Hostname: page-component-848d4c4894-x24gv Total loading time: 0 Render date: 2024-06-12T06:15:02.841Z Has data issue: false hasContentIssue false
  • English
  • Français

Development of functional units within trigeminal ganglia correlates with increased expression of proteins involved in neuron–glia interactions

Published online by Cambridge University Press:  16 December 2010

Paul L. Durham  and
F.G. Garrett
Paul L. Durham*
Affiliation:
Center for Biomedical and Life Sciences, Missouri State University, Springfield, MO, USA
F.G. Garrett
Affiliation:
Center for Biomedical and Life Sciences, Missouri State University, Springfield, MO, USA
*
Correspondence should be addressed to: Paul L. Durham, Missouri State University, 524 N Boonville Avenue, Springfield, MO 65806, USA phone: 417-836-4869 fax: 417-836-7602 email: pauldurham@missouristate.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Cell bodies of trigeminal nerves, which are located in the trigeminal ganglion, are completely surrounded by satellite glial cells and together form a functional unit that regulates neuronal excitability. The goals of this study were to investigate the cellular organization of the rat trigeminal ganglia during postnatal development and correlate those findings with expression of proteins implicated in neuron–glia interactions. During postnatal development there was an increase in the volume of the neuronal cell body, which correlated with a steady increase in the number of glial cells associated with an individual neuron from an average of 2.16 at birth to 7.35 on day 56 in young adults. Interestingly, while the levels of the inwardly rectifying K+ channel Kir4.1 were barely detectable during the first week, its expression in satellite glial cells increased by day 9 and correlated with initial formation of functional units. Similarly, expression of the vesicle docking protein SNAP-25 and neuropeptide calcitonin gene-related peptide was readily detected beginning on day 9 and remained elevated throughout postnatal development. Based on our findings, we propose that the expression of proteins involved in facilitating neuron–glia interactions temporally correlates with the formation of mature functional units during postnatal development of trigeminal ganglion.

Keywords

Kir4.1CGRPSNAP-25
Type
Research Article
Information
Neuron Glia Biology , Volume 6 , Issue 3 , August 2010 , pp. 171 - 181
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Altman, J. and Bayer, S.A. (1982) Development of the cranial nerve ganglia and related nuclei in the rat. Advances in Anatomy, Embryology, and Cell Biology 74, 1–90.CrossRefGoogle ScholarPubMed
Amir, R. and Devor, M. (1996) Chemically mediated cross-excitation in rat dorsal root ganglia. Journal of Neuroscience 16, 4733–4741.CrossRefGoogle ScholarPubMed
Amir, R. and Devor, M. (2000) Functional cross-excitation between afferent A- and C-neurons in dorsal root ganglia. Neuroscience 95, 189–195.CrossRefGoogle ScholarPubMed
Amir, R. and Devor, M. (2003a) Electrical excitability of the soma of sensory neurons is required for spike invasion of the soma, but not for through-conduction. Biophysics Journal 84, 2181–2191.CrossRefGoogle Scholar
Amir, R. and Devor, M. (2003b) Extra spike formation in sensory neurons and the disruption of afferent spike patterning. Biophysics Journal 84, 2700–2708.CrossRefGoogle ScholarPubMed
Bachert, C., Wagenmann, M. and Hauser, U. (1995) Proinflammatory cytokines: measurement in nasal secretion and induction of adhesion receptor expression. International Archives of Allergy and Immunology 107, 106–108.CrossRefGoogle ScholarPubMed
Bensch, G., Nelson, H. and Borish, L. (2002) Evaluation of cytokines in nasal secretions after nasal antigen challenge: lack of influence of antihistamines. Annals of Allergy, Asthma and Immunology 88, 457–462.CrossRefGoogle ScholarPubMed
Bradding, P., Mediwake, R., Feather, I., Madden, J., Church, M., Holgate, S. et al. (1995) TNF alpha is localized to nasal mucosal mast cells and is released in acute allergic rhinitis. Clinical and Experimental Allergy 25, 406–415.CrossRefGoogle ScholarPubMed
Britsch, S., Goerich, D.E., Riethmacher, D., Peirano, R.I., Rossner, M., Nave, K.A. et al. (2001) The transcription factor Sox10 is a key regulator of peripheral glial development. Genes and Development 15, 66–78.CrossRefGoogle ScholarPubMed
Cady, R. and Schreiber, C. (2002) Sinus headache or migraine? Considerations in making a differential diagnosis. Neurology 58, S10–S14.CrossRefGoogle ScholarPubMed
Cady, R.J. and Durham, P.L. (2010) Cocoa-enriched diets enhance expression of phosphatases and decrease expression of inflammatory molecules in trigeminal ganglion neurons. Brain Research 1323, 18–23.CrossRefGoogle ScholarPubMed
Capuano, A., De Corato, A., Lisi, L., Tringali, G., Navarra, P. and Dello Russo, C. (2009) Proinflammatory-activated trigeminal satellite cells promote neuronal sensitization: relevance for migraine pathology. Molecular Pain 5, 43.CrossRefGoogle ScholarPubMed
Cheng, J. and Ji, R. (2008) Intracellular signaling in primary sensory neurons and persistent pain. Neurochemical Research 33, 1970–1978.CrossRefGoogle ScholarPubMed
Cherkas, P., Huang, T., Pannicke, T., Tal, M., Reichenbach, A. and Hanani, M. (2004) The effects of axotomy on neurons and satellite glial cells in mouse trigeminal ganglion. Pain 110, 290–298.CrossRefGoogle ScholarPubMed
D'Amico-Martel, A. and Noden, D.M. (1983) Contributions of placodal and neural crest cells to avian cranial peripheral ganglia. American Journal of Anatomy 166, 445–468.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
Davies, A.M. (1988) The trigeminal system: an advantageous experimental model for studying neuronal development. Development 103, Suppl, 175–183.CrossRefGoogle ScholarPubMed
Djukic, B., Casper, K., Philpot, B., Chin, L. and McCarthy, K. (2007) Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. Journal of Neuroscience 27, 11354–11365.CrossRefGoogle ScholarPubMed
Dubner, R. (1978) Neurophysiology of pain. Dental Clinics of North America 22, 11–30.Google ScholarPubMed
Durham, P., Cady, R. and Cady, R. (2004) Regulation of calcitonin gene-related peptide secretion from trigeminal nerve cells by botulinum toxin type A: implications for migraine therapy. Headache 44, 35–42.CrossRefGoogle ScholarPubMed
Freeman, S., Patil, V. and Durham, P. (2008) Nitric oxide-proton stimulation of trigeminal ganglion neurons increases mitogen-activated protein kinase and phosphatase expression in neurons and satellite glial cells. Neuroscience 157, 542–555.CrossRefGoogle ScholarPubMed
Hamburger, V. (1961) Experimental analysis of the dual origin of the trigeminal ganglion in the chick embryo. Journal of Experimental Zoology 148, 91–123.CrossRefGoogle ScholarPubMed
Hanani, M. (2005) Satellite glial cells in sensory ganglia: from form to function. Brain Research Reviews 48, 457–476.CrossRefGoogle ScholarPubMed
Jahn, R. and Scheller, R.H. (2006) SNAREs – engines for membrane fusion. Nature Reviews. Molecular Cell Biology 7, 631–643.CrossRefGoogle ScholarPubMed
Ji, R. and Suter, M. (2007) p38 MAPK, microglial signaling, and neuropathic pain. Molecular Pain 3, 33.CrossRefGoogle ScholarPubMed
Kalcheim, C. and Le Douarin, N.M. (1986) Requirement of a neural tube signal for the differentiation of neural crest cells into dorsal root ganglia. Developmental Biology 116, 451–466.CrossRefGoogle ScholarPubMed
Ku, M., Silverman, B., Prifti, N., Ying, W., Persaud, Y. and Schneider, A. (2006) Prevalence of migraine headaches in patients with allergic rhinitis. Annals of Allergy, Asthma and Immunology 97, 226–230.CrossRefGoogle ScholarPubMed
Kucheryavykh, Y., Kucheryavykh, L., Nichols, C., Maldonado, H., Baksi, K., Reichenbach, A. et al. (2007) Downregulation of Kir4.1 inward rectifying potassium channel subunits by RNAi impairs potassium transfer and glutamate uptake by cultured cortical astrocytes. Glia 55, 274–281.CrossRefGoogle ScholarPubMed
Lagares, A., Li, H.Y., Zhou, X.F. and Avendano, C. (2007) Primary sensory neuron addition in the adult rat trigeminal ganglion: evidence for neural crest glio-neuronal precursor maturation. Journal of Neuroscience 27, 7939–7953.CrossRefGoogle ScholarPubMed
Lawson, S.N. (1992) Morphological and biochemical cell types of sensory neurons. In Scott, S.A. (ed) Sensory Neurons. New York: Oxford University Press, pp. 27–59.Google Scholar
Lazarov, N. (2002) Comparative analysis of the chemical neuroanatomy of the mammalian trigeminal ganglion and mesencephalic trigeminal nucleus. Progress in Neurobiology 66, 19–59.CrossRefGoogle ScholarPubMed
Le Douarin, N.M. and Kalcheim, C. (1999) The Neural Crest. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Ledda, M., De Palo, S. and Pannese, E. (2004) Ratios between number of neuroglial cells and number and volume of nerve cells in the spinal ganglia of two species of reptiles and three species of mammals. Tissue Cell 36, 55–62.CrossRefGoogle ScholarPubMed
Li, J., Vause, C. and Durham, P. (2008) Calcitonin gene-related peptide stimulation of nitric oxide synthesis and release from trigeminal ganglion glial cells. Brain Research 1196, 22–32.CrossRefGoogle ScholarPubMed
Lieberman, A.R. (1976) Sensory Ganglia. London: Chapman and Hall.Google Scholar
McGraw, H.F., Nechiporuk, A. and Raible, D.W. (2008) Zebrafish dorsal root ganglia neural precursor cells adopt a glial fate in the absence of neurogenin1. Journal of Neuroscience 28, 12558–12569.CrossRefGoogle ScholarPubMed
Mehta, P., Battenberg, E. and Wilson, M. (1996) SNAP-25 and synaptotagmin involvement in the final Ca2+-dependent triggering of neurotransmitter exocytosis. Proceedings of the National Academy of Sciences of the U.S.A. 93, 10471–10476.CrossRefGoogle Scholar
Morrison, S.J., Perez, S.E., Qiao, Z., Verdi, J.M., Hicks, C., Weinmaster, G. et al. (2000) Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101, 499–510.CrossRefGoogle ScholarPubMed
Neubert, J.K., Maidment, N.T., Matsuka, Y., Adelson, D.W., Kruger, L. and Spigelman, I. (2000) Inflammation-induced changes in primary afferent-evoked release of substance P within trigeminal ganglia in vivo. Brain Research 871, 181–191.CrossRefGoogle ScholarPubMed
Oh, E.J. and Weinreich, D. (2002) Chemical communication between vagal afferent somata in nodose ganglia of the rat and the Guinea pig in vitro. Journal of Neurophysiology 87, 2801–2807.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
Olsen, M. and Sontheimer, H. (2008) Functional implications for Kir4.1 channels in glial biology: from K+ buffering to cell differentiation. Journal of Neurochemistry 107, 589–601.CrossRefGoogle Scholar
Ota, M. and Ito, K. (2003) Induction of neurogenin-1 expression by sonic hedgehog: its role in development of trigeminal sensory neurons. Developmental Dynamics 227, 544–551.CrossRefGoogle ScholarPubMed
Pannese, E. (1960) Observations on the morphology, submicroscopic structure and biological properties of satellite cells (s.c.) in sensory ganglia of mammals. Zeitschrift für Zellforschung und Mikroskopische Anatomie 52, 567–597.CrossRefGoogle ScholarPubMed
Pannese, E. (1964) Number and structure of perisomatic satellite cells of spinal ganglia under normal conditions or during axon regeneration and neuronal hypertrophy. Zeitschrift für Zellforschung und Mikroskopische Anatomie 63, 568–592.CrossRefGoogle ScholarPubMed
Pannese, E. (1969) Electron microscopical study on the development of the satellite cell sheath in spinal ganglia. Journal of Comparative Neurology 135, 381–422.CrossRefGoogle Scholar
Pannese, E. (1974) The histogenesis of the spinal ganglia. Advances in Anatomy, Embryology, and Cell Biology 47, 7–97.Google ScholarPubMed
Pannese, E. (1981) The satellite cells of the sensory ganglia. Advances in Anatomy, Embryology, and Cell Biology 65, 1–111.CrossRefGoogle ScholarPubMed
Pannese, E., Bianchi, R., Calligaris, B., Ventura, R. and Weibel, E.R. (1972) Quantitative relationships between nerve and satellite cells in spinal ganglia. An electron microscopical study. I. Mammals. Brain Research 46, 215–234.CrossRefGoogle ScholarPubMed
Repka-Ramirez, S., Naranch, K., Park, Y., Clauw, D. and Baraniuk, J. (2002) Cytokines in nasal lavage fluids from acute sinusitis, allergic rhinitis, and chronic fatigue syndrome subjects. Allergy and Asthma Proceedings 23, 185–190.Google ScholarPubMed
Robinson, P., Boissonade, F., Loescher, A., Smith, K., Yates, J., Elcock, C. et al. (2004) Peripheral mechanisms for the initiation of pain following trigeminal nerve injury. Journal of Orofacial Pain 18, 287–292.Google ScholarPubMed
Rothwell, N. and Hopkins, S. (1995) Cytokines and the nervous system II: actions and mechanisms of action. Trends in Neurosciences 18, 130–136.CrossRefGoogle ScholarPubMed
Schreiber, C., Hutchinson, S., Webster, C., Ames, M., Richardson, M. and Powers, C. (2004) Prevalence of migraine in patients with a history of self-reported or physician-diagnosed “sinus” headache. Archives of Internal Medicine 164, 1769–1772.CrossRefGoogle ScholarPubMed
Shah, N.M., Groves, A.K. and Anderson, D.J. (1996) Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 85, 331–343.CrossRefGoogle ScholarPubMed
Shah, N.M., Marchionni, M.A., Isaacs, I., Stroobant, P. and Anderson, D.J. (1994) Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77, 349–360.CrossRefGoogle ScholarPubMed
Takeda, M., Takahashi, M. and Matsumoto, S. (2009) Contribution of the activation of satellite glia in sensory ganglia to pathological pain. Neuroscience and Biobehavioral Reviews 33, 784–792.CrossRefGoogle 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 ScholarPubMed
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
Ulrich-Lai, Y.M., Flores, C.M., Harding-Rose, C.A., Goodis, H.E. and Hargreaves, K.M. (2001) Capsaicin-evoked release of immunoreactive calcitonin gene-related peptide from rat trigeminal ganglion: evidence for intraganglionic neurotransmission. Pain 91, 219–226.CrossRefGoogle ScholarPubMed
Vause, C.V. and Durham, P.L. (2010) Calcitonin gene-related peptide differentially regulates gene and protein expression in trigeminal glia cells: findings from array analysis. Neuroscience Letters 473, 163–167.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
Vitkovic, L., Bockaert, J. and Jacque, C. (2000) “Inflammatory” cytokines: neuromodulators in normal brain? Journal of Neurochemistry 74, 457–471.CrossRefGoogle ScholarPubMed
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
Zhang, X., Chen, Y., Wang, C. and Huang, M. (2007a) Neuronal somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia. Proceedings of the National Academy of Sciences of the U.S.A. 104, 9864–9869.CrossRefGoogle ScholarPubMed
Zhang, Z., Winborn, C., Marquez de Prado, B. and Russo, A. (2007b) Sensitization of calcitonin gene-related peptide receptors by receptor activity-modifying protein-1 in the trigeminal ganglion. Journal of Neuroscience 27, 2693–2703.CrossRefGoogle ScholarPubMed
Zimmerman, H. and Braun, N. (1999) Ecto-nucleotidases-molecular structures, catalytic properties, and junctional roles in the nervous system. Progress in Brain Research 120, 371–385.CrossRefGoogle Scholar