPubMed
Hanani, M. (2005) Satellite glial cells in sensory ganglia: from form to function. Brain Research Reviews 48, 457–476.CrossRefGoogle ScholarPubMed
Haydon, P. (2001) Glia: listening and talking to the synapse. Nature 2, 185–193.Google Scholar
Holthoff, K. and Witte, O. (2000) Directed spatial potassium redistribution in rat neocortex. Glia 29, 288–292.3.0.CO;2-8>CrossRefGoogle ScholarPubMed
Hucho, T. and Levine, J.D. (2007) Signaling pathways in sensitization: toward a nociceptor cell biology. Neuron 55, 365–376.CrossRefGoogle Scholar
Isong, U., Gansky, S. and Plesh, O. (2008) Temporomandibular joint and muscle disorder-type pain in U.S. adults: the National Health Interview Survey. Journal of Orofacial Pain 22, 317–322.Google ScholarPubMed
Laird, D. (2006) Life cycle of connexins in health and disease. Biochemical Journal 394, 527–543.CrossRefGoogle ScholarPubMed
Lipton, J., Ship, J. and Larach-Robinson, D. (1993) Estimated prevalence and distribution of reported orofacial pain in the United States. Journal of the American Dental Association 124, 115–121.CrossRefGoogle ScholarPubMed
Mobbs, P., Brew, H. and Attwell, D. (1998) A quantitative analysis of glial cell coupling in the retina of the axolotl (Ambystoma mexicanum). Brain Research 460, 235–245.CrossRefGoogle Scholar
Nagy, J., Li, X., Rempel, J., Stelmack, G., Patel, D., Staines, W. et al. (2001) Connexin26 in adult rodent central nervous system: demonstration at astrocytic gap junctions and colocalization with connexin30 and connexin43. Journal of Comparative Neurology 441, 302–323.CrossRefGoogle ScholarPubMed
Nakase, T. and Naus, C. (2004) Gap junctions and neurological disorders of the central nervous system. Biochimica et Biophysica Acta 1662, 149–158.CrossRefGoogle ScholarPubMed
Ohara, P., Vit, J., Bhargava, A. and Jasmin, L. (2008) Evidence for a role of connexin 43 in trigeminal pain using RNA interference in vivo. Journal of Neurophysiology 100, 3064–3073.CrossRefGoogle ScholarPubMed
Rash, J., Staines, W., Yasunura, T., Patel, D., Furman, C., Stelmack, G. et al. (2000) Immunogold evidence that neuronal gap junctions in adult rat brain and spinal cord contain connexin-36 but not connexin-32 or connexin-43. Proceedings of the National Academy of Sciences of the U.S.A. 97, 7573–7578.CrossRefGoogle ScholarPubMed
Rose, C. and Ransom, B. (1997) Gap junctions equalize intracellular Na+ concentration in astrocytes. Glia 20, 299–307.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Rouach, N., Avignone, E., Meme, W., Koulakoff, A., Venance, L., Blomstrand, F. et al. (2002) Gap junctions and connexin expression in the normal and pathological central nervous system. Biology of the Cell 94, 457–475.CrossRefGoogle ScholarPubMed
Saez, J., Berthoud, V., Branes, M., Martinez, A. and Byer, E. (2003) Plasma membrane channels formed by connexins: their regulation and function. Physiological Reviews 83, 1359–1400.CrossRefGoogle Scholar
Schock, S., Leblanc, D., Hakim, A. and Thompson, C. (2008) ATP release by way of connexin 36 hemichannels mediates ischemic tolerance in vitro. Biochemical and Biophysical Research Communications 368, 138–144.CrossRefGoogle ScholarPubMed
Sessle, B. (1987) The neurobiology of facial and dental pain: present knowledge, future directions. Journal of Dental Research 66, 962–981.CrossRefGoogle ScholarPubMed
Shankland, W. (2000) The trigeminal nerve. Part I: An over-view. Cranio 18, 238–248.CrossRefGoogle ScholarPubMed
Spears, R., Hutchins, B. and Hinton, R. (1998) Capsaicin application to the temporomandibular joint alters calcitonin gene-related peptide levels in the trigeminal ganglion of the rat. Journal of Orofacial Pain 12, 108–115.Google Scholar
Suzuki, I., Harada, T., Asano, M., Tsuboi, Y., Kondo, M., Gionhaku, N. et al. (2007) Phosphorylation of ERK in trigeminal spinal nucleus neurons following passive jaw movement in rats with chronic temporomandibular joint inflammation. Journal of Orofacial Pain 21, 225–231.Google ScholarPubMed
Takeda, M., Tanimoto, T., Kadoi, J., Nasu, M., Takahashi, M., Kitagawa, J. et al. (2007) Enhanced excitability of nociceptive trigeminal ganglion neurons by satellite glial cytokine following peripheral inflammation. Pain 129, 155–166.CrossRefGoogle Scholar
Thalakoti, S., Patil, V., Damodaram, S., Vause, C., Langford, L., Freeman, S. et al. (2007) Neuron–glia signaling in trigeminal ganglion: implications for migraine pathology. Headache 47, 1008–1023.CrossRefGoogle ScholarPubMed
Thut, P., Hermanstyne, T., Flake, N. and Gold, M. (2007) An operant conditioning model to assess changes in feeding behavior associated with temporomandibular joint inflammation in the rat. Journal of Orofacial Pain 21, 7–18.Google ScholarPubMed
Toma, I., Bansal, E., Meer, E.J., Kang, J.J., Vargas, S.L. and Peti-Peterdi, J. (2008) Connexin 40 and ATP-dependent intercellular calcium wave in renal glomerular endothelial cells. American Journal of Physiology Regulatory, Integrative and Comparative Physiology 294, R1769–R1776.CrossRefGoogle ScholarPubMed
Venance, L., Prémont, J., Glowinski, J. and Giaume, C. (1998) Gap junctional communication and pharmacological heterogeneity in astrocytes cultured from the rat striatum. Journal of Physiology 510, 429–440.CrossRefGoogle ScholarPubMed
Venance, L., Rozov, A., Blatow, M., Burnashev, N., Feldmeyer, D. and Monyer, H. (2000) Connexin expression in electrically coupled postnatal rat brain neurons. Proceedings of the National Academy of Sciences of the U.S.A. 97, 10260–10265.CrossRefGoogle ScholarPubMed
Vit, J., Jasmin, L., Bhargava, A. and Ohara, P. (2006) Satellite glial cells in the trigeminal ganglion as a determinant of orofacial neuropathic pain. Neuron Glia Biology 2, 247–257.CrossRefGoogle ScholarPubMed
Vit, J.P., Ohara, P.T., Bhargava, A., Kelley, K. and Jasmin, L. (2008) 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. Journal of Neuroscience 28, 4161–4171.CrossRefGoogle ScholarPubMed
Wang, S., Lim, G., Mao, J., Backil, S. and Jianren, M. (2008) Regulation of the trigeminal NR1 subunit expression induced by inflammation of the temporomandibular joint region in rats. Pain 10, 1–7.Google Scholar
Watkins, L. and Maier, S. (2002) Beyond neurons: evidence that immune and glial cells contribute to pathological pain states. Physiological Reviews 82, 981–1011.CrossRefGoogle ScholarPubMed
Watkins, L., Milligan, E. and Maier, S. (2001a) Glial activation: a driving force for pathological pain. Trends in Neurosciences 24, 450–455.CrossRefGoogle ScholarPubMed
Watkins, L., Milligan, E. and Maier, S. (2001b) Spinal cord glia: new players in pain. Pain 93, 201–205.CrossRefGoogle ScholarPubMed
White, T. and Bruzzone, R. (1996) Multiple connexin proteins in single intercellular channels: connexin compatibility and functional consequences. Journal of Bioenergetics and Biomembranes 28, 339–350.CrossRefGoogle ScholarPubMed
Wieseler-Frank, J., Maier, S. and Watkins, L. (2004) Glial activation and pathological pain. Neurochemistry International 45, 389–395.CrossRefGoogle ScholarPubMed
Xu, Q., Garraway, S., Weyerbacher, A., Shin, S. and Inturrisi, C. (2008) 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. Journal of Neuroscience 28, 14087–14096.CrossRefGoogle ScholarPubMed
Ye, Z., Wyeth, M., Baltan-Tekkok, S. and Ransom, B. (2003) Functional hemichannels in astrocytes: a novel mechanism of glutamate release. Journal of Neuroscience 23, 3588–3596.CrossRefGoogle ScholarPubMed