دورية أكاديمية
Upregulation of Spinal MDGA1 in Rats After Nerve Injury Alters Interactions Between Neuroligin-2 and Postsynaptic Scaffolding Proteins and Increases GluR1 Subunit Surface Delivery in the Spinal Cord Dorsal Horn.
| العنوان: | Upregulation of Spinal MDGA1 in Rats After Nerve Injury Alters Interactions Between Neuroligin-2 and Postsynaptic Scaffolding Proteins and Increases GluR1 Subunit Surface Delivery in the Spinal Cord Dorsal Horn. |
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| المؤلفون: | Li HL; Department of Anesthesiology, Beijing Friendship Hospital, Capital Medical University, No. 95, Yongan Road, Xicheng District, Beijing, 100050, China., Guo RJ; Department of Anesthesiology, Beijing Friendship Hospital, Capital Medical University, No. 95, Yongan Road, Xicheng District, Beijing, 100050, China., Ai ZR; Department of Anesthesiology, Beijing Chaoyang Hospital, Capital Medical University, Beijing, 100020, China., Han S; Department of Neurobiology, Capital Medical University, Beijing, 100069, China., Guan Y; Department of Anesthesiology and Critical Care Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, 21205, USA., Li JF; Department of Neurobiology, Capital Medical University, Beijing, 100069, China., Wang Y; Department of Anesthesiology, Beijing Friendship Hospital, Capital Medical University, No. 95, Yongan Road, Xicheng District, Beijing, 100050, China. wangyun129@ccmu.edu.cn. |
| المصدر: | Neurochemical research [Neurochem Res] 2024 Feb; Vol. 49 (2), pp. 507-518. Date of Electronic Publication: 2023 Nov 13. |
| نوع المنشور: | Journal Article |
| اللغة: | English |
| بيانات الدورية: | Publisher: Kluwer Academic/Plenum Publishers Country of Publication: United States NLM ID: 7613461 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1573-6903 (Electronic) Linking ISSN: 03643190 NLM ISO Abbreviation: Neurochem Res Subsets: MEDLINE |
| أسماء مطبوعة: | Publication: 1999- : New York, NY : Kluwer Academic/Plenum Publishers Original Publication: New York, Plenum Press |
| مواضيع طبية MeSH: | Neuroligins* , Neuralgia*/pathology, Rats ; Animals ; Up-Regulation ; Rats, Sprague-Dawley ; Spinal Cord Dorsal Horn/metabolism ; Posterior Horn Cells/metabolism ; Spinal Nerves ; RNA, Small Interfering/metabolism ; Hyperalgesia/metabolism ; Spinal Cord/pathology |
| مستخلص: | Previous studies suggested that postsynaptic neuroligin-2 may shift from inhibitory toward excitatory function under pathological pain conditions. We hypothesize that nerve injury may increase the expression of spinal MAM-domain GPI-anchored molecule 1 (MDGA1), which can bind to neuroligin-2 and thereby, alter its interactions with postsynaptic scaffolding proteins and increase spinal excitatory synaptic transmission, leading to neuropathic pain. Western blot, immunofluorescence staining, and co-immunoprecipitation studies were conducted to examine the critical role of MDGA1 in the lumbar spinal cord dorsal horn in rats after spinal nerve ligation (SNL). Small interfering ribonucleic acids (siRNAs) targeting MDGA1 were used to examine the functional roles of MDGA1 in neuropathic pain. Protein levels of MDGA1 in the ipsilateral dorsal horn were significantly upregulated at day 7 post-SNL, as compared to that in naïve or sham rats. The increased levels of GluR1 in the synaptosomal membrane fraction of the ipsilateral dorsal horn tissues at day 7 post-SNL was normalized to near sham level by pretreatment with intrathecal MDGA1 siRNA (© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.) |
| References: | Cathenaut L, Leonardon B, Kuster R et al (2022) Inhibitory interneurons with differential plasticities at their connections tune excitatory-inhibitory balance in the spinal nociceptive system. Pain 163(5):e675–e688. (PMID: 10.1097/j.pain.000000000000246034490851) Huang Y, Chen SR, Pan HL (2022) Calcineurin regulates synaptic plasticity and nociceptive transmission at the spinal cord level. Neuroscientist 28(6):628–638. (PMID: 10.1177/1073858421104688834791930) Li HL, Guo RJ, Guan Y et al (2022) Modulation of trans-synaptic neurexin-neuroligin interaction in pathological pain. Cells 11(12):1940. (PMID: 10.3390/cells11121940357410699222181) Prange O, Wong TP, Gerrow K et al (2004) A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin. Proc Natl Acad Sci USA 101(38):13915–13920. (PMID: 10.1073/pnas.040593910115358863518853) Ali H, Marth L, Krueger-Burg D (2020) Neuroligin-2 as a central organizer of inhibitory synapses in health and disease. Sci Signal 13(663):eabd8379. (PMID: 10.1126/scisignal.abd837933443230) Liu X, Hua F, Yang D et al (2022) Roles of neuroligins in central nervous system development: focus on glial neuroligins and neuron neuroligins. J Transl Med 20(1):418. (PMID: 10.1186/s12967-022-03625-y360883439463862) Wu XB, Zhu Q, Gao YJ (2021) CCL2/CCR2 contributes to the altered excitatory-inhibitory synaptic balance in the nucleus accumbens shell following peripheral nerve injury-induced neuropathic pain. Neurosci Bull 37(7):921–933. (PMID: 10.1007/s12264-021-00697-6340034668275785) Dolique T, Favereaux A, Roca-Lapirot O et al (2013) Unexpected association of the “inhibitory” neuroligin 2 with excitatory PSD95 in neuropathic pain. Pain 154(11):2529–2546. (PMID: 10.1016/j.pain.2013.07.03523891900) Guo RJ, Li HL, Li XY et al (2018) Increased neuroligin 2 levels in the postsynaptic membrane in spinal dorsal horn may contribute to postoperative pain. Neuroscience 382(2018):14–22. (PMID: 10.1016/j.neuroscience.2018.04.02829715511) Connor SA, Elegheert J, Xie Y et al (2019) Pumping the brakes: suppression of synapse development by MDGA-neuroligin interactions. Curr Opin Neurobiol 57(2019):71–80. (PMID: 10.1016/j.conb.2019.01.00230771697) Kim JA, Kim D, Won SY et al (2017) Structural insights into modulation of neurexin-neuroligin trans-synaptic adhesion by MDGA1/neuroligin-2 complex. Neuron 94(6):1121–1131. (PMID: 10.1016/j.neuron.2017.05.03428641111) Elegheert J, Cvetkovska V, Clayton AJ et al (2017) Structural mechanism for modulation of synaptic neuroligin-neurexin signaling by MDGA proteins. Neuron 95(4):896–913. (PMID: 10.1016/j.neuron.2017.07.040288178045563082) Elegheert J, Cvetkovska V, Clayton AJ et al (2021) Structural mechanism for modulation of synaptic neuroligin-neurexin signaling by MDGA proteins. Neuron 109(1):189–190. (PMID: 10.1016/j.neuron.2020.12.006334120947837113) Kim J, Kim S, Kim H et al (2022) MDGA1 negatively regulates amyloid precursor protein-mediated synapse inhibition in the hippocampus. Proc Natl Acad Sci USA 119(4):e2115326119. (PMID: 10.1073/pnas.2115326119350749128795569) Lee K, Kim Y, Lee SJ et al (2013) MDGAs interact selectively with neuroligin-2 but not other neuroligins to regulate inhibitory synapse development. Proc Natl Acad Sci USA 110(1):336–341. (PMID: 10.1073/pnas.121998711023248271) Toledo A, Letellier M, Bimbi G et al (2022) (2022) MDGAs are fast-diffusing molecules that delay excitatory synapse development by altering neuroligin behavior. Elife 11:e75233. (PMID: 10.7554/eLife.75233355321059084894) Ho KS, Mo CJ (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50(3):355–363. (PMID: 10.1016/0304-3959(92)90041-9) Guo RJ, Li HL, Shi R et al (2021) Intrathecal injection of GRIP-siRNA reduces postoperative synaptic abundance of kainate receptor GluK2 subunits in rat dorsal horns and pain hypersensitivity. Neurochem Res 46(7):1771–1780. (PMID: 10.1007/s11064-021-03323-z33847855) Guo RJ, Li HL, Li XY et al (2018) (2018) Downregulation of neuroligin1 ameliorates postoperative pain through inhibiting neuroligin1/postsynaptic density 95-mediated synaptic targeting of α-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptor GluA1 subunits in rat dorsal horns. Mol Pain 14:1744806918766745. (PMID: 10.1177/1744806918766745295927805881971) Dunah AW, Standaert DG (2021) Dopamine D1 receptor dependent trafficking of striatal NMDA glutamate receptors to the postsynaptic membrane. J Neurosci 21(15):5546–5558. (PMID: 10.1523/JNEUROSCI.21-15-05546.2001) Guo RJ, Zhao YJ, Zhang MJ et al (2014) Down-regulation of stargazin inhibits the enhanced surface delivery of α-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptor GluR1 subunit in rat dorsal horn and ameliorates postoperative pain. Anesthesiology 121(3):609–619. (PMID: 10.1097/ALN.000000000000029125093662) Litwack ED, Babey R, Buser R et al (2004) Identification and characterization of two novel brain-derived immunoglobulin superfamily members with a unique structural organization. Mol Cell Neurosci 25(2):263–274. (PMID: 10.1016/j.mcn.2003.10.01615019943) Fujimura Y, Iwashita M, Matsuzaki F et al (2006) MDGA1, an IgSF molecule containing a MAM domain, heterophilically associates with axon- and muscle-associated binding partners through distinct structural domains. Brain Res 1101(1):12–19. (PMID: 10.1016/j.brainres.2006.05.03016782075) Eisenach JC (1999) Muscarinic-mediated analgesia. Life Sci 64(6–7):549–554. (PMID: 10.1016/S0024-3205(98)00600-610069522) Connor SA, Ammendrup-Johnsen I, Kishimoto Y et al (2017) Loss of synapse repressor MDGA1 enhances perisomatic inhibition, confers resistance to network excitation, and impairs cognitive function. Cell Rep 21(13):3637–3645. (PMID: 10.1016/j.celrep.2017.11.10929281813) Pettem KL, Yokomaku D, Takahashi H et al (2013) Interaction between autism-linked MDGAs and neuroligins suppresses inhibitory synapse development. J Cell Biol 200(3):321–336. (PMID: 10.1083/jcb.201206028233582453563690) Hossain MR, Jamal M, Tanoue Y et al (2020) MDGA1-deficiency attenuates prepulse inhibition with alterations of dopamine and serotonin metabolism: An ex vivo HPLC-ECD analysis. Neurosci Lett 716:134677. (PMID: 10.1016/j.neulet.2019.13467731812551) Phelps CE, Navratilova E, Porreca F (2021) Cognition in the chronic pain experience: preclinical insights. Trends Cogn Sci 25(5):365–376. (PMID: 10.1016/j.tics.2021.01.001335097338035230) O’Gara BP, Gao L, Marcantonio ER et al (2021) Sleep, pain, and cognition: modifiable targets for optimal perioperative brain health. Anesthesiology 135(6):1132–1152. (PMID: 10.1097/ALN.000000000000404634731233) Chanda S, Hale WD, Zhang B et al (2017) Unique versus redundant functions of neuroligin genes in shaping excitatory and inhibitory synapse properties. J Neurosci 37(29):6816–6836. (PMID: 10.1523/JNEUROSCI.0125-17.2017286071665518416) Hale WD, Südhof TC, Huganir RL (2023) Engineered adhesion molecules drive synapse organization. Proc Natl Acad Sci USA 120(3):e2215905120. (PMID: 10.1073/pnas.2215905120366382149934208) Halff EF, Hannan S, Kwanthongdee J et al (2022) Phosphorylation of neuroligin-2 by PKA regulates its cell surface abundance and synaptic stabilization. Sci Signal 15(739):eabg2505. (PMID: 10.1126/scisignal.abg250535727864) Zhang W, Chen Y, Qin J et al (2022) Prolonged sevoflurane exposure causes abnormal synapse development and dysregulates beta-neurexin and neuroligins in the hippocampus in neonatal rats. J Affect Disord 312(2022):22–29. (PMID: 10.1016/j.jad.2022.05.11535691415) Halff EF, Szulc BR, Lesept F et al (2019) SNX27-mediated recycling of neuroligin-2 regulates inhibitory signaling. Cell Rep 29(9):2599–2607. (PMID: 10.1016/j.celrep.2019.10.096317750316899438) Guo C (2021) Ma YY (2021) Calcium permeable-AMPA receptors and excitotoxicity in neurological disorders. Front Neural Circuits 15:711564. (PMID: 10.3389/fncir.2021.711564344838488416103) Miyagi Y, Fujiwara K, Hikishima K et al (2022) Altered calcium permeability of AMPA receptor drives NMDA receptor inhibition in the hippocampus of murine obesity models. Mol Neurobiol 59(8):4902–4925. (PMID: 10.1007/s12035-022-02834-235657456) Zhang W, Lei M, Wen QW et al (2022) Dopamine receptor D2 regulates GLUA1-containing AMPA receptor trafficking and central sensitization through the PI3K signaling pathway in a male rat model of chronic migraine. J Headache Pain 23(1):98. (PMID: 10.1186/s10194-022-01469-x359488679364568) |
| معلومات مُعتمدة: | 82171217, 81771181, 81571065 National Natural Science Foundation of China; 7202053 Beijing Natural Science Foundation |
| فهرسة مساهمة: | Keywords: AMPA receptor; MDGA1; NLG-2; Neuropathic pain; Spinal dorsal horn |
| المشرفين على المادة: | 0 (Neuroligins) 0 (RNA, Small Interfering) |
| تواريخ الأحداث: | Date Created: 20231113 Date Completed: 20240115 Latest Revision: 20240115 |
| رمز التحديث: | 20240115 |
| DOI: | 10.1007/s11064-023-04049-w |
| PMID: | 37955815 |
| قاعدة البيانات: | MEDLINE |
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Full Text Finder | تدمد: | 1573-6903 |
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| DOI: | 10.1007/s11064-023-04049-w |