Display options
Cite
Huang B, Zdora I, de Buhr N, et al. Phenotypical changes of satellite glial cells in a murine model of G. J Cell Mol Med. 2021;doi: 10.1111/jcmm.17113.
Huang, B., Zdora, I., de Buhr, N., Eikelberg, D., Baumgärtner, W., & Leitzen, E. (2021). Phenotypical changes of satellite glial cells in a murine model of G. Journal of cellular and molecular medicine, . https://doi.org/10.1111/jcmm.17113
Huang, Bei, et al. "Phenotypical changes of satellite glial cells in a murine model of G." Journal of cellular and molecular medicine vol. (2021). doi: https://doi.org/10.1111/jcmm.17113
Huang B, Zdora I, de Buhr N, Eikelberg D, Baumgärtner W, Leitzen E. Phenotypical changes of satellite glial cells in a murine model of G. J Cell Mol Med. 2021 Dec 07; doi: 10.1111/jcmm.17113. Epub 2021 Dec 07. PMID: 34877779.
Copy Download .nbib Format: NLM
Share it on

J Cell Mol Med. 2021 Dec 07; doi: 10.1111/jcmm.17113. Epub 2021 Dec 07.

Phenotypical changes of satellite glial cells in a murine model of G.

Journal of cellular and molecular medicine

Bei Huang, Isabel Zdora, Nicole de Buhr, Deborah Eikelberg, Wolfgang Baumgärtner, Eva Leitzen

Affiliations

  1. Department of Pathology, University of Veterinary Medicine Hannover, Hannover, Germany.
  2. Center of Systems Neuroscience, Hannover, Germany.
  3. Department of Biochemistry, University of Veterinary Medicine Hannover, Hannover, Germany.
  4. Research Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Hannover, Germany.

PMID: 34877779 DOI: 10.1111/jcmm.17113

Abstract

Satellite glial cells (SGCs) of dorsal root ganglia (DRG) react in response to various injuries in the nervous system. This study investigates reactive changes within SGCs in a murine model for G

© 2021 The Authors. Journal of Cellular and Molecular Medicine published by Foundation for Cellular and Molecular Medicine and John Wiley & Sons Ltd.

Keywords: GM1-gangliosidosis; dorsal root ganglia; mouse; satellite glial cells; spinal ganglia

References

  1. Pannese E. The satellite cells of the sensory ganglia. Adv Anat Embryol Cell Biol. 1981;65:1-111. - PubMed
  2. Hanani M. Satellite glial cells in sensory ganglia: from form to function. Brain Res Brain Res Rev. 2005;48(3):457-476. - PubMed
  3. Hanani M, Huang TY, Cherkas PS, Ledda M, Pannese E. Glial cell plasticity in sensory ganglia induced by nerve damage. Neuroscience. 2002;114(2):279-283. - PubMed
  4. 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(5):337-347. - PubMed
  5. Goncalves NP, Vaegter CB, Pallesen LT. Peripheral glial cells in the development of diabetic neuropathy. Front Neurol. 2018;9:268. - PubMed
  6. Huang LY, Gu Y, Chen Y. Communication between neuronal somata and satellite glial cells in sensory ganglia. Glia. 2013;61(10):1571-1581. - PubMed
  7. Robering JW, Gebhardt L, Wolf K, Kuhn H, Kremer AE, Fischer MJM. Lysophosphatidic acid activates satellite glia cells and Schwann cells. Glia. 2019;67(5):999-1012. - PubMed
  8. Kato J, Takai Y, Hayashi MK, et al. Expression and localization of aquaporin-4 in sensory ganglia. Biochem Biophys Res Commun. 2014;451(4):562-567. - PubMed
  9. Huang B, Zdora I, de Buhr N, Lehmbecker A, Baumgärtner W, Leitzen E. Phenotypical peculiarities and species-specific differences of canine and murine satellite glial cells of spinal ganglia. J Cell Mol Med. 2021;25(14):6909-6924. - PubMed
  10. Lemes JBP, de Campos LT, Santos DO, et al. Participation of satellite glial cells of the dorsal root ganglia in acute nociception. Neurosci Lett. 2018;676:8-12. - PubMed
  11. Liu H, Zhao L, Gu W, et al. Activation of satellite glial cells in trigeminal ganglion following dental injury and inflammation. J Mol Histol. 2018;49(3):257-263. - PubMed
  12. Schmitt LI, Leo M, Kutritz A, Kleinschnitz C, Hagenacker T. Activation and functional modulation of satellite glial cells by oxaliplatin lead to hyperexcitability of sensory neurons in vitro. Mol Cell Neurosci. 2020;105:103499. - PubMed
  13. Warwick RA, Hanani M. The contribution of satellite glial cells to chemotherapy-induced neuropathic pain. Eur J Pain. 2013;17(4):571-580. - PubMed
  14. Burda JE, Bernstein AM, Sofroniew MV. Astrocyte roles in traumatic brain injury. Exp Neurol. 2016;275(Pt 3):305-315. - PubMed
  15. Lee J, Ohara K, Shinoda M, et al. Involvement of satellite cell activation via nitric oxide signaling in ectopic orofacial hypersensitivity. Int J Mol Sci. 2020;21(4):1252. - PubMed
  16. Afroz S, Arakaki R, Iwasa T, et al. CGRP induces differential regulation of cytokines from satellite glial cells in trigeminal ganglia and orofacial nociception. Int J Mol Sci. 2019;20(3):711. - PubMed
  17. Hanani M, Blum E, Liu S, Peng L, Liang S. Satellite glial cells in dorsal root ganglia are activated in streptozotocin-treated rodents. J Cell Mol Med. 2014;18(12):2367-2371. - PubMed
  18. Donegan M, Kernisant M, Cua C, Jasmin L, Ohara PT. Satellite glial cell proliferation in the trigeminal ganglia after chronic constriction injury of the infraorbital nerve. Glia. 2013;61(12):2000-2008. - PubMed
  19. Elson K, Simmons A, Speck P. Satellite cell proliferation in murine sensory ganglia in response to scarification of the skin. Glia. 2004;45(1):105-109. - PubMed
  20. Liu FY, Sun YN, Wang FT, et al. Activation of satellite glial cells in lumbar dorsal root ganglia contributes to neuropathic pain after spinal nerve ligation. Brain Res. 2012;1427:65-77. - PubMed
  21. Vit JP, Ohara PT, Bhargava A, Kelley K, Jasmin L. 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. J Neurosci. 2008;28(16):4161-4171. - PubMed
  22. Takeda M, Takahashi M, Matsumoto S. Contribution of the activation of satellite glia in sensory ganglia to pathological pain. Neurosci Biobehav Rev. 2009;33(6):784-792. - PubMed
  23. Zhang L, Xie R, Yang J, et al. Chronic pain induces nociceptive neurogenesis in dorsal root ganglia from Sox2-positive satellite cells. Glia. 2019;67(6):1062-1075. - PubMed
  24. Avraham O, Deng PY, Jones S, et al. Satellite glial cells promote regenerative growth in sensory neurons. Nat Commun. 2020;11(1):4891. - PubMed
  25. Wang F, Xiang H, Fischer G, et al. HMG-CoA synthase isoenzymes 1 and 2 localize to satellite glial cells in dorsal root ganglia and are differentially regulated by peripheral nerve injury. Brain Res. 2016;1652:62-70. - PubMed
  26. Wang S, Wang Z, Li L, et al. P2Y12 shRNA treatment decreases SGC activation to relieve diabetic neuropathic pain in type 2 diabetes mellitus rats. J Cell Physiol. 2018;233(12):9620-9628. - PubMed
  27. Rahman MH, Jha MK, Kim JH, et al. Pyruvate dehydrogenase kinase-mediated glycolytic metabolic shift in the dorsal root ganglion drives painful diabetic neuropathy. J Biol Chem. 2016;291(11):6011-6025. - PubMed
  28. Feldman-Goriachnik R, Belzer V, Hanani M. Systemic inflammation activates satellite glial cells in the mouse nodose ganglion and alters their functions. Glia. 2015;63(11):2121-2132. - PubMed
  29. Blum E, Procacci P, Conte V, Hanani M. Systemic inflammation alters satellite glial cell function and structure. A possible contribution to pain. Neuroscience. 2014;274:209-217. - PubMed
  30. Shin SM, Itson-Zoske B, Cai Y, et al. Satellite glial cells in sensory ganglia express functional transient receptor potential ankyrin 1 that is sensitized in neuropathic and inflammatory pain. Mol Pain. 2020;16:1744806920925425. - PubMed
  31. 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. - PubMed
  32. Warwick RA, Hanani M. Involvement of aberrant calcium signalling in herpetic neuralgia. Exp Neurol. 2016;277:10-18. - PubMed
  33. Muratori L, Ronchi G, Raimondo S, Geuna S, Giacobini-Robecchi MG, Fornaro M. Generation of new neurons in dorsal root ganglia in adult rats after peripheral nerve crush injury. Neural Plast. 2015;2015:860546. - PubMed
  34. Heinecke KA, Luoma A, d'Azzo A, Kirschner DA, Seyfried TN. Myelin abnormalities in the optic and sciatic nerves in mice with GM1-gangliosidosis. ASN Neuro. 2015;7(1):175909141556891. - PubMed
  35. Hahn CN, del Pilar MM, Schröder M, et al. Generalized CNS disease and massive GM1-ganglioside accumulation in mice defective in lysosomal acid beta-galactosidase. Hum Mol Genet. 1997;6(2):205-211. - PubMed
  36. Yamano T, Shimada M, Okada S, et al. Ultrastructural study on nervous system of fetus with GM1-gangliosidosis type 1. Acta Neuropathol. 1983;61(1):15-20. - PubMed
  37. Brunetti-Pierri N, Scaglia F. GM1 gangliosidosis: review of clinical, molecular, and therapeutic aspects. Mol Genet Metab. 2008;94(4):391-396. - PubMed
  38. Tonin R, Caciotti A, Procopio E, et al. Pre-diagnosing and managing patients with GM1 gangliosidosis and related disorders by the evaluation of GM1 ganglioside content. Sci Rep. 2019;9(1):17684. - PubMed
  39. Sandhoff K, Harzer K. Gangliosides and gangliosidoses: principles of molecular and metabolic pathogenesis. J Neurosci. 2013;33(25):10195-10208. - PubMed
  40. Eikelberg D, Lehmbecker A, Brogden G, et al. Axonopathy and reduction of membrane resistance: Key features in a new murine model of human GM1-gangliosidosis. J Clin Med. 2020;9(4):1004. - PubMed
  41. Tessitore A, Martin MDP, Sano R, et al. GM1-ganglioside-mediated activation of the unfolded protein response causes neuronal death in a neurodegenerative gangliosidosis. Mol Cell. 2004;15(5):753-766. - PubMed
  42. Matsuda J, Suzuki O, Oshima A, Ogura A, Naiki M, Suzuki Y. Neurological manifestations of knockout mice with beta-galactosidase deficiency. Brain Dev. 1997;19(1):19-20. - PubMed
  43. Tang X, Schmidt TM, Perez-Leighton CE, Kofuji P. Inwardly rectifying potassium channel Kir4.1 is responsible for the native inward potassium conductance of satellite glial cells in sensory ganglia. Neuroscience. 2010;166(2):397-407. - PubMed
  44. Nadeau JR, Wilson-Gerwing TD, Verge VM. Induction of a reactive state in perineuronal satellite glial cells akin to that produced by nerve injury is linked to the level of p75NTR expression in adult sensory neurons. Glia. 2014;62(5):763-777. - PubMed
  45. Romero A, Romero-Alejo E, Vasconcelos N, Puig MM. Glial cell activation in the spinal cord and dorsal root ganglia induced by surgery in mice. Eur J Pharmacol. 2013;702(1-3):126-134. - PubMed
  46. Belzer V, Hanani M. Nitric oxide as a messenger between neurons and satellite glial cells in dorsal root ganglia. Glia. 2019;67(7):1296-1307. - PubMed
  47. Krishnan A, Bhavanam S, Zochodne D. An intimate role for adult dorsal root ganglia resident cycling cells in the generation of local macrophages and satellite glial cells. J Neuropathol Exp Neurol. 2018;77(10):929-941. - PubMed
  48. Christie K, Koshy D, Cheng C, et al. Intraganglionic interactions between satellite cells and adult sensory neurons. Mol Cell Neurosci. 2015;67:1-12. - PubMed
  49. Bernal A, Arranz L. Nestin-expressing progenitor cells: function, identity and therapeutic implications. Cell Mol Life Sci. 2018;75(12):2177-2195. - PubMed
  50. Ogawa R, Fujita K, Ito K. Mouse embryonic dorsal root ganglia contain pluripotent stem cells that show features similar to embryonic stem cells and induced pluripotent stem cells. Biol Open. 2017;6(5):602-618. - PubMed
  51. Tongtako W, Lehmbecker A, Wang Y, Hahn K, Baumgärtner W, Gerhauser I. Canine dorsal root ganglia satellite glial cells represent an exceptional cell population with astrocytic and oligodendrocytic properties. Sci Rep. 2017;7(1):13915. - PubMed
  52. Middeldorp J, Hol EM. GFAP in health and disease. Prog Neurogibol. 2011;93(3):421-443. - PubMed
  53. Brenner M, Messing A. Regulation of GFAP expression. ASN Neuro. 2021;13:1759091420981206. - PubMed
  54. Yang Z, Wang KK. Glial fibrillary acidic protein: from intermediate filament assembly and gliosis to neurobiomarker. Trends Neurosci. 2015;38(6):364-374. - PubMed
  55. Müller G, Alldinger S, Moritz A, et al. GM1-gangliosidosis in Alaskan huskies: clinical and pathologic findings. Vet Pathol. 2001;38(3):281-290. - PubMed
  56. van der Voorn JP, Kamphorst W, van der Knaap MS, Powers JM. The leukoencephalopathy of infantile GM1 gangliosidosis: oligodendrocytic loss and axonal dysfunction. Acta Neuropathol. 2004;107(6):539-545. - PubMed
  57. Hanani M, Verkhratsky A. Satellite glial cells and astrocytes, a comparative review. Neurochem Res. 2021;46(10):2525-2537. - PubMed
  58. Ohtori S, Takahashi K, Moriya H, Myers RR. 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. - PubMed
  59. Steward O, Torre ER, Tomasulo R, Lothman E. Neuronal activity up-regulates astroglial gene expression. Proc Natl Acad Sci USA. 1991;88(15):6819-6823. - PubMed
  60. Triolo D, Dina G, Lorenzetti I, et al. Loss of glial fibrillary acidic protein (GFAP) impairs Schwann cell proliferation and delays nerve regeneration after damage. J Cell Sci. 2006;119(Pt 19):3981-3993. - PubMed
  61. Nascimento DS, Castro-Lopes JM, Moreira Neto FL. Satellite glial cells surrounding primary afferent neurons are activated and proliferate during monoarthritis in rats: is there a role for ATF3? PLoS One. 2014;9(9):e108152. - PubMed
  62. Gaudet AD, Fonken LK. Glial cells shape pathology and repair after spinal cord injury. Neurotherapeutics. 2018;15(3):554-577. - PubMed
  63. Zimmerman L, Parr B, Lendahl U, et al. Independent regulatory elements in the nestin gene direct transgene expression to neural stem cells or muscle precursors. Neuron. 1994;12(1):11-24. - PubMed
  64. Li L, Mignone J, Yang M, et al. Nestin expression in hair follicle sheath progenitor cells. Proc Natl Acad Sci USA. 2003;100(17):9958-9961. - PubMed
  65. Delacour A, Nepote V, Trumpp A, Herrera PL. Nestin expression in pancreatic exocrine cell lineages. Mech Dev. 2004;121(1):3-14. - PubMed
  66. About I, Laurent-Maquin D, Lendahl U, Mitsiadis TA. Nestin expression in embryonic and adult human teeth under normal and pathological conditions. Am J Pathol. 2000;157(1):287-295. - PubMed
  67. Gilyarov AV. Nestin in central nervous system cells. Neurosci Behav Physiol. 2008;38(2):165-169. - PubMed
  68. Mokry J, Ehrmann J, Karbanova J, et al. Expression of intermediate filament nestin in blood vessels of neural and non-neural tissues. Acta Medica (Hradec Kralove). 2008;51(3):173-179. - PubMed
  69. Krupkova O Jr, Loja T, Zambo I, Veselska R. Nestin expression in human tumors and tumor cell lines. Neoplasma. 2010;57(4):291-298. - PubMed
  70. Tamagno I, Schiffer D. Nestin expression in reactive astrocytes of human pathology. J Neurooncol. 2006;80(3):227-233. - PubMed
  71. Lin RC, Matesic DF, Marvin M, McKay RD, Brustle O. Re-expression of the intermediate filament nestin in reactive astrocytes. Neurobiol Dis. 1995;2(2):79-85. - PubMed
  72. Gallaher ZR, Johnston ST, Czaja K. Neural proliferation in the dorsal root ganglia of the adult rat following capsaicin-induced neuronal death. J Comp Neurol. 2014;522(14):3295-3307. - PubMed
  73. Wang D, Lu J, Xu X, et al. Satellite glial cells give rise to nociceptive sensory neurons. Stem Cell Rev Rep. 2021;17(3):999-1013. - PubMed
  74. Frisén J, Johansson CB, Török C, Risling M, Lendahl U. Rapid, widespread, and longlasting induction of nestin contributes to the generation of glial scar tissue after CNS injury. J Cell Biol. 1995;131(2):453-464. - PubMed
  75. Ayanlaja AA, Xiong Y, Gao Y, et al. Distinct features of doublecortin as a marker of neuronal migration and its implications in cancer cell mobility. Front Mol Neurosci. 2017;10:199. - PubMed
  76. Dellarole A, Grilli M. Adult dorsal root ganglia sensory neurons express the early neuronal fate marker doublecortin. J Comp Neurol. 2008;511(3):318-328. - PubMed
  77. Salzer JL, Zalc B. Myelination. Curr Biol. 2016;26(20):R971-R975. - PubMed
  78. Myllykoski M, Seidel L, Muruganandam G, Raasakka A, Torda AE, Kursula P. Structural and functional evolution of 2’,3'-cyclic nucleotide 3'-phosphodiesterase. Brain Res. 2016;1641(Pt A):64-78. - PubMed
  79. Han H, Myllykoski M, Ruskamo S, Wang C, Kursula P. Myelin-specific proteins: a structurally diverse group of membrane-interacting molecules. BioFactors. 2013;39(3):233-241. - PubMed
  80. Gillespie CS, Sherman DL, Blair GE, Brophy PJ. Periaxin, a novel protein of myelinating Schwann cells with a possible role in axonal ensheathment. Neuron. 1994;12(3):497-508. - PubMed
  81. Kursula P. Structural properties of proteins specific to the myelin sheath. Amino Acids. 2008;34(2):175-185. - PubMed
  82. Makhani N, Tremlett H. The multiple sclerosis prodrome. Nat Rev Neurol. 2021;17(8):515-521. - PubMed
  83. Shandilya A, Mehan S. Dysregulation of IGF-1/GLP-1 signaling in the progression of ALS: potential target activators and influences on neurological dysfunctions. Neurol Sci. 2021;42(8):3145-3166. - PubMed
  84. Koike H, Chiba A, Katsuno M. Emerging infection, vaccination, and Guillain-Barré syndrome: a review. Neurol Ther. 2021;10(2):523-537. - PubMed
  85. Hattori N, Yamamoto M, Yoshihara T, et al. Demyelinating and axonal features of Charcot-Marie-Tooth disease with mutations of myelin-related proteins (PMP22, MPZ and Cx32): a clinicopathological study of 205 Japanese patients. Brain. 2003;126(Pt 1):134-151. - PubMed
  86. Toma JS, McPhail LT, Ramer MS. Differential RIP antigen (CNPase) expression in peripheral ensheathing glia. Brain Res. 2007;1137(1):1-10. - PubMed
  87. Fex Svenningsen A, Colman DR, Pedraza L. Satellite cells of dorsal root ganglia are multipotential glial precursors. Neuron Glia Biology. 2004;1(1):85-93. - PubMed
  88. George D, Ahrens P, Lambert S. Satellite glial cells represent a population of developmentally arrested Schwann cells. Glia. 2018;66(7):1496-1506. - PubMed
  89. Weider M, Wegener A, Schmitt C, et al. Elevated in vivo levels of a single transcription factor directly convert satellite glia into oligodendrocyte-like cells. PLoS Genet. 2015;11(2):e1005008. - PubMed

Publication Types