Astrocyte marker GFAP in gliocytes of the peripheral nervous system

Capa

Citar

Texto integral

Acesso aberto Acesso aberto
Acesso é fechado Acesso está concedido
Acesso é fechado Somente assinantes

Resumo

The study of peripheral nervous system glial cells is an actual problem of modern neurobiology. The purpose of this work was to summarize our own and published data on the distribution of glial fibrillary acidic protein (GFAP) in peripheral nervous system (PNS) glial cells. The features of GFAP expression in glial cells of the enteric nervous system, dorsal root ganglion and peripheral nerve were examined. A comparative study of different populations of PNS gliocytes led to the conclusion that the intermediate filament protein GFAP is distributed differently in them. Analysis of the literature showed that despite the fact that this protein is widely used as a molecular marker of glial activation, there is still no understanding of the exact mechanisms of GFAP participation in the glial reactive response. The described features of GFAP+gliocytes from different parts of the PNS demonstrate the functional polymorphism of this protein. Its ability to be expressed in peripheral nervous system gliocytes in response to injury requires further research.

Texto integral

Acesso é fechado

Sobre autores

E. Petrova

Institute of Experimental Medicine

Autor responsável pela correspondência
Email: iempes@yandex.ru
Rússia, St. Petersburg

E. Kolos

Institute of Experimental Medicine

Email: iempes@yandex.ru
Rússia, St. Petersburg

Bibliografia

  1. Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119(1): 7–35. https://doi.org/10.1007/s00401-009-0619-8
  2. Sukhorukova EG, Korzhevskii DE, Alekseeva OS (2015) Glial fibrillary acidic protein: The component of iintermediate filaments in the vertebrate brain astrocytes. J Evol Biochem Phys 51: 1–10. https://doi.org/10.1134/S0022093015010019
  3. McGinnis A, Ji R-R (2023) The Similar and Distinct Roles of Satellite Glial Cells and Spinal Astrocytes in Neuropathic Pain. Cells 12(6): 965. https://doi.org/10.3390/cells12060965
  4. Liedtke W, Edelmann W, Bieri PL, Chiu FC, Cowan NJ, Kucherlapati R, Raine CS (1996) GFAP is necessary for the integrity of CNS white matter architecture and long-term maintenance of myelination. Neuron 17(4): 607–615. https://doi.org/10.1016/s0896-6273(00)80194-4.
  5. Hol EM, Pekny M (2015) Glial fibrillary acidic protein (GFAP) and the astrocyte intermediate filament system in diseases of the central nervous system. Curr Opin Cell Biol 32: 121–130. https://doi.org/10.1016/j.ceb.2015.02.004
  6. Hanani M, Verkhratsky A (2021) Satellite Glial Cells and Astrocytes, a Comparative Review. Neurochem Res 46(10): 2525–2537. https://doi.org/10.1007/s11064-021-03255-8
  7. Middeldorp J, Hol EM (2011) GFAP in health and disease Prog Neurobiol 93(3): 421–443. https://doi.org/10.1016/j.pneurobio.2011.01.005
  8. Sullivan SM (2014) GFAP variants in health and disease: stars of the brain… and gut. J Neurochem 130(6): 729–732. https://doi.org/10.1111/jnc.12754
  9. Messing A, Brenner M (2020) GFAP at 50. ASN Neuro 12: 1759091420949680. https://doi.org/10.1177/1759091420949680
  10. De Reus AJEM, Basak O, Dykstra W, van Asperen JV, van Bodegraven EJ, Hol EM (2024) GFAP-isoforms in the nervous system: Understanding the need for diversity. Curr Opin Cell Biol 87: 102340. https://doi.org/10.1016/j.ceb.2024.102340
  11. Mamber C, Kamphuis W, Haring NL, Peprah N, Middeldorp J, Hol EM (2012) GFAPδ expression in glia of the developmental and adolescent mouse brain. PLoS One 7(12): e52659. https://doi.org/10.1371/journal.pone.0052659
  12. Kamphuis W, Mamber C, Moeton M, Kooijman L, Sluijs JA, Jansen AH, Verveer M, de Groot LR, Smith VD, Rangarajan S, Rodríguez JJ, Orre M, Hol EM (2012) GFAP Isoforms in Adult Mouse Brain with a Focus on Neurogenic Astrocytes and Reactive Astrogliosis in Mouse Models of Alzheimer Disease. PLoS ONE7(8): e42823. https://doi.org/10.1371/journal.pone.0042823
  13. Moeton M, Stassen OM, Sluijs JA, van der Meer VW, Kluivers LJ, van Hoorn H, Schmidt T, Reits EA, van Strien ME, Hol EM (2016) GFAP isoforms control intermediate filament network dynamics, cell morphology, and focal adhesions. Cell Mol Life Sci 73(21): 4101–4120. https://doi.org/10.1007/s00018-016-2239-5
  14. Sullivan SM, Lee A, Bjorkman ST, Miller SM, Sullivan RK, Poronnik P, Colditz PB, Pow DV (2007) Cytoskeletal anchoring of GLAST determines susceptibility to brain damage: an identified role for GFAP. J Biol Chem 282: 29414–29423. https://doi.org/10.1074/jbc.M704152200
  15. Eng LF, Ghirnikar RS (1994) GFAP and astrogliosis. Brain Pathol 4(3): 229–237. https://doi.org/10.1111/j.1750-3639.1994.tb00838.x
  16. Brenner M (2014) Role of GFAP in CNS injuries. Neurosci Lett 565: 7–13. https://doi.org/10.1016/j.neulet.2014.01.055
  17. Wang X, Messing A, David S (1997) Axonal and Nonneuronal Cell Responses to Spinal Cord Injury in Mice Lacking Glial Fibrillary Acidic Protein. Exp Neurol 148: 568–576. https://doi.org/10.1006/exnr.1997.6702
  18. Jurga AM, Paleczna M, Kadluczka J, Kuter KZ (2021) Beyond the GFAP-Astrocyte Protein Markers in the Brain. Biomolecules 11: 1361. https://doi.org/10.3390/biom11091361
  19. Escartin C, Galea E, Lakatos A, O'Callaghan JP, Petzold GC, Serrano-Pozo A, Steinhäuser C, Volterra A, Carmignoto G, Agarwal A, Allen NJ, Araque A, Barbeito L, Barzilai A, Bergles DE, Bonvento G, Butt AM, Chen WT, Cohen-Salmon M, Cunningham C, Deneen B, De Strooper B, Díaz-Castro B, Farina C, Freeman M, Gallo V, Goldman JE, Goldman SA, Götz M, Gutiérrez A, Haydon PG, Heiland DH, Hol EM, Holt MG, Iino M, Kastanenka KV, Kettenmann H, Khakh BS, Koizumi S, Lee CJ, Liddelow SA, MacVicar BA, Magistretti P, Messing A, Mishra A, Molofsky AV, Murai KK, Norris CM, Okada S, Oliet SHR, Oliveira JF, Panatier A, Parpura V, Pekna M, Pekny M, Pellerin L, Perea G, Pérez-Nievas BG, Pfrieger FW, Poskanzer KE, Quintana FJ, Ransohoff RM, Riquelme-Perez M, Robel S, Rose CR, Rothstein JD, Rouach N, Rowitch DH, Semyanov A, Sirko S, Sontheimer H, Swanson RA, Vitorica J, Wanner IB, Wood LB, Wu J, Zheng B, Zimmer ER, Zorec R, Sofroniew MV, Verkhratsky A (2021) Reactive astrocyte nomenclature, definitions, and future directions. Nat Neurosci 24(3): 312–325. https://doi.org/10.1038/s41593-020-00783-4
  20. Yang Z, Wang KK (2015) Glial fibrillary acidic protein: from intermediate filament assembly and gliosis to neurobiomarker. Trends Neurosci 38(6): 364–374. https://doi.org/10.1016/j.tins.2015.04.003
  21. Lawrence JM, Schardien K, Wigdahl B, Nonnemacher MR (2023) Roles of neuropathology-associated reactive astrocytes: a systematic review. Acta Neuropathol Commun 11: 42. https://doi.org/10.1186/s40478-023-01526-9
  22. Kanazawa S, Nishizawa S, Takato T, Hoshi K (2017) Biological roles of glial fibrillary acidic protein as a biomarker in cartilage regenerative medicine. J Cell Physiol 232(11): 3182–3193. https://doi.org/10.1002/jcp.25771
  23. Shang L, Hosseini M, Liu X, Kisseleva T, Brenner DA (2018) Human hepatic stellate cell isolation and characterization. J Gastroenterol 53(1): 6–17. https://doi.org/10.1007/s00535-017-1404-4
  24. Jessen KR, Mirsky R (1983) Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of enteric glia. J Neurosci 3: 2206–2218.
  25. Kato H, Yamamoto T, Yamamoto H, Ohi R, So N, Iwasaki Y (1990) Immunocytochemical characterization of supporting cells in the enteric nervous system in Hirschsprung's disease. J Pediatr Surg 25(5): 514–519. https://doi.org/10.1016/0022-3468(90)90563-o
  26. Jessen KR, Morgan L, Stewart HJ, Mirsky R (1990) Three markers of adult non-myelin-forming Schwann cells, 217c(Ran-1), A5E3 and GFAP: development and regulation by neuron-Schwann cell interactions. Development 109(1): 91–103. https://doi.org/10.1242/dev.109.1.91
  27. Jessen KR, Mirsky R, Lloyd AC (2015) Schwann Cells: Development and Role in Nerve Repair. Cold Spring Harb Perspect Biol 7(7): a020487. https://doi.org/10.1101/cshperspect.a020487
  28. Jessen KR, Arthur-Farraj P (2019) Repair Schwann cell update: Adaptive reprogramming, EMT, and stemness in regenerating nerves. Glia 67(3): 437. https://doi.org/10.1002/glia.23532
  29. Mohr KM, Pallesen LT, Richner M, Vaegter CB (2021) Discrepancy in the Usage of GFAP as a Marker of Satellite Glial Cell Reactivity. Biomedicines 9(8): 1022. https://doi.org/10.3390/biomedicines9081022
  30. Kolos EA, Korzhevskii DE (2020) Immunohistological Detection of Active Satellite Cellsin Rat Dorsal Root Ganglia after Parenteral Administration of Lipopolysaccharide and during Aging. Bull Exp Biol Med 169(5): 665–668. https://doi.org/10.1007/s10517-020-04950-2
  31. Konnova EA, Deftu AF, Chu Sin Chung P, Pertin M, Kirschmann G, Decosterd I, Suter MR (2023) Characterisation of GFAP-Expressing Glial Cells in the Dorsal Root Ganglion after Spared Nerve Injury. Int J Mol Sci 24(21): 15559. https://doi.org/10.3390/ijms242115559
  32. Georgiou J, Robitaille R, Trimble WS, Charlton MP (1994). Synaptic regulation of glial protein expression in vivo. Neuron 12(2): 443–455. https://doi.org/10.1016/0896-6273(94)90284-4
  33. Georgiou J, Robitaille R, Charlton MP (1999) Muscarinic control of cytoskeleton in perisynaptic glia. J Neurosci 19(10): 3836–3846. https://doi.org/10.1523/JNEUROSCI.19-10-03836.1999
  34. Von Boyen GB, Steinkamp M, Reinshagen M, Schäfer KH, Adler G, Kirsch J (2004) Proinflammatory cytokines increase glial fibrillary acidic protein expression in enteric glia. Gut 53(2): 222–228. https://doi.org/10.1136/gut.2003.012625
  35. Grundmann D, Loris E, Maas-Omlor S, Huang W, Scheller A, Kirchhoff F, Schäfer KH (2019) Enteric glia: S100, GFAP, and beyond. Anat Rec (Hoboken) 302(8): 1333–1344. https://doi.org/10.1002/ar.24128
  36. Cobo R, García-Piqueras J, Cobo J, Vega JA (2021) The Human Cutaneous Sensory Corpuscles: An Update. J Clin Med 10(2): 227. https://doi.org/10.3390/jcm10020227
  37. Ноздрачев АД, Чумасов ЕИ (1999) Периферическая нервная система. СПб. Наука. [Nozdrachev AD, Chumasov EI (1999) Peripheral nervous system. Sankt-Peterburg. Nauka. (In Russ)].
  38. Lu T, Huang C, Weng R, Wang Z, Sun H, Ma X (2024) Enteric glial cells contribute to chronic stress-induced alterations in the intestinal microbiota and barrier in rats. Heliyon 10(3): e24899. https://doi.org/10.1016/j.heliyon.2024.e24899
  39. Gulbransen BD, Sharkey KA (2012) Novel functional roles for enteric glia in the gastrointestinal tract. Nat Rev Gastroenterol Hepatol 9: 625–632.
  40. Pawolski V, Schmidt MH (2021) Neuron–glia interaction in the developing and adult enteric nervous system. Cells 10: 47. https://doi.org/10.3390/cells10010047
  41. Чумасов ЕИ, Майстренко НА, Ромащенко ПН, Самедов ВБ, Петрова ЕС, Коржевский ДЭ (2023) Патологические изменения глиальных клеток в энтеральной нервной системе толстой кишки при хроническом медленно-транзитном запоре. Сибирск науч мед журн 43(6): 191–202. [Chumasov EI, Majstrenko NA, Romashhenko PN, Samedov VB, Petrova ES, Korzhevskij DE (2023) `Pathological changes in glial cells in the enteric nervous system of the colon during chronic slow-transit constipation. Sibirsk nauch med zhurn 43(6): 191–202. (In Russ)]. https://doi.org/10.18699/SSMJ20230624
  42. Boesmans W, Lasrado R, Vanden Berghe P, Pachnis V (2015) Heterogeneity and phenotypic plasticity of glial cells in the mammalian enteric nervous system. Glia 63(2): 229–241. https://doi.org/10.1002/glia.22746
  43. Lasrado R, Boesmans W, Kleinjung J, Pin C, Bell D, Bhaw L, McCallum S, Zong H, Luo L, Clevers H, Vanden Berghe P, Pachnis V (2017) Lineage-dependent spatial and functional organization of the mammalian enteric nervous system. Science 356(6339): 722–726. https://doi.org/10.1126/science.aam7511
  44. Hanani M (2010) Satellite glial cells: more than just 'rings around the neuron'. Neuron Glia Biol 6(1): 1–2. https://doi.org/10.1017/S1740925X10000104
  45. Seguella L, Gulbransen BD (2021) Enteric glial biology, intercellular signalling and roles in gastrointestinal disease. Nat Rev Gastroenterol Hepatol 18(8): 571–587. https://doi.org/10.1038/s41575-021-00423-7
  46. Clairembault T, Kamphuis W, Leclair-Visonneau L, Rolli-Derkinderen M, Coron E, Neunlist M, Hol EM, Derkinderen P (2014) Enteric GFAP expression and phosphorylation in Parkinson's disease. J Neurochem 130(6): 805–815. https://doi.org/10.1111/jnc.12742
  47. Pannese E (2018) Biology and Pathology of Perineuronal Satellite Cells in Sensory Ganglia. Springer. Berlin/Heidelberg. Germany.
  48. George D, Ahrens P, Lambert S (2018) Satellite glial cells represent a population of developmentally arrested Schwann cells. Glia 66(7): 1496–1506. https://doi.org/10.1002/glia.23320
  49. Huang LY, Gu Y, Chen Y (2013) Communication between neuronal somata and satellite glial cells in sensory ganglia. Glia 61(10): 1571–1581. https://doi.org/10.1002/glia.22541
  50. Costa FA, Moreira Neto FL (2015) Células gliais satélite de gânglios sensitivos: o seu papel na dor [Satellite glial cells in sensory ganglia: its role in pain]. Rev Bras Anestesiol 65(1): 73–81. https://doi.org/10.1016/j.bjan.2013.07.013
  51. Izmiryan A, Li Z, Nothias F, Eyer J, Paulin D, Soares S, Xue Z (2021). Inactivation of vimentin in satellite glial cells affects dorsal root ganglion intermediate filament expression and neuronal axon growth in vitro. Mol Cell Neurosci 115: 103659. https://doi.org/10.1016/j.mcn.2021.103659
  52. Li Y, North RY, Rhines LD, Tatsui CE, Rao G, Edwards DD, Cassidy RM, Harrison DS, Johansson CA, Zhang H, Dougherty PM (2018) DRG Voltage-Gated Sodium Channel 1.7 Is Upregulated in Paclitaxel-Induced Neuropathy in Rats and in Humans with Neuropathic Pain. J Neurosci 38: 1124–1136. https://doi.org/10.1523/JNEUROSCI.0899-17.2017
  53. Hanani M, Blum E, Liu S, Peng L, Liang S (2014) Satellite glial cells in dorsal root ganglia are activated in streptozotocin-treated rodents. J Cell Mol Med 18(12): 2367–2371. https://doi.org/10.1111/jcmm.12406
  54. Schulte A, Lohner H, Degenbeck J, Segebarth D, Rittner HL, Blum R, Aue A (2023) Unbiased analysis of the dorsal root ganglion after peripheral nerve injury: no neuronal loss, no gliosis, but satellite glial cell plasticity. Pain 164(4): 728–740. https://doi.org/10.1097/j.pain.0000000000002758
  55. Renthal W, Tochitsky I, Yang L, Cheng YC, Li E., Kawaguchi R, Geschwind DH, Woolf CJ (2020) Transcriptional Reprogramming of Distinct Peripheral Sensory Neuron Subtypes after Axonal Injury. Neuron 108(1): 128–144.e9. https://doi.org/10.1016/j.neuron.2020.07.026
  56. Krishnan A, Areti A, Komirishetty P, Chandrasekhar A, Cheng C, Zochodne DW (2022) Survival of compromised adult sensory neurons involves macrovesicular formation. Cell Death Discov 8: 462. https://doi.org/10.1038/s41420-022-01247-3
  57. Hanani M, Spray DC (2013) Glial Cells in Autonomic and Sensory Ganglia. In: Kettenmann H RB (Eds) Neuroglia. Oxford Univer Press. 122–133.
  58. Nascimento DS, Castro-Lopes JM, Moreira Neto FL (2014) Satellite glial cells surrounding primary afferent neurons are activated and proliferate during monoarthritis in rats: is there a role for ATF3? PLoS One 9(9): e108152 https://doi.org/10.1371/journal.pone.0108152
  59. Zhang L, Xie R, Yang J, Zhao Y, Qi C, Bian G, Wang M, Shan J, Wang C, Wang D, Luo C, Wang Y, Wu S (2019) Chronic pain induces nociceptive neurogenesis in dorsal root ganglia from Sox2-positive satellite cells. Glia 67(6): 1062–1075. https://doi.org/10.1002/glia.23588
  60. Huang B, Zdora I, de Buhr N, Lehmbecker A, Baumgärtner W, Leitzen E (2021) Phenotypical peculiarities and species-specific differences of canine and murine satellite glial cells of spinal ganglia. J Cell Mol Med 25(14): 6909–6924. https://doi.org/10.1111/jcmm.16701
  61. Avraham O, Deng PY, Jones S, Kuruvilla R, Semenkovich CF, Klyachko VA, Cavalli V (2020) Satellite glial cells promote regenerative growth in sensory neurons. Nat Commun 11(1): 4891. https://doi.org/10.1038/s41467-020-18642-y
  62. Jager SE, Pallesen LT, Richner M, Harley P, Hore Z, McMahon S, Denk F, Vaegter CB (2020) Changes in the transcriptional fingerprint of satellite glial cells following peripheral nerve injury. Glia 68(7): 1375–1395. https://doi.org/10.1002/glia.23785
  63. Hanani M (2022) How Is Peripheral Injury Signaled to Satellite Glial Cells in Sensory Ganglia? Cells 11(3): 512. https://doi.org/10.3390/cells11030512
  64. Steward O, Torre ER, Tomasulo R, Lothman E (1991) Neuronal activity up-regulates astroglial gene expression. Proc Natl Acad Sci U S A 88(15): 6819–6823.
  65. Christie K, Koshy D, Cheng C, Guo G, Martinez JA, Duraikannu A, Zochodne DW (2015) Intraganglionic interactions between satellite cells and adult sensory neurons. Mol Cell Neurosci 67:1–12. https://doi.org/10.1016/j.mcn.2015.05.001
  66. Wang F, Xiang H, Fischer G, Liu Z, Dupont MJ, Hogan QH, Yu HH (2016) MG-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 1652: 62–70. https://doi.org/10.1016/j.brainres.2016.09.032
  67. Zeisel A, Hochgerner H, Lönnerberg P, Johnsson A, Memic F, van der Zwan J, Häring M, Braun E, Borm LE, La Manno G, Codeluppi S, Furlan A, Lee K, Skene N, Harris KD, Hjerling-Leffler J, Arenas E, Ernfors P, Marklund U, Linnarsson S (2018) Molecular architecture of the mouse nervous system. Cell 174(4): 999–1014.e22. https://doi.org/10.1016/j.cell.2018.06.021
  68. Carlin D, Halevi AE, Ewan EE, Moore AM, Cavalli V (2019) Nociceptor deletion of Tsc2 enhances axon regeneration by inducing a conditioning injury response in dorsal root ganglia. eNeuro 6(3): ENEURO.0168–19.2019. https://doi.org/10.1523/ENEURO.0168-19.2019
  69. Petrova ES (2019) Current views on Schwann cells: development, plasticity, functions. J Evol Biochem Physiol 55(6): 433–447. https://doi.org/10.1134/S0022093019060012
  70. Pannese E (1994) Neurocytology: Fine Structure of Neurons, Nerve Processes, and Neuroglial Cells. G. Thieme Verlag, Stuttgart. Thieme Med Publ. New York.
  71. Campana WM (2007) Schwann cells: activated peripheral glia and their role in neuropathic pain. Brain Behav Immun 21(5): 522–527. https://doi.org/10.1016/j.bbi.2006.12.008
  72. Gomez-Sanchez JA, Pilch KS, van der Lans M, Fazal SV, Benito C, Wagstaff LJ, Mirsky R, Jessen KR (2017) After Nerve Injury, Lineage Tracing Shows That Myelin and Remak Schwann Cells Elongate Extensively and Branch to Form Repair Schwann Cells, Which Shorten Radically on Remyelination. J Neurosci 37(37): 9086–9099. https://doi.org/10.1523/JNEUROSCI.1453–17.2017
  73. Петрова ЕС, Колос ЕА (2023) Морфологическое исследование процессов валлеровской дегенерации в седалищном нерве крысы после механического повреждения. Клин экспер морфол 12(4): 62–70. [Petrova ES, Kolos EA (2023) Morphological study of Wallerian processes degeneration in the rat sciatic nerve after mechanical injury. Klin eksp morfol 12(4): 62–70. (In Russ)]. https://doi.org/10.31088/cem2023.12.4.62-70
  74. Triolo D, Dina G, Lorenzetti I, Malaguti M, Morana P, Del Carro U, Comi G, Messing A, Quattrini A, Previtali SC (2006) Loss of glial fibrillary acidic protein (GFAP) impairs Schwann cell proliferation and delays nerve regeneration after damage. J Cell Sci 119(Pt 19): 3981–3993. https://doi.org/10.1242/jcs.03168
  75. Berg A, Zelano J, Pekna M, Wilhelmsson U, Pekny M, Cullheim S (2013) Axonal regeneration after sciatic nerve lesion is delayed but complete in GFAP- and vimentin-deficient mice. PLoS One 8(11): e79395. https://doi.org/10.1371/journal.pone.0079395
  76. Ko CP, Robitaille R (2015) Perisynaptic Schwann Cells at the Neuromuscular Synapse: Adaptable, Multitasking Glial Cells. Cold Spring Harb Perspect Biol 7(10): a020503. https://doi.org/10.1101/cshperspect.a020503
  77. Fields RD (2009) Schwann Cells and Axon Relationship. In: Larry R Squire (Ed) Encyclopedia of Neuroscience. Acad Press. 485–489. https://doi.org/10.1016/B978-008045046-9.00698-7
  78. Reed CB, Feltri ML, Wilson ER (2022) Peripheral glia diversity. J Anat 241(5): 1219–1234. https://doi.org/10.1111/joa.13484
  79. Hastings RL, Mikesh M, Lee YI, Thompson WJ (2020) Morphological remodeling during recovery of the neuromuscular junction from terminal Schwann cell ablation in adult mice. Sci Rep 10(1): 11132. https://doi.org/10.1038/s41598-020-67630-1
  80. Powell JA, Molgó J, Adams DS, Colasante C, Williams A, Bohlen M, Jaimovich E (2003) IP3 receptors and associated Ca2+ signals localize to satellite cells and to components of the neuromuscular junction in skeletal muscle. J Neurosci 10(23): 8185–8192. https://doi.org/10.1523/JNEUROSCI.23-23-08185.2003
  81. Liu JX, Brännström T, Andersen PM, Pedrosa-Domellöf F (2013) Distinct changes in synaptic protein composition at neuromuscular junctions of extraocular muscles versus limb muscles of ALS donors. PLoS One 8(2): e57473. https://doi.org/10.1371/journal.pone.0057473
  82. Günther HS, Henne S, Oehlmann J, Urban J, Pleizier D, Renevier N, Lohr C, Wülfing C (2021) GFAP and desmin expression in lymphatic tissues leads to difficulties in distinguishing between glial and stromal cells. Sci Rep 11(1): 13322. https://doi.org/10.1038/s41598-021-92364-z
  83. Kolos EA, Korzhevskii DE (2021) Glutamine Synthetase in the Cells of the Developing Rat Spinal Cord. Russ J Dev Biol 52: 334–343. https://doi.org/10.1134/S1062360421050040
  84. Radomska KJ, Topilko P (2017) Boundary cap cells in development and disease. Curr Opin Neurobiol 47: 209–215. https://doi.org/10.1016/j.conb.2017.11.003

Arquivos suplementares

Arquivos suplementares
Ação
1. JATS XML
2. Fig. 1. Astrocyte-like glial cells in the ganglia of the intermuscular plexus. N – neurons; I – interganglionic cord; M – muscles; LC – lymphatic capillary; AG – aganglionic region. Immunohistochemical reaction to GFAP, ×400 (figure from the article by Chumasov et al., 2023 [41]).

Baixar (809KB)
3. Fig. 2. Increase in GFAP-immunopositive satellite cells in DRG during aging. (a) – three-month-old rat; (b) – 18-month-old rat. Immunohistochemical reaction for GFAP, ×400. Own data.

Baixar (526KB)
4. Fig. 3. Schwann cells (repair Schwann cells) in the distal segment of the injured rat nerve 7 days after surgery (ligature, 40 s). (a) – general view of the distal segment of the nerve, longitudinal section, (b) – fragment of endoneurium with Schwann cells, (c) – mitotically dividing (m) Schwann cell. En – endoneurium of the rat sciatic nerve. Immunohistochemical reaction to GFAP. Visualization with TRITC fluorochrome (red), staining of nuclei with DAPI (blue), ×100 (a), ×400 (b), ×600 (c) (figure from the article by Petrova E.S., Kolos E.A. [73]).

Baixar (1MB)

Declaração de direitos autorais © Russian Academy of Sciences, 2024