دورية أكاديمية
أعرض في EDS

Temporal-Specific Sex and Injury-Dependent Changes on Neurogranin-Associated Synaptic Signaling After Controlled Cortical Impact in Rats.

التفاصيل البيبلوغرافية
العنوان: Temporal-Specific Sex and Injury-Dependent Changes on Neurogranin-Associated Synaptic Signaling After Controlled Cortical Impact in Rats.
المؤلفون: Svirsky SE; Center for Neuroscience, University of Pittsburgh, Pittsburgh, PA, USA.; Department of Neurological Surgery, University of Pittsburgh Medical Center, 4401 Penn Ave, Pittsburgh, PA, 15224, USA., Henchir J; Department of Neurological Surgery, University of Pittsburgh Medical Center, 4401 Penn Ave, Pittsburgh, PA, 15224, USA., Li Y; Department of Neurological Surgery, University of Pittsburgh Medical Center, 4401 Penn Ave, Pittsburgh, PA, 15224, USA., Carlson SW; Department of Neurological Surgery, University of Pittsburgh Medical Center, 4401 Penn Ave, Pittsburgh, PA, 15224, USA., Dixon CE; Center for Neuroscience, University of Pittsburgh, Pittsburgh, PA, USA. dixoec@upmc.edu.; Department of Neurological Surgery, University of Pittsburgh Medical Center, 4401 Penn Ave, Pittsburgh, PA, 15224, USA. dixoec@upmc.edu.; V.A. Pittsburgh Healthcare System, Pittsburgh, PA, USA. dixoec@upmc.edu.
المصدر: Molecular neurobiology [Mol Neurobiol] 2024 Sep; Vol. 61 (9), pp. 7256-7268. Date of Electronic Publication: 2024 Feb 20.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Humana Press Country of Publication: United States NLM ID: 8900963 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1559-1182 (Electronic) Linking ISSN: 08937648 NLM ISO Abbreviation: Mol Neurobiol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Clifton, NJ : Humana Press, c1987-
مواضيع طبية MeSH: Brain Injuries, Traumatic*/metabolism , Brain Injuries, Traumatic*/pathology , Brain Injuries, Traumatic*/complications , Calcium-Calmodulin-Dependent Protein Kinase Type 2*/metabolism , Hippocampus*/metabolism , Hippocampus*/pathology , Neurogranin*/metabolism , Rats, Sprague-Dawley* , Signal Transduction*/physiology , Synapses*/metabolism , Synapses*/pathology, Animals ; Female ; Male ; Rats ; Calmodulin/metabolism ; Cerebral Cortex/metabolism ; Cerebral Cortex/pathology ; Phosphorylation ; Sex Characteristics ; Synaptosomes/metabolism ; Time Factors
مستخلص: Extensive effort has been made to study the role of synaptic deficits in cognitive impairment after traumatic brain injury (TBI). Neurogranin (Ng) is a calcium-sensitive calmodulin (CaM)-binding protein essential for Ca 2+ /CaM-dependent kinase II (CaMKII) autophosphorylation which subsequently modulates synaptic plasticity. Given the loss of Ng expression after injury, additional research is warranted to discern changes in hippocampal post-synaptic signaling after TBI. Under isoflurane anesthesia, adult, male and female Sprague-Dawley rats received a sham/control or controlled cortical impact (CCI) injury. Ipsilateral hippocampal synaptosomes were isolated at 24 h and 1, 2, and 4 weeks post-injury, and western blot was used to evaluate protein expression of Ng-associated signaling proteins. Non-parametric Mann-Whitney tests were used to determine significance of injury for each sex at each time point. There were significant changes in the hippocampal synaptic expression of Ng and associated synaptic proteins such as phosphorylated Ng, CaMKII, and CaM up to 4 weeks post-CCI, demonstrating TBI alters hippocampal post-synaptic signaling. This study furthers our understanding of mechanisms of cognitive dysfunction within the synapse sub-acutely after TBI.
(© 2024. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.)
References: Lundin A, de Boussard C, Edman G, Borg J (2006) Symptoms and disability until 3 months after mild TBI. Brain Inj 20:799–806. https://doi.org/10.1080/02699050600744327. (PMID: 17060147)
Arciniegas DB, Held K, Wagner P (2002) Cognitive impairment following traumatic brain injury. Curr Treat Options Neurol 4:43–57. (PMID: 11734103)
Cristofori I, Levin HS (2015) Traumatic brain injury and cognition. Handb Clin Neurol 128:579–611. https://doi.org/10.1016/B978-0-444-63521-1.00037-6. (PMID: 25701909)
Levin HS (1998) Cognitive function outcomes after traumatic brain injury. Curr Opin Neurol 11:643–646. (PMID: 9870131)
Rabinowitz AR, Levin HS (2014) Cognitive sequelae of traumatic brain injury. Psychiatr Clin North Am 37:1–11. https://doi.org/10.1016/j.psc.2013.11.004. (PMID: 245294203927143)
Stocchetti N, Zanier ER (2016) Chronic impact of traumatic brain injury on outcome and quality of life: a narrative review. Crit Care 20 https://doi.org/10.1186/s13054-016-1318-1.
Pagulayan KF, Temkin NR, Machamer JE, Dikmen SS (2007) The measurement and magnitude of awareness difficulties after traumatic brain injury: a longitudinal study. J Int Neuropsychol Soc 13:561–570. https://doi.org/10.1017/S1355617707070713. (PMID: 17521477)
Mayford M, Siegelbaum SA, Kandel ER (2012) Synapses and memory storage. Cold Spring Harb Perspect Biol 4 https://doi.org/10.1101/cshperspect.a005751.
Tang-Schomer MD, Johnson VE, Baas PW et al (2012) Partial interruption of axonal transport due to microtubule breakage accounts for the formation of periodic varicosities after traumatic axonal injury. Exp Neurol 233:364–372. https://doi.org/10.1016/j.expneurol.2011.10.030. (PMID: 22079153)
Sullivan PG, Keller JN, Mattson MP, Scheff SW (1998) Traumatic brain injury alters synaptic homeostasis: implications for impaired mitochondrial and transport function. J Neurotrauma 15:789–798. https://doi.org/10.1089/neu.1998.15.789. (PMID: 9814635)
Ansari MA, Roberts KN, Scheff SW (2008) Oxidative stress and modification of synaptic proteins in hippocampus after traumatic brain injury. Free Radic Biol Med 45:443–452. https://doi.org/10.1016/j.freeradbiomed.2008.04.038. (PMID: 185012002586827)
Burda JE, Bernstein AM, Sofroniew MV (2016) Astrocyte roles in traumatic brain injury. Exp Neurol 275:305–315. https://doi.org/10.1016/j.expneurol.2015.03.020. (PMID: 25828533)
Winston CN, Chellappa D, Wilkins T et al (2013) Controlled cortical impact results in an extensive loss of dendritic spines that is not mediated by injury-induced amyloid-beta accumulation. J Neurotrauma 30:1966–1972. https://doi.org/10.1089/neu.2013.2960. (PMID: 238795603837436)
Gao X, Deng P, Xu ZC, Chen J (2011) Moderate traumatic brain injury causes acute dendritic and synaptic degeneration in the hippocampal dentate gyrus. PLoS ONE 6 https://doi.org/10.1371/journal.pone.0024566.
Gobbel GT, Bonfield C, Carson-Walter EB, Adelson PD (2007) Diffuse alterations in synaptic protein expression following focal traumatic brain injury in the immature rat. Childs Nerv Syst 23:1171–1179. https://doi.org/10.1007/s00381-007-0345-2. (PMID: 17457592)
Campbell JN, Low B, Kurz JE et al (2012) Mechanisms of dendritic spine remodeling in a rat model of traumatic brain injury. J Neurotrauma 29:218–234. https://doi.org/10.1089/neu.2011.1762. (PMID: 218385183261790)
Zhang Y, Chopp M, Rex CS et al (2018) A small molecule spinogenic compound enhances functional outcome and dendritic spine plasticity in a rat model of traumatic brain injury. J Neurotrauma 36:589–600. https://doi.org/10.1089/neu.2018.5790. (PMID: 30014757)
D’Ambrosio R, Maris DO, Grady MS et al (1998) Selective loss of hippocampal long-term potentiation, but not depression, following fluid percussion injury. Brain Res 786:64–79. https://doi.org/10.1016/S0006-8993(97)01412-1. (PMID: 9554957)
Miyazaki S, Katayama Y, Lyeth BG et al (1992) Enduring suppression of hippocampal long-term potentiation following traumatic brain injury in rat. Brain Res 585:335–339. https://doi.org/10.1016/0006-8993(92)91232-4. (PMID: 1511317)
Sanders MJ, Sick TJ, Perez-Pinzon MA et al (2000) Chronic failure in the maintenance of long-term potentiation following fluid percussion injury in the rat. Brain Res 861:69–76. https://doi.org/10.1016/S0006-8993(00)01986-7. (PMID: 10751566)
Schwarzbach E, Bonislawski DP, Xiong G, Cohen AS (2006) Mechanisms underlying the inability to induce area CA1 LTP in the mouse after traumatic brain injury. Hippocampus 16:541–550. https://doi.org/10.1002/hipo.20183. (PMID: 166340773951737)
Sick TJ, Pérez-Pinzón MA, Feng Z-Z (1998) Impaired expression of long-term potentiation in hippocampal slices 4 and 48 h following mild fluid-percussion brain injury in vivo. Brain Res 785:287–292. https://doi.org/10.1016/S0006-8993(97)01418-2. (PMID: 9518654)
Vogel EW, Rwema SH, Meaney DF et al (2016) Primary blast injury depressed hippocampal long-term potentiation through disruption of synaptic proteins. J Neurotrauma 34:1063–1073. https://doi.org/10.1089/neu.2016.4578. (PMID: 27573357)
Norris CM, Scheff SW (2009) Recovery of afferent function and synaptic strength in hippocampal CA1 following traumatic brain injury. J Neurotrauma 26:2269–2278. https://doi.org/10.1089/neu.2009.1029. (PMID: 196040982824230)
Reeves TM, Lyeth BG, Povlishock JT (1995) Long-term potentiation deficits and excitability changes following traumatic brain injury. Exp Brain Res 106:248–256. (PMID: 8566189)
Albensi BC, Sullivan PG, Thompson MB et al (2000) Cyclosporin ameliorates traumatic brain-injury-induced alterations of hippocampal synaptic plasticity. Exp Neurol 162:385–389. https://doi.org/10.1006/exnr.1999.7338. (PMID: 10739643)
Bonini JS, Da Silva WC, Bevilaqua LRM et al (2007) On the participation of hippocampal PKC in acquisition, consolidation and reconsolidation of spatial memory. Neuroscience 147:37–45. https://doi.org/10.1016/j.neuroscience.2007.04.013. (PMID: 17499932)
Alkon DL, Epstein H, Kuzirian A et al (2005) Protein synthesis required for long-term memory is induced by PKC activation on days before associative learning. Proc Natl Acad Sci 102:16432–16437. https://doi.org/10.1073/pnas.0508001102. (PMID: 162580641283453)
Noguès X (1997) Protein kinase C, Learning and memory: a circular determinism between physiology and behaviour. Prog Neuropsychopharmacol Biol Psychiatry 21:507–529. https://doi.org/10.1016/S0278-5846(97)00015-8. (PMID: 9153070)
Lledo PM, Hjelmstad GO, Mukherji S et al (1995) Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. Proc Natl Acad Sci USA 92:11175–11179. (PMID: 747996040594)
Tan S-E, Liang K-C (1996) Spatial learning alters hippocampal calcium/calmodulin-dependent protein kinase II activity in rats. Brain Res 711:234–240. https://doi.org/10.1016/0006-8993(95)01411-X. (PMID: 8680867)
Atkins CM, Selcher JC, Petraitis JJ et al (1998) The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1:602–609. https://doi.org/10.1038/2836. (PMID: 10196568)
Peng S, Zhang Y, Zhang J et al (2010) ERK in learning and memory: a review of recent research. Int J Mol Sci 11:222–232. https://doi.org/10.3390/ijms11010222. (PMID: 201620122821000)
Atkins CM (2011) Decoding hippocampal signaling deficits after traumatic brain injury. Transl Stroke Res 2:546–555. https://doi.org/10.1007/s12975-011-0123-z. (PMID: 232271333514866)
Yang K, Taft WC, Dixon CE et al (1993) Alterations of protein kinase C in rat hippocampus following traumatic brain injury. J Neurotrauma 10:287–295. https://doi.org/10.1089/neu.1993.10.287. (PMID: 8258841)
Folkerts MM, Parks EA, Dedman JR et al (2007) Phosphorylation of calcium calmodulin—dependent protein kinase II following lateral fluid percussion brain injury in rats. J Neurotrauma 24:638–650. https://doi.org/10.1089/neu.2006.0188. (PMID: 17439347)
Atkins CM, Chen S, Alonso OF et al (2006) Activation of calcium/calmodulin-dependent protein kinases after traumatic brain injury. J Cereb Blood Flow Metab 26:1507–1518. https://doi.org/10.1038/sj.jcbfm.9600301. (PMID: 16570077)
Dash PK, Mach SA, Moore AN (2002) The role of extracellular signal-regulated kinase in cognitive and motor deficits following experimental traumatic brain injury. Neuroscience 114:755–767. https://doi.org/10.1016/S0306-4522(02)00277-4. (PMID: 12220576)
Otani N, Nawashiro H, Fukui S et al (2002) Temporal and spatial profile of phosphorylated mitogen-activated protein kinase pathways after lateral fluid percussion injury in the cortex of the rat brain. J Neurotrauma 19:1587–1596. https://doi.org/10.1089/089771502762300247. (PMID: 12542859)
Dixon CE, Kochanek PM, Yan HQ et al (1999) One-year study of spatial memory performance, brain morphology, and cholinergic markers after moderate controlled cortical impact in rats. J Neurotrauma 16:109–122. https://doi.org/10.1089/neu.1999.16.109. (PMID: 10098956)
Pierce JES, Smith DH, Trojanowski JQ, McIntosh TK (1998) Enduring cognitive, neurobehavioral and histopathological changes persist for up to one year following severe experimental brain injury in rats. Neuroscience 87:359–369. https://doi.org/10.1016/S0306-4522(98)00142-0. (PMID: 9740398)
Zhong L, Kaleka KS, Gerges NZ (2011) Neurogranin phosphorylation fine-tunes long-term potentiation. Eur J Neurosci 33:244–250. https://doi.org/10.1111/j.1460-9568.2010.07506.x. (PMID: 21198977)
Huang K-P, Huang FL, Jäger T et al (2004) Neurogranin/RC3 enhances long-term potentiation and learning by promoting calcium-mediated signaling. J Neurosci 24:10660–10669. https://doi.org/10.1523/JNEUROSCI.2213-04.2004. (PMID: 155645826730132)
Zhong L, Cherry T, Bies CE et al (2009) Neurogranin enhances synaptic strength through its interaction with calmodulin. EMBO J 28:3027–3039. https://doi.org/10.1038/emboj.2009.236. (PMID: 197139362736013)
Petersen A, Gerges NZ (2015) Neurogranin regulates CaM dynamics at dendritic spines. Sci Rep 5:11135. https://doi.org/10.1038/srep11135. (PMID: 260844734471661)
Gerendasy DD, Sutcliffe JG (1997) RC3/neurogranin, a postsynaptic calpacitin for setting the response threshold to calcium influxes. Mol Neurobiol 15:131–163. (PMID: 9396008)
Malenka RC (1994) Synaptic plasticity in the hippocampus: LTP and LTD. Cell 78:535–538. https://doi.org/10.1016/0092-8674(94)90517-7. (PMID: 8069904)
Pettit DL, Perlman S, Malinow R (1994) Potentiated transmission and prevention of further LTP by increased CaMKII activity in postsynaptic hippocampal slice neurons. Science 266:1881–1885. https://doi.org/10.1126/science.7997883. (PMID: 7997883)
Fukunaga K, Muller D, Miyamoto E (1995) Increased phosphorylation of Ca/Calmodulin-dependent protein kinase II and its endogenous substrates in the induction of long term potentiation. J Biol Chem 270:6119–6124. https://doi.org/10.1074/jbc.270.11.6119. (PMID: 7890745)
Giese KP, Fedorov NB, Filipkowski RK, Silva AJ (1998) Autophosphorylation at Thr286 of the α calcium-calmodulin kinase II in LTP and learning. Science 279:870–873. https://doi.org/10.1126/science.279.5352.870. (PMID: 9452388)
Lisman J, Schulman H, Cline H (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3:175–190. https://doi.org/10.1038/nrn753. (PMID: 11994750)
Fukunaga K, Stoppini L, Miyamoto E, Muller D (1993) Long-term potentiation is associated with an increased activity of Ca2+/calmodulin-dependent protein kinase II. J Biol Chem 268:7863–7867. (PMID: 8385124)
Pak JH, Huang FL, Li J et al (2000) Involvement of neurogranin in the modulation of calcium/calmodulin-dependent protein kinase II, synaptic plasticity, and spatial learning: a study with knockout mice. Proc Natl Acad Sci 97:11232–11237. https://doi.org/10.1073/pnas.210184697. (PMID: 1101696917183)
Miyakawa T, Yared E, Pak JH et al (2001) Neurogranin null mutant mice display performance deficits on spatial learning tasks with anxiety related components. Hippocampus 11:763–775. https://doi.org/10.1002/hipo.1092. (PMID: 11811671)
Ramakers GMJ, Graan PNED, Urban IJA et al (1995) Temporal differences in the phosphorylation state of pre- and postsynaptic protein kinase C substrates B-50/GAP-43 and neurogranin during long term potentiation. J Biol Chem 270:13892–13898. https://doi.org/10.1074/jbc.270.23.13892. (PMID: 7775448)
Chen S-J, Sweatt JD, Klann E (1997) Enhanced phosphorylation of the postsynaptic protein kinase C substrate RC3/neurogranin during long-term potentiation. Brain Res 749:181–187. https://doi.org/10.1016/S0006-8993(96)01159-6. (PMID: 9138717)
Ramakers GMJ, Heinen K, Gispen W-H, de Graan PNE (2000) Long term depression in the CA1 field is associated with a transient decrease in pre- and postsynaptic PKC substrate phosphorylation. J Biol Chem 275:28682–28687. https://doi.org/10.1074/jbc.M003068200. (PMID: 10867003)
Seki K, Chen HC, Huang KP (1995) Dephosphorylation of protein kinase C substrates, neurogranin, neuromodulin, and MARCKS, by calcineurin and protein phosphatases 1 and 2A. Arch Biochem Biophys 316:673–679. https://doi.org/10.1006/abbi.1995.1090. (PMID: 7864622)
Xiang Y, Xin J, Le W, Yang Y (2020) Neurogranin: A Potential Biomarker of Neurological and Mental Diseases. Front Aging Neurosci 12:584743.  https://doi.org/10.3389/fnagi.2020.584743. (PMID: 331329037573493)
Peacock WF, Van Meter TE, Mirshahi N et al (2017) Derivation of a three biomarker panel to improve diagnosis in patients with mild traumatic brain injury. Front Neurol 8:641. https://doi.org/10.3389/fneur.2017.00641. (PMID: 292500275714862)
Winston CN, Romero HK, Ellisman M, Nauss S, Julovich DA, Conger T, Hall JR, Campana W, O’Bryant SE, Nievergelt CM, Baker DG, Risbrough VB, Rissman RA (2019) Assessing neuronal and astrocyte derived exosomes from individuals with mild traumatic brain injury for markers of neurodegeneration and cytotoxic activity. Front Neurosci 13:1005. https://doi.org/10.3389/fnins.2019.01005. (PMID: 316807976797846)
Yang J, Korley FK, Dai M, Everett AD (2015) Serum neurogranin measurement as a biomarker of acute traumatic brain injury. Clin Biochem 48:843–848. https://doi.org/10.1016/j.clinbiochem.2015.05.015. (PMID: 260257744603564)
Svirsky S, Henchir J, Li Y et al (2020) Neurogranin protein expression is reduced after controlled cortical impact in rats. J Neurotrauma 37:939–949. https://doi.org/10.1089/neu.2019.6759. (PMID: 316916477175627)
Ehrlich I, Klein M, Rumpel S, Malinow R (2007) PSD-95 is required for activity-driven synapse stabilization. Proc Natl Acad Sci 104:4176–4181. https://doi.org/10.1073/pnas.0609307104. (PMID: 173604961820728)
El-Husseini AE-D, Schnell E, Chetkovich DM et al (2000) PSD-95 involvement in maturation of excitatory synapses. Science 290:1364–1368. https://doi.org/10.1126/science.290.5495.1364. (PMID: 11082065)
Cora MC, Kooistra L, Travlos G (2015) Vaginal cytology of the laboratory rat and mouse: review and criteria for the staging of the estrous cycle using stained vaginal smears. Toxicol Pathol 43:776–793. https://doi.org/10.1177/0192623315570339. (PMID: 25739587)
Fortress AM, Avcu P, Wagner AK et al (2019) Experimental traumatic brain injury results in estrous cycle disruption, neurobehavioral deficits, and impaired GSK3β/β-catenin signaling in female rats. Exp Neurol 315:42–51. https://doi.org/10.1016/j.expneurol.2019.01.017. (PMID: 30710530)
Svirsky SE, Ranellone NS, Parry M et al (2022) All-trans retinoic acid has limited therapeutic effects on cognition and hippocampal protein expression after controlled cortical impact. Neuroscience 499:130–141. https://doi.org/10.1016/j.neuroscience.2022.07.021. (PMID: 35878718)
Dixon CE, Clifton GL, Lighthall JW et al (1991) A controlled cortical impact model of traumatic brain injury in the rat. J Neurosci Methods 39:253–262. https://doi.org/10.1016/0165-0270(91)90104-8. (PMID: 1787745)
Berman R, Spencer H, Boese M et al (2023) Loss of consciousness and righting reflex following traumatic brain injury: predictors of post-injury symptom development (a narrative review). Brain Sci 13:750. https://doi.org/10.3390/brainsci13050750. (PMID: 3723922210216326)
Carlson SW, Yan H, Dixon CE (2017) Lithium increases hippocampal SNARE protein abundance after traumatic brain injury. Exp Neurol 289:55–63. https://doi.org/10.1016/j.expneurol.2016.12.006. (PMID: 28011122)
Scheff SW, Price DA, Hicks RR et al (2005) Synaptogenesis in the hippocampal CA1 field following traumatic brain injury. J Neurotrauma 22:719–732. https://doi.org/10.1089/neu.2005.22.719. (PMID: 16004576)
Ansari MA, Roberts KN, Scheff SW (2008) A time course of contusion-induced oxidative stress and synaptic proteins in cortex in a rat model of TBI. J Neurotrauma 25:513–526. https://doi.org/10.1089/neu.2007.0451. (PMID: 18533843)
Wakade C, Sangeetha SR, Laird MD et al (2010) Delayed reduction in hippocampal post-synaptic density protein-95 expression temporally correlates with cognitive dysfunction following controlled cortical impact in mice. J Neurosurg 113:1195–1201. https://doi.org/10.3171/2010.3.JNS091212. (PMID: 203978933155981)
Jones KJ, Templet S, Zemoura K et al (2018) Rapid, experience-dependent translation of neurogranin enables memory encoding. Proc Natl Acad Sci 115:E5805–E5814. https://doi.org/10.1073/pnas.1716750115. (PMID: 298807156016824)
Weber JT (2012) Altered calcium signaling following traumatic brain injury. Front Pharmacol 3. https://doi.org/10.3389/fphar.2012.00060.
Hill CS, Coleman MP, Menon DK (2016) Traumatic axonal injury: mechanisms and translational opportunities. Trends Neurosci 39:311–324. https://doi.org/10.1016/j.tins.2016.03.002. (PMID: 270407295405046)
Liu-Yesucevitz L, Bassell GJ, Gitler AD et al (2011) Local RNA translation at the synapse and in disease. J Neurosci 31:16086–16093. https://doi.org/10.1523/JNEUROSCI.4105-11.2011. (PMID: 220726603241995)
Lighthall JW, Goshgarian HG, Pinderski CR (1990) Characterization of axonal injury produced by controlled cortical impact. J Neurotrauma 7:65–76. https://doi.org/10.1089/neu.1990.7.65. (PMID: 2376865)
Osier ND, Dixon CE (2016) The controlled cortical impact model: applications, considerations for researchers, and future directions. Front Neurol 7 https://doi.org/10.3389/fneur.2016.00134.
Li J, Yang C, Han S et al (2006) Increased phosphorylation of neurogranin in the brain of hypoxic preconditioned mice. Neurosci Lett 391:150–153. https://doi.org/10.1016/j.neulet.2005.08.046. (PMID: 16182446)
Kim SH, Kim MK, Yu HS et al (2010) Electroconvulsive seizure increases phosphorylation of PKC substrates, including GAP-43, MARCKS, and neurogranin, in rat brain. Prog Neuropsychopharmacol Biol Psychiatry 34:115–121. https://doi.org/10.1016/j.pnpbp.2009.10.009. (PMID: 19837121)
Baudier J, Deloulme JC, Dorsselaer AV et al (1991) Purification and characterization of a brain-specific protein kinase C substrate, neurogranin (p17). Identification of a consensus amino acid sequence between neurogranin and neuromodulin (GAP43) that corresponds to the protein kinase C phosphorylation site and the calmodulin-binding domain. J Biol Chem 266:229–237. (PMID: 1824695)
Sarkis GA, Lees-Gayed N, Banoub J et al (2022) Generation and release of neurogranin, vimentin, and MBP proteolytic peptides, following traumatic brain injury. Mol Neurobiol 59:731–747. https://doi.org/10.1007/s12035-021-02600-w. (PMID: 34762230)
Hwang H, Szucs MJ, Ding LJ et al (2021) Neurogranin, encoded by the schizophrenia risk gene NRGN, bidirectionally modulates synaptic plasticity via calmodulin-dependent regulation of the neuronal phosphoproteome. Biol Psychiatry 89:256–269. https://doi.org/10.1016/j.biopsych.2020.07.014. (PMID: 33032807)
Spaethling JM, Klein DM, Singh P, Meaney DF (2008) Calcium-permeable AMPA receptors appear in cortical neurons after traumatic mechanical injury and contribute to neuronal fate. J Neurotrauma 25:1207–1216. https://doi.org/10.1089/neu.2008.0532. (PMID: 189862222799682)
Spaethling J, Le L, Meaney DF (2012) NMDA receptor mediated phosphorylation of GluR1 subunits contributes to the appearance of calcium-permeable AMPA receptors after mechanical stretch injury. Neurobiol Dis 46:646–654. https://doi.org/10.1016/j.nbd.2012.03.003. (PMID: 224263934946953)
Bigford GE, Alonso OF, Dietrich D, Keane RW (2009) A novel protein complex in membrane rafts linking the NR2B glutamate receptor and autophagy is disrupted following traumatic brain injury. J Neurotrauma 26:703–720. https://doi.org/10.1089/neu.2008.0783. (PMID: 193352062848823)
Lisman J, Yasuda R, Raghavachari S (2012) Mechanisms of CaMKII action in long-term potentiation. Nat Rev Neurosci 13:169–182. https://doi.org/10.1038/nrn3192. (PMID: 223342124050655)
Wu P, Zhao Y, Haidacher SJ et al (2013) Detection of structural and metabolic changes in traumatically injured hippocampus by quantitative differential proteomics. J Neurotrauma 30:775–788. https://doi.org/10.1089/neu.2012.2391. (PMID: 227576923941921)
Bales JW, Ma X, Yan HQ et al (2009) Expression of protein phosphatase 2B (calcineurin) subunit A isoforms in rat hippocampus after traumatic brain injury. J Neurotrauma 27:109–120. https://doi.org/10.1089/neu.2009.1072.
Bales JW, Ma X, Yan HQ et al (2010) Regional calcineurin subunit B isoform expression in rat hippocampus following a traumatic brain injury. Brain Res 1358:211–220. https://doi.org/10.1016/j.brainres.2010.08.029. (PMID: 207130272949526)
Dixon CE, Bramlett HM, Dietrich WD et al (2015) Cyclosporine treatment in traumatic brain injury: operation brain trauma therapy. J Neurotrauma 33:553–566. https://doi.org/10.1089/neu.2015.4122.
Reeves TM, Phillips LL, Lee NN, Povlishock JT (2007) Preferential neuroprotective effect of tacrolimus (FK506) on unmyelinated axons following traumatic brain injury. Brain Res 1154:225–236. https://doi.org/10.1016/j.brainres.2007.04.002. (PMID: 174815962703421)
Mazzeo AT, Brophy GM, Gilman CB et al (2009) Safety and tolerability of cyclosporin A in severe traumatic brain injury patients: results from a prospective randomized trial. J Neurotrauma 26:2195–2206. https://doi.org/10.1089/neu.2009.1012. (PMID: 196219852824218)
Rubin TG, Lipton ML (2019) Sex differences in animal models of traumatic brain injury. J Exp Neurosci 13:1179069519844020. https://doi.org/10.1177/1179069519844020. (PMID: 312054216537488)
Gupte R, Brooks W, Vukas R et al (2019) Sex differences in traumatic brain injury: what we know and what we should know. J Neurotrauma 36:3063–3091. https://doi.org/10.1089/neu.2018.6171. (PMID: 307940286818488)
Semple BD, Dixit S, Shultz SR et al (2017) Sex-dependent changes in neuronal morphology and psychosocial behaviors after pediatric brain injury. Behav Brain Res 319:48–62. https://doi.org/10.1016/j.bbr.2016.10.045. (PMID: 27829127)
فهرسة مساهمة: Keywords: Cognition; Controlled cortical impact; Neurogranin; Synapses; Traumatic brain injury
المشرفين على المادة: EC 2.7.11.17 (Calcium-Calmodulin-Dependent Protein Kinase Type 2)
0 (Calmodulin)
132654-77-4 (Neurogranin)
0 (Nrgn protein, rat)
تواريخ الأحداث: Date Created: 20240220 Date Completed: 20240821 Latest Revision: 20240826
رمز التحديث: 20240826
DOI: 10.1007/s12035-024-04043-5
PMID: 38376763
قاعدة البيانات: MEDLINE
الوصف
تدمد:1559-1182
DOI:10.1007/s12035-024-04043-5