Astrocyte reactivity in the glia limitans superficialis of the rat medial prefrontal cortex following sciatic nerve injury
Jazyk angličtina Země Německo Médium print-electronic
Typ dokumentu časopisecké články
PubMed
36326875
DOI
10.1007/s00418-022-02161-6
PII: 10.1007/s00418-022-02161-6
Knihovny.cz E-zdroje
- Klíčová slova
- Glial fibrillary acidic protein, Glutamine synthetase, NFκBp65, Peripheral nerve lesion, Reactive astrocytes,
- MeSH
- astrocyty * metabolismus patologie MeSH
- gliový fibrilární kyselý protein metabolismus MeSH
- krysa rodu Rattus MeSH
- nervus ischiadicus zranění metabolismus MeSH
- poranění periferního nervu * metabolismus MeSH
- prefrontální mozková kůra metabolismus MeSH
- zvířata MeSH
- Check Tag
- krysa rodu Rattus MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- gliový fibrilární kyselý protein MeSH
The glia limitans superficialis (GLS) on the rodent cortical surface consists of astrocyte bodies intermingled with their cytoplasmic processes. Many studies have observed astrocyte reactivity in the medial prefrontal cortex (mPFC) parenchyma induced by a peripheral nerve injury, while the response of GLS astrocytes is still not fully understood. The aim of our study was to identify the reactivity of rat GLS astrocytes in response to sciatic nerve compression (SNC) over different time periods. The alteration of GLS astrocyte reactivity was monitored using immunofluorescence (IF) intensities of glial fibrillary acidic protein (GFAP), glutamine synthetase (GS), and NFκBp65. Our results demonstrated that SNC induced GLS astrocyte reactivity seen as increased intensities of GFAP-IF, and longer extensions of cytoplasmic processes into lamina I. First significant increase of GFAP-IF was observed on post-operation day 7 (POD7) after SNC with further increases on POD14 and POD21. In contrast, dynamic alteration of the extension of cytoplasmic processes into lamina I was detected as early as POD1 and continued throughout the monitored survival periods of both sham and SNC operations. The reactivity of GLS astrocytes was not associated with their proliferation. In addition, GLS astrocytes also displayed a significant decrease in GS immunofluorescence (GS-IF) and NFκB immunofluorescence (NFκB-IF) in response to sham and SNC operation compared with naïve control rats. These results suggest that damaged peripheral tissues (following sham operation as well as peripheral nerve lesions) may induce significant changes in GLS astrocyte reactivity. The signaling mechanism from injured peripheral tissue and nerve remains to be elucidated.
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Abbott NJ, Pizzo ME, Preston JE et al (2018) The role of brain barriers in fluid movement in the CNS: is there a ‘glymphatic’ system? Acta Neuropathol 135:387–407. https://doi.org/10.1007/s00401-018-1812-4 DOI
Aldskogius H, Kozlova EN (1998) Central neuron–glial and glial–glial interactions following axon injury. Prog Neurobiol 55:1–26. https://doi.org/10.1016/S0301-0082(97)00093-2 DOI
Almeida TF, Roizenblatt S, Tufik S (2004) Afferent pain pathways: a neuroanatomical review. Brain Res 1000:40–56. https://doi.org/10.1016/j.brainres.2003.10.073 DOI
Anastasiades PG, Carter AG (2021) Circuit organization of the rodent medial prefrontal cortex. Trends Neurosci 44:550–563. https://doi.org/10.1016/j.tins.2021.03.006 DOI
Anlauf E, Derouiche A (2013) Glutamine synthetase as an astrocytic marker: its cell type and vesicle localization. Front Endocrinol 4:144. https://doi.org/10.3389/fendo.2013.00144 DOI
Blom SM, Pfister J-P, Santello M et al (2014) Nerve injury-induced neuropathic pain causes disinhibition of the anterior cingulate cortex. J Neurosci 34:5754–5764. https://doi.org/10.1523/JNEUROSCI.3667-13.2014 DOI
Brøchner CB, Holst CB, Møllgård K (2015) Outer brain barriers in rat and human development. Front Neurosci 9:75. https://doi.org/10.3389/fnins.2015.00075 DOI
Chaboub LS, Deneen B (2012) Developmental origins of astrocyte heterogeneity: the final frontier of CNS development. Dev Neurosci 34:379–388. https://doi.org/10.1159/000343723 DOI
Chaudhry F, Lehre K, Campagne M et al (1995) Glutamate transporters in glial plasma-membranes—highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15:711–720. https://doi.org/10.1016/0896-6273(95)90158-2 DOI
Chen L-F, Greene WC (2004) Shaping the nuclear action of NF-κB. Nat Rev Mol Cell Biol 5:392–401. https://doi.org/10.1038/nrm1368 DOI
Chen F-L, Dong Y-L, Zhang Z-J et al (2012) Activation of astrocytes in the anterior cingulate cortex contributes to the affective component of pain in an inflammatory pain model. Brain Res Bull 87:60–66. https://doi.org/10.1016/j.brainresbull.2011.09.022 DOI
Cho J, Huh Y (2020) Astrocytic calcium dynamics along the pain pathway. Front Cell Neurosci 14:594216. https://doi.org/10.3389/fncel.2020.594216 DOI
Chowdhury GMI, Patel AB, Mason GF et al (2007) Glutamatergic and GABAergic neurotransmitter cycling and energy metabolism in rat cerebral cortex during postnatal development. J Cereb Blood Flow Metab 27:1895–1907. https://doi.org/10.1038/sj.jcbfm.9600490 DOI
Chu Sin Chung P, Panigada T, Cardis R et al (2017) Peripheral nerve injury induces a transitory microglial reaction in the rat infralimbic cortex. Neurosci Lett 655:14–20. https://doi.org/10.1016/j.neulet.2017.06.037 DOI
Colombo E, Farina C (2016) Astrocytes: key regulators of neuroinflammation. Trends Immunol 37:608–620. https://doi.org/10.1016/j.it.2016.06.006 DOI
Coulter DA, Steinhauser C (2015) Role of astrocytes in epilepsy. CSH Perspect Med 5:a022434–a022434. https://doi.org/10.1101/cshperspect.a022434 DOI
Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1–105. https://doi.org/10.1016/S0301-0082(00)00067-8 DOI
Dellarole A, Morton P, Brambilla R et al (2014) Neuropathic pain-induced depressive-like behavior and hippocampal neurogenesis and plasticity are dependent on TNFR1 signaling. Brain Behav Immun 41:65–81. https://doi.org/10.1016/j.bbi.2014.04.003 DOI
Dubový P (2002) Computer-assisted quantitative analysis of immunofluorescence staining of the extracellular matrix in rat dorsal and ventral spinal roots. Acta Histochem 104:371–374. https://doi.org/10.1078/0065-1281-00664 DOI
Eid T, Tu N, Lee T-SW, Lai JCK (2013) Regulation of astrocyte glutamine synthetase in epilepsy. Neurochem Int 63:670–681. https://doi.org/10.1016/j.neuint.2013.06.008 DOI
Emsley JG, Macklis JD (2006) Astroglial heterogeneity closely reflects the neuronal-defined anatomy of the adult murine CNS. Neuron Glia Biol 2:175–186. https://doi.org/10.1017/S1740925X06000202 DOI
Engelhardt B, Coisne C (2011) Fluids and barriers of the CNS establish immune privilege by confining immune surveillance to a two-walled castle moat surrounding the CNS castle. Fluids Barriers CNS 8:1–9. https://doi.org/10.1186/2045-8118-8-4 DOI
Escartin C, Galea E, Lakatos A et al (2021) Reactive astrocyte nomenclature, definitions, and future directions. Nat Neurosci 24:312–325. https://doi.org/10.1038/s41593-020-00783-4 DOI
Eto K, Kim SK, Takeda I, Nabekura J (2018) The roles of cortical astrocytes in chronic pain and other brain pathologies. Neurosci Res 126:3–8. https://doi.org/10.1016/j.neures.2017.08.009 DOI
Falcone C, Wolf-Ochoa M, Amina S et al (2019) Cortical interlaminar astrocytes across the therian mammal radiation. J Comp Neur 527:1654–1674. https://doi.org/10.1002/cne.24605 DOI
Falcone C, Penna E, Hong T et al (2021) Cortical interlaminar astrocytes are generated prenatally, mature postnatally, and express unique markers in human and nonhuman primates. Cereb Cortex 31:379–395. https://doi.org/10.1093/cercor/bhaa231 DOI
Farina C, Aloisi F, Meinl E (2007) Astrocytes are active players in cerebral innate immunity. Trends Immun 28:138–145. https://doi.org/10.1016/j.it.2007.01.005 DOI
Feig SL, Haberly LB (2011) Surface-associated astrocytes, not endfeet, form the glia limitans in posterior piriform cortex and have a spatially distributed, not a domain, organization. J Comp Neur 519:1952–1969. https://doi.org/10.1002/cne.22615 DOI
Fiore NT, Austin PJ (2019) Peripheral nerve injury triggers neuroinflammation in the medial prefrontal cortex and ventral hippocampus in a subgroup of rats with coincident affective behavioural changes. Neuroscience 416:147–167. https://doi.org/10.1016/j.neuroscience.2019.08.005 DOI
Ghosh G, Wang VY-F, Huang D-B, Fusco A (2012) NF-κB regulation: lessons from structures. Immunol Rev 246:36–58. https://doi.org/10.1111/j.1600-065X.2012.01097.x DOI
Guida F, Luongo L, Marmo F et al (2015) Palmitoylethanolamide reduces pain-related behaviors and restores glutamatergic synapses homeostasis in the medial prefrontal cortex of neuropathic mice. Mol Brain 8:47. https://doi.org/10.1186/s13041-015-0139-5 DOI
Hansson E, Muyderman H, Leonova J et al (2000) Astroglia and glutamate in physiology and pathology: aspects on glutamate transport, glutamate-induced cell swelling and gap-junction communication. Neurochem Int 37:317–329. https://doi.org/10.1016/S0197-0186(00)00033-4 DOI
Hayden MS, Ghosh S (2008) Shared principles in NF-kappaB signaling. Cell 132:344–362. https://doi.org/10.1016/j.cell.2008.01.020 DOI
Hung K-L, Wang S-J, Wang Y-C et al (2014) Upregulation of presynaptic proteins and protein kinases associated with enhanced glutamate release from axonal terminals (synaptosomes) of the medial prefrontal cortex in rats with neuropathic pain. Pain 155:377–387. https://doi.org/10.1016/j.pain.2013.10.026 DOI
Joukal M, Klusáková I, Solár P et al (2016) Cellular reactions of the choroid plexus induced by peripheral nerve injury. Neurosci Lett 628:73–77. https://doi.org/10.1016/j.neulet.2016.06.019 DOI
Lattke M, Reichel SN, Magnutzki A et al (2017) Transient IKK2 activation in astrocytes initiates selective non-cell-autonomous neurodegeneration. Mol Neurodegener 12:16. https://doi.org/10.1186/s13024-017-0157-0 DOI
Lim TKY, Shi XQ, Martin HC et al (2014) Blood–nerve barrier dysfunction contributes to the generation of neuropathic pain and allows targeting of injured nerves for pain relief. Pain 155:954–967. https://doi.org/10.1016/j.pain.2014.01.026 DOI
Liu X, Zhang Z, Guo W et al (2013) The superficial glia limitans of mouse and monkey brain and spinal cord: glia limitans of brain and spinal cord. Anat Rec 296:995–1007. https://doi.org/10.1002/ar.22717 DOI
Mahmoud S, Gharagozloo M, Simard C, Gris D (2019) Astrocytes maintain glutamate homeostasis in the CNS by controlling the balance between glutamate uptake and release. Cells 8:184. https://doi.org/10.3390/cells8020184 DOI
Mémet S (2006) NF-κB functions in the nervous system: from development to disease. Biochem Pharmacol 72:1180–1195. https://doi.org/10.1016/j.bcp.2006.09.003 DOI
Miguel-Hidalgo JJ, Waltzer R, Whittom AA et al (2010) Glial and glutamatergic markers in depression, alcoholism, and their comorbidity. J Affect Disord 127:230–240. https://doi.org/10.1016/j.jad.2010.06.003 DOI
Miller SJ (2018) Astrocyte heterogeneity in the adult central nervous system. Front Cell Neurosci 12:401. https://doi.org/10.3389/fncel.2018.00401 DOI
Morel L, Chiang MSR, Higashimori H et al (2017) Molecular and functional properties of regional astrocytes in the adult brain. J Neurosci 37:8706–8717. https://doi.org/10.1523/JNEUROSCI.3956-16.2017 DOI
Morel L, Men Y, Chiang MSR et al (2019) Intracortical astrocyte subpopulations defined by astrocyte reporter mice in the adult brain. Glia 67:171–181. https://doi.org/10.1002/glia.23545 DOI
Narita M, Kuzumaki N, Narita M et al (2006) Chronic pain-induced emotional dysfunction is associated with astrogliosis due to cortical δ-opioid receptor dysfunction. J Neurochem 97:1369–1378. https://doi.org/10.1111/j.1471-4159.2006.03824.x DOI
Norenberg MD (1979) Distribution of glutamine synthetase in the rat central nervous system. J Histochem Cytochem 27:756–762. https://doi.org/10.1177/27.3.39099 DOI
Ortinski PI, Dong J, Mungenast A et al (2010) Selective induction of astrocytic gliosis generates deficits in neuronal inhibition. Nat Neurosci 13:584–591. https://doi.org/10.1038/nn.2535 DOI
Papageorgiou IE, Gabriel S, Fetani AF et al (2011) Redistribution of astrocytic glutamine synthetase in the hippocampus of chronic epileptic rats. Glia 59:1706–1718. https://doi.org/10.1002/glia.21217 DOI
Pasti L, Zonta M, Pozzan T et al (2001) Cytosolic calcium oscillations in astrocytes may regulate exocytotic release of glutamate. J Neurosci 21:477–484. https://doi.org/10.1523/JNEUROSCI.21-02-00477.2001 DOI
Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates. Elsevier Academic Press, San Diego
Pekny M, Pekna M (2004) Astrocyte intermediate filaments in CNS pathologies and regeneration. J Pathol 204:428–437. https://doi.org/10.1002/path.1645 DOI
Peters A, Palay S, Webster H (1991) The fine structure of the nervous system: neurons and their supporting cells. Oxford University Press, New York
Pradère J-P, Hernandez C, Koppe C et al (2016) Negative regulation of NF-κB p65 activity by serine 536 phosphorylation. Sci Signal. https://doi.org/10.1126/scisignal.aab2820 DOI
Rakic P (2003) Elusive radial glial cells: historical and evolutionary perspective. Glia 43:19–32. https://doi.org/10.1002/glia.10244 DOI
Sang K, Bao C, Xin Y et al (2018) Plastic change of prefrontal cortex mediates anxiety-like behaviors associated with chronic pain in neuropathic rats. Mol Pain 14:1744806918783931. https://doi.org/10.1177/1744806918783931 DOI
Schiweck J, Eickholt BJ, Murk K (2018) Important shapeshifter: mechanisms allowing astrocytes to respond to the changing nervous system during development, injury and disease. Front Cell Neurosci 12:261. https://doi.org/10.3389/fncel.2018.00261 DOI
Seltzer Z, Dubner R, Shir Y (1990) A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43:205–218. https://doi.org/10.1016/0304-3959(90)91074-S DOI
Semyanov A, Verkhratsky A (2021) Astrocytic processes: from tripartite synapses to the active milieu. Trends Neurosci 44:781–792. https://doi.org/10.1016/j.tins.2021.07.006 DOI
Shlosberg D, Patrick SL, Buskila Y, Amitai Y (2003) Inhibitory effect of mouse neocortex layer I on the underlying cellular network. Eur J Neurosci 18:2751–2759. https://doi.org/10.1111/j.1460-9568.2003.03016.x DOI
Svíženská IH, Brázda V, Klusáková I, Dubový P (2013) Bilateral changes of cannabinoid receptor type 2 protein and mRNA in the dorsal root ganglia of a rat neuropathic pain model. J Histochem Cytochem 61:529–547. https://doi.org/10.1369/0022155413491269 DOI
Tang J, Bair M, Descalzi G (2021) Reactive astrocytes: critical players in the development of chronic pain. Front Psychiatry 12:682056. https://doi.org/10.3389/fpsyt.2021.682056 DOI
van der Hel WS, Notenboom RGE, Bos IWM et al (2005) Reduced glutamine synthetase in hippocampal areas with neuron loss in temporal lobe epilepsy. Neurology 64:326–333. https://doi.org/10.1212/01.WNL.0000149636.44660.99 DOI
Verkhratsky A, Nedergaard M (2018) Physiology of astroglia. Physiol Rev 98:239–389. https://doi.org/10.1152/physrev.00042.2016 DOI
Villarreal A, Vidos C, Monteverde Busso M et al (2021) Pathological neuroinflammatory conversion of reactive astrocytes is induced by microglia and involves chromatin remodeling. Front Pharmacol 12:689346. https://doi.org/10.3389/fphar.2021.689346 DOI
Wei F, Guo W, Zou S et al (2008) Supraspinal glial–neuronal interactions contribute to descending pain facilitation. J Neurosci 28:10482–10495. https://doi.org/10.1523/JNEUROSCI.3593-08.2008 DOI
Yamashita A, Hamada A, Suhara Y et al (2014) Astrocytic activation in the anterior cingulate cortex is critical for sleep disorder under neuropathic pain. Synapse 68:235–247. https://doi.org/10.1002/syn.21733 DOI
Yoon H, Walters G, Paulsen AR, Scarisbrick IA (2017) Astrocyte heterogeneity across the brain and spinal cord occurs developmentally, in adulthood and in response to demyelination. PLoS ONE 12:e0180697. https://doi.org/10.1371/journal.pone.0180697 DOI
Zamboni L, Demartin.c, (1967) Buffered picric acid-formaldehyde—a new rapid fixative for electron microscopy. J Cell Biol 35:148A
Zhang Y, Reichel JM, Han C et al (2017) Astrocytic process plasticity and IKKβ/NF-κB in central control of blood glucose, blood pressure, and body weight. Cell Metab 25:1091–1102. https://doi.org/10.1016/j.cmet.2017.04.002 DOI
Zhuo M (2016) Neural mechanisms underlying anxiety–chronic pain interactions. Trends Neurosci 39:136–145. https://doi.org/10.1016/j.tins.2016.01.006 DOI