open access

Ahead of Print
Review article
Published online: 2020-12-05
Submitted: 2020-07-28
Accepted: 2020-11-12
Get Citation

Morphological and functional characteristics of satellite glial cells in the peripheral nervous system

A. Milosavljević1, J. Jančić2, A. Mirčić1, A. Dožić3, J. Boljanović4, M. Milisavljević4, M. Ćetković1
DOI: 10.5603/FM.a2020.0141
·
Pubmed: 33330971
Affiliations
  1. Institute of Histology and Embryology, Faculty of Medicine, University of Belgrade, Serbia
  2. Clinic of Neurology and Psychiatry for Children and Youth, Faculty of Medicine, University of Belgrade, Serbia
  3. Institute of Anatomy, Faculty of Dental Medicine, University of Belgrade, Serbia
  4. Laboratory for Vascular Anatomy, Institute of Anatomy, Faculty of Medicine, University of Belgrade, Serbia

open access

Ahead of Print
REVIEW ARTICLES
Published online: 2020-12-05
Submitted: 2020-07-28
Accepted: 2020-11-12

Abstract

Satellite glial cells are specialized cells that form a functional perineuronal sheath around sensory ganglion neurons. There are a large number of studies that reveal the morphological and functional characteristics of these cells. Satellite glial cells have been studied both in intact ganglions and in tissue cultures, using light and transmission electron microscopy, immunohistochemical and other methods. Satellite glial cells have polygonal form; they are mononuclear and have developed synthetic organelles, numerous receptors, adhesion molecules and ion channels, which enable them to interact with adjacent neurons, as well as transmit signals in the ganglions of the peripheral nervous system. Based on the literature data, satellite glial cells thanks to their characteristics can receive signals from other cells and react to changes in their surroundings. Previous studies have investigated the potential role of satellite glial cells in the formation of the blood-nervous tissue barrier of the peripheral nervous system, as well as in the neuropathic pain genesis. Some recent discoveries support the fact that satellite glial cells can participate in controlling of local viral infections and protecting pseudounipolar neurons from mentioned infections.

Abstract

Satellite glial cells are specialized cells that form a functional perineuronal sheath around sensory ganglion neurons. There are a large number of studies that reveal the morphological and functional characteristics of these cells. Satellite glial cells have been studied both in intact ganglions and in tissue cultures, using light and transmission electron microscopy, immunohistochemical and other methods. Satellite glial cells have polygonal form; they are mononuclear and have developed synthetic organelles, numerous receptors, adhesion molecules and ion channels, which enable them to interact with adjacent neurons, as well as transmit signals in the ganglions of the peripheral nervous system. Based on the literature data, satellite glial cells thanks to their characteristics can receive signals from other cells and react to changes in their surroundings. Previous studies have investigated the potential role of satellite glial cells in the formation of the blood-nervous tissue barrier of the peripheral nervous system, as well as in the neuropathic pain genesis. Some recent discoveries support the fact that satellite glial cells can participate in controlling of local viral infections and protecting pseudounipolar neurons from mentioned infections.

Get Citation

Keywords

satellite glial cell, sensory ganglion, peripheral nervous system, pseudounipolar neuron

About this article
Title

Morphological and functional characteristics of satellite glial cells in the peripheral nervous system

Journal

Folia Morphologica

Issue

Ahead of Print

Article type

Review article

Published online

2020-12-05

DOI

10.5603/FM.a2020.0141

Pubmed

33330971

Keywords

satellite glial cell
sensory ganglion
peripheral nervous system
pseudounipolar neuron

Authors

A. Milosavljević
J. Jančić
A. Mirčić
A. Dožić
J. Boljanović
M. Milisavljević
M. Ćetković

References (83)
  1. Anzil AP, Blinzinger K, Herrlinger H. Fenestrated blood capillaries in rat cranio-spinal sensory ganglia. Cell Tissue Res. 1976; 167(4): 563–567.
  2. Aoki E, Semba R, Kashiwamata S. Evidence for the presence of L-arginine in the glial components of the peripheral nervous system. Brain Res. 1991; 559(1): 159–162.
  3. Blum E, Procacci P, Conte V, et al. Systemic inflammation alters satellite glial cell function and structure. A possible contribution to pain. Neuroscience. 2014; 274: 209–217.
  4. Brown DA, Galvan M. Influence of neuroglial transport on the action of gamma-aminobutyric acid on mammalian ganglion cells. Br J Pharmacol. 1977; 59(2): 373–378.
  5. Bunge MB, Bunge RP, Peterson ER, et al. A light and electron microscope study of long-term organized cultures of rat dorsal root ganglia. J Cell Biol. 1967; 32(2): 439–466.
  6. Carozzi VA, Canta A, Oggioni N, et al. Expression and distribution of 'high affinity' glutamate transporters GLT1, GLAST, EAAC1 and of GCPII in the rat peripheral nervous system. J Anat. 2008; 213(5): 539–546.
  7. Cherkas PS, Huang TY, Pannicke T, et al. The effects of axotomy on neurons and satellite glial cells in mouse trigeminal ganglion. Pain. 2004; 110(1-2): 290–298.
  8. Chudler EH, Anderson LC, Byers MR. Trigeminal ganglion neuronal activity and glial fibrillary acidic protein immunoreactivity after inferior alveolar nerve crush in the adult rat. Pain. 1997; 73(2): 141–149.
  9. Devor M, Seltzer Z. Pathophysiology of damaged nerves in relation to chronic pain. In: Wall PD, Melzack R (eds) Textbook of pain. Churcill Livingston, London 1999: 129–164.
  10. Dillard SH, Cheatham WJ, Moses HL. Electron microscopy of zosteriform herpes simplex infection in the mouse. Lab Invest. 1972; 26(4): 391–402.
  11. Djukic B, Casper KB, Philpot BD, 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(42): 11354–11365.
  12. Dubový P, Klusáková I, Svízenská I, et al. Satellite glial cells express IL-6 and corresponding signal-transducing receptors in the dorsal root ganglia of rat neuropathic pain model. Neuron Glia Biol. 2010; 6(1): 73–83.
  13. Eames RA, Gamble HJ. Schwann cell relationships in normal human cutaneous nerves. J Anat. 1970; 106(Pt 3): 417–435.
  14. Elfvin LG, Forsman C. The ultrastructure of junctions between satellite cells in mammalian sympathetic ganglia as revealed by freeze-etching. J Ultrastruct Res. 1978; 63(3): 261–274.
  15. Elson K, Speck P, Simmons A. Herpes simplex virus infection of murine sensory ganglia induces proliferation of neuronal satellite cells. J Gen Virol. 2003; 84(Pt 5): 1079–1084.
  16. Gotow T, Yoshikawa H, Hashimoto PH. Distribution patterns of orthogonal arrays and alkaline phosphatase in plasma membranes of satellite cells in rat spinal ganglia. Anat Embryol (Berl). 1985; 171(2): 171–179.
  17. Hanani M. Satellite glial cells in sensory ganglia: from form to function. Brain Res Brain Res Rev. 2005; 48(3): 457–476.
  18. Hanker JS, Romanovicz DK, Moore GH. Peroxisomes in satellite, Schwann and laminarcells associated with trigeminal sensory neurons. J Cell Biol. 1974; 63: 131a.
  19. Herman SP, Klein R, Talley FA, et al. An ultrastructural study of methylmercury-induced primary sensory neuropathy in the rat. Lab Invest. 1973; 28(1): 104–118.
  20. Hess A. The fine structure of young and old spinal ganglia. Anat Rec. 1955; 123(4): 399–423.
  21. Hill TJ, Field HJ. The interaction of herpes simplex virus with cultures of peripheral nervous tissue: an electron microscopic study. J Gen Virol. 1973; 21: 123–133.
  22. Holtzman E, Peterson ER. Uptake of protein by mammalian neurons. J Cell Biol. 1969; 40(3): 863–869.
  23. Hösli E, Hösli L. Autoradiographic localization of the uptake of [3H]- GABA and [3H]L-glutamic acid in neurones and glial cells of cultured dorsal root ganglia. Neurosci Lett. 1978; 7(2-3): 173–176.
  24. Huang TY, Cherkas PS, Rosenthal DW, et al. Dye coupling among satellite glial cells in mammalian dorsal root ganglia. Brain Res. 2005; 1036(1-2): 42–49.
  25. Jessen KR, Thorpe R, Mirsky R. Molecular identity, distribution and heterogeneity of glial fibrillary acidic protein: an immunoblotting and immunohistochemical study of Schwann cells, satellite cells, enteric glia and astrocytes. J Neurocytol. 1984; 13(2): 187–200.
  26. Jessen KR, Thorpe R, Mirsky R. Molecular identity, distribution and heterogeneity of glial fibrillary acidic protein: an immunoblotting and immunohistochemical study of Schwann cells, satellite cells, enteric glia and astrocytes. J Neurocytol. 1984; 13(2): 187–200.
  27. Jones D. Studies on the origin of sheath cells and sympathetic ganglia in the chick. Anat Rec. 1939; 73(3): 343–357.
  28. Julius D, Basbaum AI. Molecular mechanisms of nociception. Nature. 2001; 413(6852): 203–210.
  29. King JS. A light and electron microscopic study of perineuronal glial cells and processes in the rabbit neccortex. Anat Rec. 1968; 161(1): 111–123.
  30. Krawczyk WS, Wilgram GF. Hemidesmosome and desmosome morphogenesis during epidermal wound healing. J Ultrastruct Res. 1973; 45(1): 93–101.
  31. Kummer W, Behrends S, Schwarzlmüller T, et al. Subunits of soluble guanylyl cyclase in rat and guinea-pig sensory ganglia. Brain Res. 1996; 721(1-2): 191–195.
  32. LaVail JH, Topp KS, Giblin PA, et al. Factors that contribute to the transneuronal spread of herpes simplex virus. J Neurosci Res. 1997; 49(4): 485–496.
  33. Levi G. La capsula delle cellule dei gangli sensitivi. Penetrazione di fibre collagene nel loro protoplasma. Monit Zool Ital. 1907; 18: 153–158.
  34. Levin MJ, Cai GY, Manchak MD, et al. Varicella-zoster virus DNA in cells isolated from human trigeminal ganglia. J Virol. 2003; 77(12): 6979–6987.
  35. Liu W, Glueckert R, Linthicum FH, et al. Possible role of gap junction intercellular channels and connexin 43 in satellite glial cells (SGCs) for preservation of human spiral ganglion neurons : A comparative study with clinical implications. Cell Tissue Res. 2014; 355(2): 267–278.
  36. Magnusson S, Ekström J, Elmér E, et al. Heme oxygenase-1, heme oxygenase-2 and biliverdin reductase in peripheral ganglia from rat, expression and plasticity. Neuroscience. 1999; 95(3): 821–829.
  37. Matthews MR, Raisman G. A light and electron microscopic study of the cellular response to axonal injury in the superior cervical ganglion of the rat. Proc R Soc Lond B Biol Sci. 1972; 181(1062): 43–79.
  38. Moses HL, Beaver DL, Ganote CE. Electron microscopy of the trigeminal ganglion. I. Comparative ultrastructure. Arch Pathol. 1965; 79: 541–556.
  39. Novikoff AB, Quintana N, Villaverde H, et al. Nucleoside phosphatase and cholinesterase activities in dorsal root ganglia and peripheral nerve. J Cell Biol. 1966; 29(3): 525–545.
  40. Ohtori S, Takahashi K, Moriya H, et al. TNF-alpha and TNF-alpha receptor type 1 upregulation in glia and neurons after peripheral nerve injury: studies in murine DRG and spinal cord. Spine (Phila Pa 1976). 2004; 29(10): 1082–1088.
  41. Pannese E, Ledda M, Cherkas PS, et al. 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(5): 337–347.
  42. Pannese E, Luciano L, Iurato S, et al. Intercellular junctions and other membrane specializations in developing spinal ganglia: a freeze-fracture study. J Ultrastruct Res. 1977; 60(2): 169–180.
  43. Pannese E. Biology and pathology of perineuronal satellite cells in sensory ganglia. Adv Anat Embryol Cell Biol. 2018: 1–63.
  44. Pannese E. Electron microscopical study on the development of the satellite cell sheath in spinal ganglia. J Comp Neurol. 1969; 135(4): 381–422.
  45. Pannese E. Number and structure of perisomatic satellite cells of spinal ganglia under normal conditions or during axon regeneration and neuronal hypertrophy. Z Zellforsch. 1964; 63(4): 568–592.
  46. Pannese E. Observations on the morphology, submicroscopic structure and biological properties of satellite cells (s.c.) in sensory ganglia of mammals. Z Zellforsch. 1960; 52: 567–597.
  47. Pannese E. The histogenesis of the spinal ganglia. Adv Anat Embryol Cell Biol. 1974; 47(5): 7–97.
  48. Pannese E. The response of the satellite and other non-neuronal cells to the degeneration of neuroblasts in chick embryo spinal ganglia. Cell Tissue Res. 1978; 190(1): 1–14.
  49. Pannese E. The satellite cells of the sensory ganglia. Adv Anat Embryol Cell Biol. 1981.
  50. Pannese E. The structure of the perineuronal sheath of satellite glial cells (SGCs) in sensory ganglia. Neuron Glia Biol. 2010; 6(1): 3–10.
  51. Pérez Armendariz EM, Norcini M, Hernández-Tellez B, et al. Neurons and satellite glial cells in adult rat lumbar dorsal root ganglia express connexin 36. Acta Histochem. 2018; 120(3): 168–178.
  52. Pilar G, Landmesser L. Ultrastructural differences during embryonic cell death in normal and peripherally deprived ciliary ganglia. J Cell Biol. 1976; 68(2): 339–356.
  53. Procacci P, Magnaghi V, Pannese E. Perineuronal satellite cells in mouse spinal ganglia express the gap junction protein connexin43 throughout life with decline in old age. Brain Res Bull. 2008; 75(5): 562–569.
  54. Ramón y Cajal S. Histologie du système nerveux de l'homme & des vertébrés. A. Maloine, Paris. 1909.
  55. Rash JE, Yasumura T, Rash JE, et al. Direct immunogold labeling of aquaporin-4 in square arrays of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord. Proc Natl Acad Sci USA. 1998; 95(20): 11981–11986.
  56. Rashid MH, Inoue M, Matsumoto M, et al. Switching of bradykinin-mediated nociception following partial sciatic nerve injury in mice. J Pharmacol Exp Ther. 2004; 308(3): 1158–1164.
  57. Reichelt M, Zerboni L, Arvin AM. Mechanisms of varicella-zoster virus neuropathogenesis in human dorsal root ganglia. J Virol. 2008; 82(8): 3971–3983.
  58. Rosenbluth J, Palay SL. The fine structure of nerve cell bodies and their myelin sheaths in the eighth nerve ganglion of the goldfish. J Biophys Biochem Cytol. 1961; 9: 853–877.
  59. Sandelin M, Zabihi S, Liu Li, et al. Metastasis-associated S100A4 (Mts1) protein is expressed in subpopulations of sensory and autonomic neurons and in Schwann cells of the adult rat. J Comp Neurol. 2004; 473(2): 233–243.
  60. Schon F, Kelly JS. Autoradiographic localisation of [3H]GABA and [3H]glutamate over satellite glial cells. Brain Res. 1974; 66(2): 275–288.
  61. Sharma K, Korade Z, Frank E. Late-migrating neuroepithelial cells from the spinal cord differentiate into sensory ganglion cells and melanocytes. Neuron. 1995; 14(1): 143–152.
  62. Shi TJS, Holmberg K, Xu ZQ, et al. Effect of peripheral nerve injury on cGMP and nitric oxide synthase levels in rat dorsal root ganglia: time course and coexistence. Pain. 1998; 78(3): 171–180.
  63. Shimeld C, Whiteland JL, Williams NA, et al. Cytokine production in the nervous system of mice during acute and latent infection with herpes simplex virus type 1. J Gen Virol. 1997; 78 ( Pt 12): 3317–3325.
  64. Shimizu Y. The satellite cells in cultures of dissociated spinal ganglia. Z Zellforsch. 1965; 67(2): 185–195.
  65. Shinder V, Devor M. Structural basis of neuron-to-neuron cross-excitation in dorsal root ganglia. J Neurocytol. 1994; 23(9): 515–531.
  66. Thippeswamy T, McKay JS, Morris R, et al. Glial-mediated neuroprotection: evidence for the protective role of the NO-cGMP pathway via neuron-glial communication in the peripheral nervous system. Glia. 2005; 49(2): 197–210.
  67. Valentin G. Über den Verlauf und die letzten Enden der Nerven. Nova acta phys med acad Caesar Leopol Carol Breslau u Bonn. 1836; 18: 51.
  68. van Velzen M, Laman JD, Kleinjan A, et al. Neuron-interacting satellite glial cells in human trigeminal ganglia have an APC phenotype. J Immunol. 2009; 183(4): 2456–2461.
  69. Verbavatz JM, Ma T, Gobin R, et al. Absence of orthogonal arrays in kidney, brain and muscle from transgenic knockout mice lacking water channel aquaporin-4. J Cell Sci. 1997; 110 ( Pt 22): 2855–2860.
  70. Vesin MF, Urade Y, Hayaishi O, et al. Neuronal and glial prostaglandin D synthase isozymes in chick dorsal root ganglia: a light and electron microscopic immunocytochemical study. J Neurosci. 1995; 15(1 Pt 1): 470–476.
  71. Vit JP, 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(4): 247–257.
  72. Wakisaka H, Kobayashi N, Mominoki K, et al. Herpes simplex virus in the vestibular ganglion and the geniculate ganglion: role of loose myelin. J Neurocytol. 2001; 30(8): 685–693.
  73. Waxman SG, Dichter MA, Hartwieg EA, et al. Recapitulation of normal neuro-glial relations in dissociated cell cultures of dorsal root ganglia. Brain Res. 1977; 122(2): 344–350.
  74. Wetmore C, Olson L. Neuronal and nonneuronal expression of neurotrophins and their receptors in sensory and sympathetic ganglia suggest new intercellular trophic interactions. J Comp Neurol. 1995; 353(1): 143–159.
  75. Wilkinson R, Leaver C, Simmons A, et al. Restricted replication of herpes simplex virus in satellite glial cell cultures clonally derived from adult mice. J Neurovirol. 1999; 5(4): 384–391.
  76. Woodham P, Anderson PN, Nadim W, et al. Satellite cells surrounding axotomised rat dorsal root ganglion cells increase expression of a GFAP-like protein. Neurosci Lett. 1989; 98(1): 8–12.
  77. Wu HH, Bellmunt E, Scheib JL, et al. Glial precursors clear sensory neuron corpses during development via Jedi-1, an engulfment receptor. Nat Neurosci. 2009; 12(12): 1534–1541.
  78. Xian CJ, Zhou XF. Neuronal-glial differential expression of TGF-alpha and its receptor in the dorsal root ganglia in response to sciatic nerve lesion. Exp Neurol. 1999; 157(2): 317–326.
  79. Young J, Brown DA, Kelly JS, et al. Autoradiographic localization of sites of [3H]γ-aminobutyric acid accumulation in peripheral autonomic ganglia. Brain Res. 1973; 63: 479–486.
  80. Zerboni L, Arvin A. Neuronal subtype and satellite cell tropism are determinants of varicella-zoster virus virulence in human dorsal root ganglia xenografts in vivo. PLoS Pathog. 2015; 11(6): e1004989.
  81. Ziegler RJ, Herman RE. Peripheral infection in culture of rat sensory neurons by herpes simplex virus. Infect Immun. 1980; 28(2): 620–623.
  82. Ziegler RJ, Pozos RS. Ultrastructural effects of herpes simplex virus type 2 infection of rat dorsal root ganglia in culture. J Neuropathol Exp Neurol. 1977; 36(4): 680–692.
  83. Zimmerman E, Karsh D, Humbertson A. Initiating factors in perineuronal cell hyperplasia associated with chromatolytic neurons. Z Zellforsch. 1971; 114(1): 73–82.

Regulations

Important: This website uses cookies. More >>

The cookies allow us to identify your computer and find out details about your last visit. They remembering whether you've visited the site before, so that you remain logged in - or to help us work out how many new website visitors we get each month. Most internet browsers accept cookies automatically, but you can change the settings of your browser to erase cookies or prevent automatic acceptance if you prefer.

By  "Via Medica sp. z o.o." sp.k., Świętokrzyska 73, 80–180 Gdańsk, Poland

tel.:+48 58 320 94 94, faks:+48 58 320 94 60, e-mail:  viamedica@viamedica.pl