Can satellite glial cells be therapeutic targets for pain control?

Neuron Glia Biology

Volumn 6, Issue 1, 2010, Pages 63-71

  Jasmin, Luc ^a,b   Vit, Jean Philippe ^b   Bhargava, Aditi ^a   Ohara, Peter T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

GABA; immune cells; Nociception; RNAi; trigeminal

Indexed keywords

4 AMINOBUTYRIC ACID; CONNEXIN 43; GLUTAMATE DECARBOXYLASE; GLUTAMIC ACID; BROXURIDINE; DOUBLE STRANDED RNA; ECTODYSPLASIN A; GLUTAMATE SYNTHASE; MEMBRANE COFACTOR PROTEIN; SK3 PROTEIN, RAT; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; BIOSYNTHESIS; CELL DIVISION; CONTROLLED STUDY; DISEASE MODEL; GAP JUNCTION; GENE SILENCING; GLIA CELL; IMMUNE RESPONSE; INFRAORBITAL NERVE; MALE; NERVE CELL EXCITABILITY; NOCICEPTION; NONHUMAN; PERIPHERAL NERVE INJURY; PHENOTYPE; PRIORITY JOURNAL; RAT; SATELLITE CELL; ANIMAL; BIOLOGICAL MODEL; BIOLOGICAL THERAPY; CELL JUNCTION; CYTOLOGY; FACE PAIN; GENETICS; GLIA; METABOLISM; METHODOLOGY; PAIN; PAIN ASSESSMENT; PERIPHERAL NEUROPATHY; PHYSIOLOGY; REWARD; SPRAGUE DAWLEY RAT; TRIGEMINUS GANGLION;

RATTUS;

ANIMALS; ANTIGENS, CD46; BROMODEOXYURIDINE; CONNEXIN 43; DISEASE MODELS, ANIMAL; ECTODYSPLASINS; FACIAL PAIN; GAP JUNCTIONS; GLUTAMATE SYNTHASE; MALE; MODELS, BIOLOGICAL; NEUROGLIA; PAIN; PAIN MEASUREMENT; PERIPHERAL NERVOUS SYSTEM DISEASES; RATS; RATS, SPRAGUE-DAWLEY; REWARD; RNA, DOUBLE-STRANDED; SMALL-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; TISSUE THERAPY; TRIGEMINAL GANGLION;

EID: 77957353403     PISSN: 1740925X     EISSN: 17410533     Source Type: Journal    
DOI: 10.1017/S1740925X10000098     Document Type: Article

References (52)

1. Adler J. E., Nico L., VandeVord P. and Skoff A. M. (2009) Modulation of neuropathic pain by a glial-derived factor. Pain Medicine 10, 1229-1236.
2. Bhargava A., Dallman M. F., Pearce D. and Choi S. (2004) Long doublestranded RNA-mediated RNA interference as a tool to achieve sitespecific silencing of hypothalamic neuropeptides. Brain Research and Brain Research Protocol 13, 115-125.
3. Campana W. M. (2007) Schwann cells: activated peripheral glia and their role in neuropathic pain. Brain, Behavior and Immunity 21, 522-527.
4. 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.
5. Carlton S. M., Du J., Tan H. Y., Nesic O., Hargett G. L., Bopp A. C. et al. (2009) Peripheral and central sensitization in remote spinal cord regions contribute to central neuropathic pain after spinal cord injury. Pain 147, 265-276.
6. Carlton S. M. and Hargett G. L. (2007) Colocalization of metabotropic glutamate receptors in rat dorsal root ganglion cells. Journal of Comparative Neurology 501, 780-789.
7. Cecchini T., Ferri P., Ciaroni S., Cuppini R., Ambrogini P., Papa S. et al. (1999) Postnatal proliferation of DRG non-neuronal cells in vitamin E-deficient rats. Anatomical Record 256, 109-115.
8. Chen Z., Muscoli C., Doyle T., Bryant L., Cuzzocrea S., Mollace V. et al. (2010) NMDA-receptor activation and nitroxidative regulation of the glutamatergic pathway during nociceptive processing. Pain 149, 100-106.
9. Cherkas P. S., Huang T. Y., 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.
10. Davis J. D. and Campbell C. S. (1973) Peripheral control of meal size in the rat. Effect of sham feeding on meal size and drinking rate. Journal of Comparative Physiology and Psychology 83, 379-387.
11. Elson K., Ribeiro R. M., Perelson A. S., Simmons A. and Speck P. (2004a) The life span of ganglionic glia in murine sensory ganglia estimated by uptake of bromodeoxyuridine. Experimental Neurology 186, 99-103.
12. Elson K., Simmons A. and Speck P. (2004b) Satellite cell proliferation in murine sensory ganglia in response to scarification of the skin. Glia 45, 105-109.
13. Elson K., Speck P. and Simmons A. (2003) Herpes simplex virus infection of murine sensory ganglia induces proliferation of neuronal satellite cells. Journal of General Virology 84, 1079-1084.
14. Gadea A. and Lopez-Colome A. M. (2001) Glial transporters for glutamate, glycine and GABA I. Glutamate transporters. Journal of Neuroscience Research 63, 453-460. (Pubitemid 32193702)
15. Gunjigake K. K., Goto T., Nakao K., Kobayashi S. and Yamaguchi K. (2009) Activation of satellite glial cells in rat trigeminal ganglion after upper molar extraction. Acta Histochemica et Cytochemica 42, 143-149.
16. Han F., Shioda N., Moriguchi S., Qin Z. H. and Fukunaga K. (2008) Downregulation of glutamate transporters is associated with elevation in extracellular glutamate concentration following rat microsphere embolism. Neuroscience Letters 430, 275-280.
17. Hanani M., Huang T. Y., Cherkas P. S., Ledda M. and Pannese E. (2002) Glial cell plasticity in sensory ganglia induced by nerve damage. Neuroscience 114, 279-283.
18. Hao S., Mata M., Wolfe D., Huang S., Glorioso J. C. and Fink D. J. (2005) Gene transfer of glutamic acid decarboxylase reduces neuropathic pain. Annals of Neurology 57, 914-918.
19. Hoffman E. M. and Miller K. E. (2010) Peripheral inhibition of glutaminase reduces carrageenan-induced Fos expression in the superficial dorsal horn of the rat. Neuroscience Letters 472, 157-160.
20. Hu P., Bembrick A. L., Keay K. A. and McLachlan E. M. (2007) Immune cell involvement in dorsal root ganglia and spinal cord after chronic constriction or transection of the rat sciatic nerve. Brain, Behavior, and Immunity 21, 599-616.
21. Hu P. and McLachlan E. M. (2002) Macrophage and lymphocyte invasion of dorsal root ganglia after peripheral nerve lesions in the rat. Neuroscience 112, 23-38.
22. Hu P. and McLachlan E. M. (2003) Distinct functional types of macrophage in dorsal root ganglia and spinal nerves proximal to sciatic and spinal nerve transections in the rat. Experimental Neurology 184, 590-605.
23. Huang T. Y., Cherkas P. S., Rosenthal D. W. and Hanani M. (2005) Dye coupling among satellite glial cells in mammalian dorsal root ganglia. Brain Research 1036, 42-49.
24. Huang T. Y. and Hanani M. (2005) Morphological and electrophysiological changes in mouse dorsal root ganglia after partial colonic obstruction. American Journal of Physiology. Gastrointestinal and Liver Physiology 289, G670-G678.
25. Humbertson A. Jr., Zimmermann E. and Leedy M. (1969) A chronological study of mitotic activity in satellite cell hyperplasia associated with chromatolytic neurons. Zeitschrift fur Zellforschung und Mikroskopische Anatomie 100, 507-515.
26. Jasmin L., Vit J. P., Sundberg C. and Ohara P. T. (2009) Silencing GLAST in the trigeminal ganglion produced mechanical hypersensitivity. Program No. 171.1 Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience. Online.
27. Kernisant M., Gear R. W., Jasmin L., Vit J. P. and Ohara P. T. (2008) Chronic constriction injury of the infraorbital nerve in the rat using modified syringe needle. Journal of Neuroscience Methods 172, 43-47.
28. Ledda M., Blum E., De Palo S. and Hanani M. (2009) Augmentation in gap junction-mediated cell coupling in dorsal root ganglia following sciatic nerve neuritis in the mouse. Neuroscience 164, 1538-1545.
29. Lee J. Y., Fink D. J. and Mata M. (2006) Vector-mediated gene transfer to express inhibitory neurotransmitters in dorsal root ganglion reduces pain in a rodent model of lumbar radiculopathy. Spine 31, 1555-1558.
30. Liu J., Wolfe D., Hao S., Huang S., Glorioso J. C., Mata M. et al. (2004) Peripherally delivered glutamic acid decarboxylase gene therapy for spinal cord injury pain. Molecular Therapy 10, 57-66.
31. McMahon S. B. and Malcangio M. (2009) Current challenges in glia-pain biology. Neuron 64, 46-54.
32. Mika J., Rojewska E., Makuch W. and Przewlocka B. (2009) Minocycline reduces the injury-induced expression of prodynorphin and pronociceptin in the dorsal root ganglion in a rat model of neuropathic pain. Neuroscience 165, 1420-1428.
33. Ohara P. T., Vit J. P., 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.
34. Pannese E., Ledda M., Cherkas P. S., Huang T. Y. and Hanani M. (2003) 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. Anatomy and Embryology 206, 337-347.
35. Procacci P., Magnaghi V. and Pannese E. (2008) Perineuronal satellite cells in mouse spinal ganglia express the gap junction protein connexin43 throughout life with decline in old age. Brain Research Bulletin 75, 562-569.
36. Raghavendra V., Tanga F. and DeLeo J. A. (2003) Inhibition of microglial activation attenuates the development but not existing hypersensitivity in a rat model of neuropathy. Journal of Pharmacology and Experimental Therapeutics 306, 624-630.
37. Ren K. and Dubner R. (1999) Central nervous system plasticity and persistent pain. Journal of Orofacial Pain 13, 155-163; discussion 164-171.
38. Siemionow K., Klimczak A., Brzezicki G., Siemionow M. and McLain R. F. (2009) The effects of inflammation on glial fibrillary acidic protein expression in satellite cells of the dorsal root ganglion. Spine (Phila Pa 1976) 34, 1631-1637.
39. Sweitzer S. M., Schubert P. and DeLeo J. A. (2001) Propentofylline, a glial modulating agent, exhibits antiallodynic properties in a rat model of neuropathic pain. Journal of Pharmacology and Experimental Therapeutics 297, 1210-1217.
40. Takeuchi H., Jin S., Suzuki H., Doi Y., Liang J., Kawanokuchi J. et al. (2008) Blockade of microglial glutamate release protects against ischemic brain injury. Experimental Neurology 214, 144-146.
41. van Velzen M., Laman J. D., Kleinjan A., Poot A., Osterhaus A. D. and Verjans G. M. (2009) Neuron-interacting satellite glial cells in human trigeminal ganglia have an APC phenotype. Journal of Immunology 183, 2456-2461.
42. Vidwans A. S. and Hewett S. J. (2004) Enhanced release of synaptic glutamate underlies the potentiation of oxygen-glucose deprivationinduced neuronal injury after induction of NOS-2. Experimental Neurology 190, 91-101.
43. Vit J. P., Jasmin L., Bhargava A. and Ohara P. T. (2006) Satellite glial cells in the trigeminal ganglion as a determinant of orofacial neuropathic pain. Neuron Glia Biology 2, 247-257.
44. 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.
45. Vit J. P., Ohara P. T., Sundberg C., Rubi B., Maechler P., Liu C. et al. (2009) Adenovector GAD65 gene delivery into the rat trigeminal ganglion produces orofacial analgesia. Molecular Pain 5, 42.
46. Vos B. P., Strassman A. M. and Maciewicz R. J. (1994) Behavioral evidence of trigeminal neuropathic pain following chronic constriction injury to the rat's infraorbital nerve. Journal of Neuroscience 14, 2708-2723.
47. Wallraff A., Kohling R., Heinemann U., Theis M., Willecke K. and Steinhauser C. (2006) The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. Journal of Neuroscience 26, 5438-5447.
48. Watkins L. R., Martin D., Ulrich P., Tracey K. J. and Maier S. F. (1997) Evidence for the involvement of spinal cord glia in subcutaneous formalin induced hyperalgesia in the rat. Pain 71, 225-235.
49. Woodham P., Anderson P. N., Nadim W. and Turmaine M. (1989) Satellite cells surrounding axotomised rat dorsal root ganglion cells increase expression of a GFAP-like protein. Neuroscience Letters 98, 8-12.
50. Xin W. J., Weng H. R. and Dougherty P. M. (2009) Plasticity in expression of the glutamate transporters GLT-1 and GLAST in spinal dorsal horn glial cells following partial sciatic nerve ligation. Molecular Pain 5, 15.
51. Zhang H., Mei X., Zhang P., Ma C., White F. A., Donnelly D. F. et al. (2009) Altered functional properties of satellite glial cells in compressed spinal ganglia. Glia 57, 1588-1599.
52. Zou J., Wang Y. X., Dou F. F., Lu H. Z., Ma Z. W., Lu P. H. et al. (2010) Glutamine synthetase down-regulation reduces astrocyte protection against glutamate excitotoxicity to neurons. Neurochemistry International 56, 577-584.