{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,7]],"date-time":"2026-11-07T00:37:50Z","timestamp":1794011870749,"version":"4.8.0"},"reference-count":93,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2024,5,4]],"date-time":"2024-05-04T00:00:00Z","timestamp":1714780800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100006314","name":"Biogen","doi-asserted-by":"publisher","award":["GR-SMG-11658"],"award-info":[{"award-number":["GR-SMG-11658"]}],"id":[{"id":"10.13039\/100006314","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Spinal muscular atrophy (SMA) is a neurodegenerative disease caused by deficiency of the survival motor neuron (SMN) protein. Although SMA is a genetic disease, environmental factors contribute to disease progression. Common pathogen components such as lipopolysaccharides (LPS) are considered significant contributors to inflammation and have been associated with muscle atrophy, which is considered a hallmark of SMA. In this study, we used the SMN\u03947 experimental mouse model of SMA to scrutinize the effect of systemic LPS administration, a strong pro-inflammatory stimulus, on disease outcome. Systemic LPS administration promoted a reduction in SMN expression levels in CNS, peripheral lymphoid organs, and skeletal muscles. Moreover, peripheral tissues were more vulnerable to LPS-induced damage compared to CNS tissues. Furthermore, systemic LPS administration resulted in a profound increase in microglia and astrocytes with reactive phenotypes in the CNS of SMN\u03947 mice. In conclusion, we hereby show for the first time that systemic LPS administration, although it may not precipitate alterations in terms of deficits of motor functions in a mouse model of SMA, it may, however, lead to a reduction in the SMN protein expression levels in the skeletal muscles and the CNS, thus promoting synapse damage and glial cells\u2019 reactive phenotype.<\/jats:p>","DOI":"10.3390\/cells13090785","type":"journal-article","created":{"date-parts":[[2024,5,6]],"date-time":"2024-05-06T15:09:36Z","timestamp":1715008176000},"page":"785","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Systemic LPS Administration Stimulates the Activation of Non-Neuronal Cells in an Experimental Model of Spinal Muscular Atrophy"],"prefix":"10.3390","volume":"13","author":[{"given":"Eleni","family":"Karafoulidou","sequence":"first","affiliation":[{"name":"Laboratory of Experimental Neurology and Neuroimmunology, 2nd Neurological University Department, AHEPA General Hospital of Thessaloniki, Faculty of Health Science, Aristotle University of Thessaloniki, 54636 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7234-2462","authenticated-orcid":false,"given":"Evangelia","family":"Kesidou","sequence":"additional","affiliation":[{"name":"Laboratory of Experimental Neurology and Neuroimmunology, 2nd Neurological University Department, AHEPA General Hospital of Thessaloniki, Faculty of Health Science, Aristotle University of Thessaloniki, 54636 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8607-6695","authenticated-orcid":false,"given":"Paschalis","family":"Theotokis","sequence":"additional","affiliation":[{"name":"Laboratory of Experimental Neurology and Neuroimmunology, 2nd Neurological University Department, AHEPA General Hospital of Thessaloniki, Faculty of Health Science, Aristotle University of Thessaloniki, 54636 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chrystalla","family":"Konstantinou","sequence":"additional","affiliation":[{"name":"Laboratory of Experimental Neurology and Neuroimmunology, 2nd Neurological University Department, AHEPA General Hospital of Thessaloniki, Faculty of Health Science, Aristotle University of Thessaloniki, 54636 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria-Konstantina","family":"Nella","sequence":"additional","affiliation":[{"name":"Laboratory of Experimental Neurology and Neuroimmunology, 2nd Neurological University Department, AHEPA General Hospital of Thessaloniki, Faculty of Health Science, Aristotle University of Thessaloniki, 54636 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Iliana","family":"Michailidou","sequence":"additional","affiliation":[{"name":"Laboratory of Experimental Neurology and Neuroimmunology, 2nd Neurological University Department, AHEPA General Hospital of Thessaloniki, Faculty of Health Science, Aristotle University of Thessaloniki, 54636 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olga","family":"Touloumi","sequence":"additional","affiliation":[{"name":"Laboratory of Experimental Neurology and Neuroimmunology, 2nd Neurological University Department, AHEPA General Hospital of Thessaloniki, Faculty of Health Science, Aristotle University of Thessaloniki, 54636 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eleni","family":"Polyzoidou","sequence":"additional","affiliation":[{"name":"Laboratory of Experimental Neurology and Neuroimmunology, 2nd Neurological University Department, AHEPA General Hospital of Thessaloniki, Faculty of Health Science, Aristotle University of Thessaloniki, 54636 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ilias","family":"Salamotas","sequence":"additional","affiliation":[{"name":"Laboratory of Experimental Neurology and Neuroimmunology, 2nd Neurological University Department, AHEPA General Hospital of Thessaloniki, Faculty of Health Science, Aristotle University of Thessaloniki, 54636 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0819-3057","authenticated-orcid":false,"given":"Ofira","family":"Einstein","sequence":"additional","affiliation":[{"name":"Department of Physical Therapy, Faculty of Health Sciences, Ariel University, Ariel 40700, Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5415-2064","authenticated-orcid":false,"given":"Athanasios","family":"Chatzisotiriou","sequence":"additional","affiliation":[{"name":"Department of Physiology, Medical School, Aristotle University of Thessaloniki, 54636 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6601-5163","authenticated-orcid":false,"given":"Marina-Kleopatra","family":"Boziki","sequence":"additional","affiliation":[{"name":"Laboratory of Experimental Neurology and Neuroimmunology, 2nd Neurological University Department, AHEPA General Hospital of Thessaloniki, Faculty of Health Science, Aristotle University of Thessaloniki, 54636 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4278-3301","authenticated-orcid":false,"given":"Nikolaos","family":"Grigoriadis","sequence":"additional","affiliation":[{"name":"Laboratory of Experimental Neurology and Neuroimmunology, 2nd Neurological University Department, AHEPA General Hospital of Thessaloniki, Faculty of Health Science, Aristotle University of Thessaloniki, 54636 Thessaloniki, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,5,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/0092-8674(95)90460-3","article-title":"Identification and characterization of a spinal muscular atrophy-determining gene","volume":"80","author":"Lefebvre","year":"1995","journal-title":"Cell"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/j.bbagrm.2016.12.008","article-title":"Diverse role of survival motor neuron protein","volume":"1860","author":"Singh","year":"2017","journal-title":"Biochim. Biophys. Acta (BBA)-Gene Regul. Mech."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1146\/annurev-genom-102319-103602","article-title":"Twenty-Five Years of Spinal Muscular Atrophy Research: From Phenotype to Genotype to Therapy, and What Comes Next","volume":"21","author":"Wirth","year":"2020","journal-title":"Annu. Rev. Genom. Hum. Genet."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"947033","DOI":"10.3389\/fnut.2022.947033","article-title":"Role of brain-gut-muscle axis in human health and energy homeostasis","volume":"9","author":"Yin","year":"2022","journal-title":"Front. Nutr."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/j.cell.2004.09.027","article-title":"IKKbeta\/NF-kappaB activation causes severe muscle wasting in mice","volume":"119","author":"Cai","year":"2004","journal-title":"Cell"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"eaan5662","DOI":"10.1126\/scitranslmed.aan5662","article-title":"The gut microbiota influences skeletal muscle mass and function in mice","volume":"11","author":"Lahiri","year":"2019","journal-title":"Sci. Transl. Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2186","DOI":"10.1016\/j.biocel.2013.06.021","article-title":"Muscle wasting: The gut microbiota as a new therapeutic target?","volume":"45","author":"Bindels","year":"2013","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Przew\u0142\u00f3cka, K., Folwarski, M., Ka\u017amierczak-Siedlecka, K., Skonieczna-\u017bydecka, K., and Kaczor, J.J. (2020). Gut-Muscle Axis Exists and May Affect Skeletal Muscle Adaptation to Training. Nutrients, 12.","DOI":"10.3390\/nu12051451"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2998","DOI":"10.1111\/bph.15472","article-title":"Triptolide prevents LPS-induced skeletal muscle atrophy via inhibiting NF-kappaB\/TNF-alpha and regulating protein synthesis\/degradation pathway","volume":"178","author":"Fang","year":"2021","journal-title":"Br. J. Pharmacol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"C300","DOI":"10.1152\/ajpcell.00007.2023","article-title":"Stimulated myotube contractions regulate membrane-bound and soluble TLR4 to prevent LPS-induced signaling and myotube atrophy in skeletal muscle cells","volume":"325","author":"Ducharme","year":"2023","journal-title":"Am. J. Physiol. Physiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1186\/s12974-019-1644-8","article-title":"Lipopolysaccharide induces neuroinflammation in microglia by activating the MTOR pathway and downregulating Vps34 to inhibit autophagosome formation","volume":"17","author":"Ye","year":"2020","journal-title":"J. Neuroinflamm."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1111\/cen3.12309","article-title":"Neuroinflammation in motor neuron disease","volume":"7","author":"Endo","year":"2016","journal-title":"Clin. Exp. Neuroimmunol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1002\/glia.20919","article-title":"Extracellular mutant SOD1 induces microglial-mediated motoneuron injury","volume":"58","author":"Zhao","year":"2010","journal-title":"Glia"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"fcaa124","DOI":"10.1093\/braincomms\/fcaa124","article-title":"Immunity in amyotrophic lateral sclerosis: Blurred lines between excessive inflammation and inefficient immune responses","volume":"2","author":"Markovinovic","year":"2020","journal-title":"Brain Commun."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1418","DOI":"10.1002\/glia.22522","article-title":"Spinal muscular atrophy astrocytes exhibit abnormal calcium regulation and reduced growth factor production","volume":"61","author":"McGivern","year":"2013","journal-title":"Glia"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1097\/NEN.0000000000000074","article-title":"Mechanisms Involved in Spinal Cord Central Synapse Loss in a Mouse Model of Spinal Muscular Atrophy","volume":"73","author":"Tarabal","year":"2014","journal-title":"J. Neuropathol. Exp. Neurol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.expneurol.2008.02.025","article-title":"Identification of a battery of tests for drug candidate evaluation in the SMNDelta7 neonate model of spinal muscular atrophy","volume":"212","author":"Edgar","year":"2008","journal-title":"Exp. Neurol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Niba, E.T.E., Nishio, H., Wijaya, Y.O.S., Rochmah, M.A., Takarada, T., Takeuchi, A., Kimizu, T., Okamoto, K., Saito, T., and Awano, H. (2022). Stability and Oligomerization of Mutated SMN Protein Determine Clinical Severity of Spinal Muscular Atrophy. Genes, 13.","DOI":"10.3390\/genes13020205"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2851","DOI":"10.1093\/hmg\/ddy195","article-title":"Temporal and tissue-specific variability of SMN protein levels in mouse models of spinal muscular atrophy","volume":"27","author":"Groen","year":"2018","journal-title":"Hum. Mol. Genet."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"581","DOI":"10.3109\/21678421.2014.907319","article-title":"Nuclear localization of SMN and FUS is not altered in fibroblasts from patients with sporadic ALS","volume":"15","author":"Kariya","year":"2014","journal-title":"Amyotroph. Lateral Scler. Front. Degener."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Eaton, S.L., Roche, S.L., Hurtado, M.L., Oldknow, K.J., Farquharson, C., Gillingwater, T.H., and Wishart, T.M. (2013). Total Protein Analysis as a Reliable Loading Control for Quantitative Fluorescent Western Blotting. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0072457"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"5074","DOI":"10.1523\/JNEUROSCI.5808-11.2012","article-title":"Survival Motor Neuron Affects Plastin 3 Protein Levels Leading to Motor Defects","volume":"32","author":"Hao","year":"2012","journal-title":"J. Neurosci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"855","DOI":"10.1038\/mt.2016.33","article-title":"Rescue of a Mouse Model of Spinal Muscular Atrophy With Respiratory Distress Type 1 by AAV9-IGHMBP2 Is Dose Dependent","volume":"24","author":"Shababi","year":"2016","journal-title":"Mol. Ther."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"630","DOI":"10.1002\/elps.201500385","article-title":"Standard loading controls are not reliable for Western blot quantification across brain development or in pathological conditions","volume":"37","author":"Goasdoue","year":"2015","journal-title":"Electrophoresis"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"4216","DOI":"10.1093\/hmg\/ddq340","article-title":"SMN deficiency disrupts brain development in a mouse model of severe spinal muscular atrophy","volume":"19","author":"Wishart","year":"2010","journal-title":"Hum. Mol. Genet."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"3127","DOI":"10.1002\/cne.24080","article-title":"Comprehensive cellular-resolution atlas of the adult human brain","volume":"524","author":"Ding","year":"2016","journal-title":"J. Comp. Neurol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"104296","DOI":"10.1016\/j.jff.2020.104296","article-title":"Edible dairy formula fortified with coconut oil for neuroprotection against aluminium chloride-induced Alzheimer\u2019s disease in rats","volume":"75","author":"Khalil","year":"2020","journal-title":"J. Funct. Foods"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1177\/03009858221128920","article-title":"Motor and somatosensory degenerative myelopathy responsive to pantothenic acid in piglets","volume":"60","author":"Lorenzett","year":"2022","journal-title":"Veter. Pathol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/B978-0-323-98817-9.00030-2","article-title":"Childhood spinal muscular atrophy","volume":"196","author":"Younger","year":"2023","journal-title":"Handb. Clin. Neurol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1827","DOI":"10.4103\/1673-5374.332153","article-title":"Effects of targeted muscle reinnervation on spinal cord motor neurons in rats following tibial nerve transection","volume":"17","author":"Yang","year":"2022","journal-title":"Neural Regen. Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1080\/13880209.2018.1502326","article-title":"Resveratrol mitigates the oxidative stress mediated by hypoxic-ischemic brain injury in neonatal rats via Nrf2\/HO-1 pathway","volume":"56","author":"Gao","year":"2018","journal-title":"Pharm. Biol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Wittekindt, M., Kaddatz, H., Joost, S., Staffeld, A., Bitar, Y., Kipp, M., and Frintrop, L. (2022). Different Methods for Evaluating Microglial Activation Using Anti-Ionized Calcium-Binding Adaptor Protein-1 Immunohistochemistry in the Cuprizone Model. Cells, 11.","DOI":"10.3390\/cells11111723"},{"key":"ref_33","first-page":"57648","article-title":"Quantifying Microglia Morphology from Photomicrographs of Immunohistochemistry Prepared Tissue Using ImageJ","volume":"5","author":"Young","year":"2018","journal-title":"J. Vis. Exp."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1038\/s41531-021-00213-7","article-title":"Genetic and environmental factors in Alzheimer\u2019s and Parkinson\u2019s diseases and promising therapeutic intervention via fecal microbiota transplantation","volume":"7","author":"Wang","year":"2021","journal-title":"npj Park. Dis."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Vasta, R., Chia, R., Traynor, B.J., and Chi\u00f2, A. (2021). Unraveling the complex interplay between genes, environment, and climate in ALS. EBioMedicine, 75.","DOI":"10.1016\/j.ebiom.2021.103795"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1038\/nature10554","article-title":"Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination","volume":"479","author":"Berer","year":"2011","journal-title":"Nature"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1126\/science.abj8222","article-title":"Longitudinal analysis reveals high prevalence of Epstein-Barr virus associated with multiple sclerosis","volume":"375","author":"Bjornevik","year":"2022","journal-title":"Science"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Berer, K., Boziki, M., and Krishnamoorthy, G. (2014). Selective Accumulation of Pro-Inflammatory T Cells in the Intestine Contributes to the Resistance to Autoimmune Demyelinating Disease. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0087876"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1038\/s41582-020-00435-y","article-title":"Neuroinflammation and microglial activation in Alzheimer disease: Where do we go from here?","volume":"17","author":"Leng","year":"2021","journal-title":"Nat. Rev. Neurol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1038\/s41582-023-00822-1","article-title":"Functional roles of reactive astrocytes in neuroinflammation and neurodegeneration","volume":"19","author":"Patani","year":"2023","journal-title":"Nat. Rev. Neurol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"3666","DOI":"10.1111\/ene.15542","article-title":"Validation of motor and functional scales for the evaluation of adult patients with 5q spinal muscular atrophy","volume":"29","author":"Povedano","year":"2022","journal-title":"Eur. J. Neurol."},{"key":"ref_42","first-page":"4061","article-title":"A severe mouse model of spinal muscular atrophy develops early systemic inflammation","volume":"27","author":"Wan","year":"2018","journal-title":"Hum. Mol. Genet."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1186\/s12974-015-0299-3","article-title":"Systemic inflammation in early neonatal mice induces transient and lasting neurodegenerative effects","volume":"12","author":"Cardoso","year":"2015","journal-title":"J. Neuroinflamm."},{"key":"ref_44","first-page":"932","article-title":"SMN deficiency negatively impacts red pulp macrophages and spleen development in mouse models of spinal muscular atrophy","volume":"26","author":"Khairallah","year":"2017","journal-title":"Hum. Mol. Genet."},{"key":"ref_45","first-page":"801","article-title":"Immune dysregulation may contribute to disease pathogenesis in spinal muscular atrophy mice","volume":"26","author":"Deguise","year":"2017","journal-title":"Hum. Mol. Genet."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Zhou, A., Li, M., He, B., Feng, W., Huang, F., Xu, B., Dunker, A.K., Balch, C., Li, B., and Liu, Y. (2016). Lipopolysaccharide treatment induces genome-wide pre-mRNA splicing pattern changes in mouse bone marrow stromal stem cells. BMC Genom., 17.","DOI":"10.1186\/s12864-016-2898-5"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"6236","DOI":"10.1074\/jbc.RA119.011495","article-title":"NF-kappaB mediates lipopolysaccharide-induced alternative pre-mRNA splicing of MyD88 in mouse macrophages","volume":"295","author":"Lee","year":"2020","journal-title":"J. Biol. Chem."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"3679","DOI":"10.1002\/art.20600","article-title":"Lipopolysaccharide-induced expression of multiple alternatively spliced MEFV transcripts in human synovial fibroblasts: A prominent splice isoform lacks the C-terminal domain that is highly mutated in familial mediterranean fever","volume":"50","author":"Diaz","year":"2004","journal-title":"Arthritis Rheum."},{"key":"ref_49","first-page":"74","article-title":"Differential distribution of PDE4B splice variant mRNAs in rat brain and the effects of systemic administration of LPS in their expression","volume":"62","author":"Palacios","year":"2007","journal-title":"Synapse"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"O\u2019connor, B.P., Danhorn, T., De Arras, L., Flatley, B.R., Marcus, R.A., Farias-Hesson, E., Leach, S.M., and Alper, S. (2015). Regulation of Toll-like Receptor Signaling by the SF3a mRNA Splicing Complex. PLoS Genet., 11.","DOI":"10.1371\/journal.pgen.1004932"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Kim, M.-B., Lee, H., Lee, C., Tan, Y., and Lee, S.G. (2023). The Anti-Muscle Atrophy Effects of Ishige sinicola in LPS-Induced C2C12 Myotubes through Its Antioxidant and Anti-Inflammatory Actions. Appl. Sci., 13.","DOI":"10.3390\/app131810115"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Liao, C.-K., Jeng, C.-J., Wang, H.-S., Wang, S.-H., and Wu, J.-C. (2013). Lipopolysaccharide Induces Degradation of Connexin43 in Rat Astrocytes via the Ubiquitin-Proteasome Proteolytic Pathway. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0079350"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1186\/1742-2094-9-87","article-title":"Lipopolysaccharide-induced neuroinflammation leads to the accumulation of ubiquitinated proteins and increases susceptibility to neurodegeneration induced by proteasome inhibition in rat hippocampus","volume":"9","author":"Pintado","year":"2012","journal-title":"J. Neuroinflamm."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Zhao, Y., Jiang, Q., Zhang, X., Zhu, X., Dong, X., Shen, L., Zhang, S., Niu, L., Chen, L., and Zhang, M. (2021). l-Arginine Alleviates LPS-Induced Oxidative Stress and Apoptosis via Activating SIRT1-AKT-Nrf2 and SIRT1-FOXO3a Signaling Pathways in C2C12 Myotube Cells. Antioxidants, 10.","DOI":"10.21203\/rs.3.rs-1045345\/v1"},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Fang, W.-Y., Lin, C.-L., Chang, W.-H., Chang, C.-H., Huang, Y.-C., Tsai, Y.-H., Chang, F.-R., and Lo, Y.-C. (2022). Protective Effects of the Chalcone-Based Derivative AN07 on Inflammation-Associated Myotube Atrophy Induced by Lipopolysaccharide. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms232112929"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1038\/s41467-020-20123-1","article-title":"Mechanisms of muscle atrophy and hypertrophy: Implications in health and disease","volume":"12","author":"Sartori","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"H1039","DOI":"10.1152\/ajpheart.00912.2014","article-title":"Redox signaling and splicing dependent change in myosin phosphatase underlie early versus late changes in NO vasodilator reserve in a mouse LPS model of sepsis","volume":"308","author":"Reho","year":"2015","journal-title":"Am. J. Physiol. Circ. Physiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1096\/fj.10-164152","article-title":"Toll-like receptor 4 mediates lipopolysaccharide-induced muscle catabolism via coordinate activation of ubiquitin-proteasome and autophagy-lysosome pathways","volume":"25","author":"Doyle","year":"2011","journal-title":"FASEB J."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1392","DOI":"10.1093\/hmg\/ddw021","article-title":"Monoubiquitination of survival motor neuron regulates its cellular localization and Cajal body integrity","volume":"25","author":"Han","year":"2016","journal-title":"Hum. Mol. Genet."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"43741","DOI":"10.1074\/jbc.M112.372318","article-title":"Ubiquitin-specific Protease 9x Deubiquitinates and Stabilizes the Spinal Muscular Atrophy Protein-Survival Motor Neuron","volume":"287","author":"Han","year":"2012","journal-title":"J. Biol. Chem."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"622","DOI":"10.1016\/j.molmed.2015.08.003","article-title":"UBA1: At the Crossroads of Ubiquitin Homeostasis and Neurodegeneration","volume":"21","author":"Groen","year":"2015","journal-title":"Trends Mol. Med."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"e13941","DOI":"10.14814\/phy2.13941","article-title":"Imoxin attenuates LPS-induced inflammation and MuRF1 expression in mouse skeletal muscle","volume":"6","author":"Valentine","year":"2018","journal-title":"Physiol. Rep."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"6829","DOI":"10.1128\/IAI.00286-06","article-title":"Toll-like receptors differentially regulate CC and CXC chemokines in skeletal muscle via NF-kappaB and calcineurin","volume":"74","author":"Boyd","year":"2006","journal-title":"Infect. Immun."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/j.bone.2015.03.015","article-title":"Inflammation induced loss of skeletal muscle","volume":"80","author":"Londhe","year":"2015","journal-title":"Bone"},{"key":"ref_65","first-page":"ftv096","article-title":"Microbiota\u2013mitochondria inter-talk: Consequence for microbiota\u2013host interaction","volume":"74","author":"Edeas","year":"2015","journal-title":"Pathog. Dis."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1016\/j.neuron.2010.12.032","article-title":"Early Functional Impairment of Sensory-Motor Connectivity in a Mouse Model of Spinal Muscular Atrophy","volume":"69","author":"Mentis","year":"2011","journal-title":"Neuron"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"15","DOI":"10.3389\/fncel.2019.00015","article-title":"The Alteration of Intrinsic Excitability and Synaptic Transmission in Lumbar Spinal Motor Neurons and Interneurons of Severe Spinal Muscular Atrophy Mice","volume":"13","author":"Sun","year":"2019","journal-title":"Front. Cell. Neurosci."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1038\/nn.4561","article-title":"Reduced sensory synaptic excitation impairs motor neuron function via Kv2.1 in spinal muscular atrophy","volume":"20","author":"Fletcher","year":"2017","journal-title":"Nat. Neurosci."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1416","DOI":"10.1016\/j.celrep.2016.06.087","article-title":"A Stem Cell Model of the Motor Circuit Uncouples Motor Neuron Death from Hyperexcitability Induced by SMN Deficiency","volume":"16","author":"Simon","year":"2016","journal-title":"Cell Rep."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"12189","DOI":"10.1038\/srep12189","article-title":"Spinal muscular atrophy patient-derived motor neurons exhibit hyperexcitability","volume":"5","author":"Liu","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"845","DOI":"10.1523\/JNEUROSCI.1654-20.2020","article-title":"Spinal Interneurons as Gatekeepers to Neuroplasticity after Injury or Disease","volume":"41","author":"Zholudeva","year":"2021","journal-title":"J. Neurosci."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"4936","DOI":"10.1038\/s41598-019-39996-4","article-title":"Pitx2 cholinergic interneurons are the source of C bouton synapses on brainstem motor neurons","volume":"9","author":"Rozani","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.neuroscience.2020.07.047","article-title":"Genetic Inactivation of Cholinergic C Bouton Output Improves Motor Performance but not Survival in a Mouse Model of Amyotrophic Lateral Sclerosis","volume":"450","author":"Konsolaki","year":"2020","journal-title":"Neuroscience"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.neuroscience.2020.08.011","article-title":"Differential Loss of Spinal Interneurons in a Mouse Model of ALS","volume":"450","author":"Salamatina","year":"2020","journal-title":"Neuroscience"},{"key":"ref_75","first-page":"496079","article-title":"Study on the Dynamic Changes in Synaptic Vesicle-Associated Protein and Axonal Transport Protein Combined with LPS Neuroinflammation Model","volume":"2013","author":"Zhang","year":"2013","journal-title":"Int. Sch. Res. Not. Neurol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1094","DOI":"10.1016\/j.bbadis.2006.04.002","article-title":"Axonal transport and neurodegenerative disease","volume":"1762","author":"Holzbaur","year":"2006","journal-title":"Biochim. Biophys. Acta Mol. Basis Dis."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1186\/s12974-019-1490-8","article-title":"Lipopolysaccharide-induced neuroinflammation induces presynaptic disruption through a direct action on brain tissue involving microglia-derived interleukin 1 beta","volume":"16","author":"Sheppard","year":"2019","journal-title":"J. Neuroinflamm."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1186\/1750-1326-6-84","article-title":"Microglial p38alpha MAPK is critical for LPS-induced neuron degeneration, through a mechanism involving TNFalpha","volume":"6","author":"Xing","year":"2011","journal-title":"Mol. Neurodegener."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1038\/s41419-017-0153-x","article-title":"Functional and structural damage of neurons by innate immune mechanisms during neurodegeneration","volume":"9","author":"Ising","year":"2018","journal-title":"Cell Death Dis."},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Abati, E., Citterio, G., Bresolin, N., Comi, G.P., and Corti, S. (2020). Glial cells involvement in spinal muscular atrophy: Could SMA be a neuroinflammatory disease?. Neurobiol. Dis., 140.","DOI":"10.1016\/j.nbd.2020.104870"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1002\/acn3.423","article-title":"New insights into SMA pathogenesis: Immune dysfunction and neuroinflammation","volume":"4","author":"Deguise","year":"2017","journal-title":"Ann. Clin. Transl. Neurol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1016\/j.it.2016.06.006","article-title":"Astrocytes: Key Regulators of Neuroinflammation","volume":"37","author":"Colombo","year":"2016","journal-title":"Trends Immunol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1038\/s41392-023-01588-0","article-title":"Microglia in neurodegenerative diseases: Mechanism and potential therapeutic targets","volume":"8","author":"Gao","year":"2023","journal-title":"Signal Transduct. Target. Ther."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1038\/s41586-018-0119-x","article-title":"Microglial control of astrocytes in response to microbial metabolites","volume":"557","author":"Rothhammer","year":"2018","journal-title":"Nature"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/j.ajpath.2012.10.014","article-title":"Lipopolysaccharide Causes an Increase in Intestinal Tight Junction Permeability in Vitro and in Vivo by Inducing Enterocyte Membrane Expression and Localization of TLR-4 and CD14","volume":"182","author":"Guo","year":"2012","journal-title":"Am. J. Pathol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"279","DOI":"10.3389\/fnagi.2019.00279","article-title":"The Immune System Drives Synapse Loss During Lipopolysaccharide-Induced Learning and Memory Impairment in Mice","volume":"11","author":"Xin","year":"2019","journal-title":"Front. Aging Neurosci."},{"key":"ref_87","doi-asserted-by":"crossref","unstructured":"Sabogal-Gu\u00e1queta, A.M., Marmolejo-Garza, A., de P\u00e1dua, V.P., Eggen, B., Boddeke, E., and Dolga, A.M. (2020). Microglia alterations in neurodegenerative diseases and their modeling with human induced pluripotent stem cell and other platforms. Prog. Neurobiol., 190.","DOI":"10.1016\/j.pneurobio.2020.101805"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"2739","DOI":"10.1007\/s00018-019-03111-7","article-title":"Astrocyte alterations in neurodegenerative pathologies and their modeling in human induced pluripotent stem cell platforms","volume":"76","author":"Oksanen","year":"2019","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1007\/s00401-023-02554-4","article-title":"Spinal astrocyte dysfunction drives motor neuron loss in late-onset spinal muscular atrophy","volume":"145","author":"Schmitt","year":"2023","journal-title":"Acta Neuropathol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"1337","DOI":"10.1002\/glia.24177","article-title":"Survival motor neuron protein deficiency alters microglia reactivity","volume":"70","author":"Khayrullina","year":"2022","journal-title":"Glia"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"215","DOI":"10.3389\/fncel.2018.00215","article-title":"Microglia Responses to Pro-inflammatory Stimuli (LPS, IFNgamma+TNFalpha) and Reprogramming by Resolving Cytokines (IL-4, IL-10)","volume":"12","author":"Lively","year":"2018","journal-title":"Front. Cell. Neurosci."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"2020","DOI":"10.2174\/1570159X21666221129121715","article-title":"Bidirectional Communication Between Microglia and Astrocytes in Neuroinflammation","volume":"21","author":"Bhusal","year":"2023","journal-title":"Curr. Neuropharmacol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"989","DOI":"10.1002\/glia.24153","article-title":"Viral mediated knockdown of GATA6 in SMA iPSC-derived astrocytes prevents motor neuron loss and microglial activation","volume":"70","author":"Allison","year":"2022","journal-title":"Glia"}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/13\/9\/785\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:39:33Z","timestamp":1760107173000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/13\/9\/785"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,5,4]]},"references-count":93,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2024,5]]}},"alternative-id":["cells13090785"],"URL":"https:\/\/doi.org\/10.3390\/cells13090785","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,5,4]]}}}