Expression of gap junctions bearing connexin-43 subunits and glial fibrillary acidic protein in the rat dorsal root ganglia following hind paw incision

Authors

  • Vishwajit Ravindra Deshmukh Department of Anatomy, All India Institute of Medical Sciences, New Delhi, India
  • Pranav Prasoon Department of Anatomy, All India Institute of Medical Sciences, New Delhi, India
  • Subrata Basu Ray Department of Anatomy, All India Institute of Medical Sciences, New Delhi, India

DOI:

https://doi.org/10.18203/2320-6012.ijrms20164568

Keywords:

Neurotransmitter, Pain, Satellite cells, Surgery

Abstract

Background: Dorsal root ganglion (DRG) neurons mediate the transmission of sensation from the periphery. DRG neurons are pseudounipolar in nature and enveloped by the satellite glial cells (SC). Satellite glial cells have been reported to influence neuronal excitability via gap junctions. Postoperative pain causes induction of various neurotransmitters such as connexin-43 and glial fibrillary acidic protein (GFAP), in the satellite cells surrounding neuronal cell bodies

Objective: To study the expression of connexin-43 and Glial fibrillary acidic protein after hind paw incision.

Methods: Male adult Sprague-Dawley rats (n=12) were used. Rats were randomly divided into two groups. Group I (n=6) and Group II (n=6) for immunohistochemical study with glial fibrillary acidic protein (GFAP) and connexin-43 (Cx-43) respectively. In this study, rats were subjected to noxious stimuli on the right hind paw under general anesthesia. Dorsal root ganglia of both sides (L4 spinal nerves) were isolated after transcardiac fixation with 4% paraformaldehyde. The ganglia from the non-incised side were taken as the control group.

Results: Unipolar neurons in the DRG were surrounded by satellite cells. The satellite cells were positive for GFAP, which showed increased expression on the surgical side after noxious stimuli. Cx-43 immunostaining also showed an increased expression in the periphery of neuronal cell bodies of surgical side representing the location of gap junctions and hyperexcitability of neurons.

Conclusions: Small to medium sized neurons carry pain sensation from the periphery to the central nervous system. Increased gap junctions were noted in small neurons and satellite cells after surgery. Gap junctions might contribute to increased excitability of small neurons in postoperative pain.

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References

Mogensen T, Eliasen K, Ejlersen E, Vegger P, Nielson IK, Kehlet H. Epidural clonidine enhances postoperative analgesia from a combined low dose epidural bupivacaine and morphine regimen, Anesth Analg. 1992;75:607-10.

Zahn EM, Zahn PK, Brennan TJ. Postoperative pain-clinical implications of basic research. Best Pract Res Clin Anaesthesiol. 2007;21(1):3-13.

Pannese E. The satellite cells of sensory ganglia, Adv. Anat. Embryol. Cell Biol. 1981;65:1-111.

Hashizume H, DeLeo JA, Colburn RW, Weinstein JN. Spinal glial activation and cytokine expression after lumbar root injury in the rat. Spine. 2000;25:1206-17.

Ledda M, De Palo S, Pannese E. 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. 2004;36:55-62.

Ozaktay AC, Kallakuri S, Takebayashi T. Effects of interleukin-1 beta, interleukin-6, and tumor necrosis factor on sensitivity of dorsal root ganglion and peripheral receptive fields in rats. Eur Spine J. 2006;15:1529-37.

Haung TY, Belzer V, Hanani M. Gap junctions in dorsal root ganglia: possible contribution to visceral pain. Eur. J. Pain. 2010;14:49. E1-49.e11.

Pannese E, Ledda M, Cherkas PS, Huang TY, Hanani M. Satellite cell reactions to axon injury of sensory ganglion neurons: increase in number of gap junctions and formation of bridges connecting previously separate perineuronal sheaths. Anat Embryol (Berl). 2003;206:337-47.

Takeda M, Tanimoto T, Kadoi J, Nasu M, Takahashi M, Kitagawa J, et al. Enhanced excitability of nociceptive trigeminal ganglion neurons by satellite glial cytokine following peripheral inflammation. Pain. 2007;129:155-66.

Suadicani SO, Cherkas PS, Zuckerman J, Smith DN, Spray DC, Hanani M. Bidirectional calcium signaling between satellite glial cells and neurons in cultured mouse trigeminal ganglia. Neuron Glia Biol. 2010;6:43-51.

Pannese E. Observation on the morphology, submicroscopic structure and biological properties of satellite cells in sensory ganglia of mammals. Z Zellforsch Mikrosk Anat. 1960;52:567-97.

Ohara PT, Vit JP, Bhargava A, Jasmin L. Evidence for a role of connexin 43 in trigeminal pain using RNA interference in vivo. J Neurophysiol. 2008;100:3064-73.

Spray DC, Scemes E, Rozental R. Introduction to cell-cell communication, in: Zigmond, Bloom, Landis, Squire (Eds), Fundamental neuroscience, Academic press, New York, NY. 1998;317-43.

Hanani M. Satellite glial cells in sensory ganglia: from form to function. Brain Res Brain Res Rev. 2005;48:457-76.

Woodham P, Anderson PN, Nadim W, Turmaine M. Satellite cells surrounding axotomised rat dorsal root ganglion cells increase expression of a GFAP-like protein. Neurosci Lett. 1989;98:8-12.

Hanani M, Haung TY, Cherkas PS, Ledda M, Pannese E. Glial cell plasticity in sensory ganglia induced by nrve damage. Neuroscience. 2002;114:279-83.

Brennan TJ, Vandermeulen EP, Gebhart GF, Characterization of the rat model of incisional pain. Pain. 1996;64:493-501.

Li J, Vause CV, Durham PL. Calcitonin gene-related peptide stimulation of nitric oxide synthesis and release from trigeminal ganglion glial cells. Brain Res. 2008;1196:22-32.

Xie W, Strong JA, Zhang JM. Early blockade of injured primary sensory afferents reduces glial cell activation in two rat neuropathic pain models. Neuroscience. 2009;16:847-57.

Garret 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.

Rouach N, Avignone E Meme W, Koulakoff A, Venance L, Blomstrand F, et al. Gap junctions and connexin expression in the normal and pathological central nervous system. Biol Cell. 2002;94(7-8):457-75.

Warwick RA, Hanani M. The contribution of satellite glial cells to chemotherapy-induced neuropathic pain. Eur J Pain. 2012. doi: 10.1002/j.1532-2149.

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Published

2016-12-19

How to Cite

Deshmukh, V. R., Prasoon, P., & Ray, S. B. (2016). Expression of gap junctions bearing connexin-43 subunits and glial fibrillary acidic protein in the rat dorsal root ganglia following hind paw incision. International Journal of Research in Medical Sciences, 5(1), 306–310. https://doi.org/10.18203/2320-6012.ijrms20164568

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Original Research Articles