Inhibition of MALT1 Alleviates Spinal Ischemia/Reperfusion Injury-Induced Neuroinflammation by Modulating Glial Endoplasmic Reticulum Stress in Rats

References

• Awad H, Ramadan ME, El Sayed HF, Tolpin DA, Tili E, Collard CD. Spinal cord injury after thoracic endovascular aortic aneurysm repair. Can J Anaesth. 2017;64(12):1218–1235.
   PubMed Web of Science ®Google Scholar
• Aucoin VJ, Eagleton MJ, Farber MA, et al. Spinal cord protection practices used during endovascular repair of complex aortic aneurysms by the U.S. Aortic Research Consortium. J Vasc Surg. 2021;73(1):323–330.
   PubMed Web of Science ®Google Scholar
• Karve IP, Taylor JM, Crack PJ. The contribution of astrocytes and microglia to traumatic brain injury. Br J Pharmacol. 2016;173(4):692–702.
   PubMed Web of Science ®Google Scholar
• Zhu P, Li JX, Fujino M, Zhuang J, Li XK. Development and treatments of inflammatory cells and cytokines in spinal cord ischemia-reperfusion injury. Mediators Inflamm. 2013;2013:701970.
   PubMed Web of Science ®Google Scholar
• Roussel BD, Kruppa AJ, Miranda E, Crowther DC, Lomas DA, Marciniak SJ. Endoplasmic reticulum dysfunction in neurological disease. Lancet Neurol. 2013;12(1):105–118.
   PubMed Web of Science ®Google Scholar
• Zhu H, Zhou H. Novel insight into the role of endoplasmic reticulum stress in the pathogenesis of myocardial ischemia-reperfusion injury. Oxid Med Cell Longev. 2021;2021:5529810.
   PubMed Web of Science ®Google Scholar
• Park SJ, Li C, Chen YM. Endoplasmic reticulum calcium homeostasis in kidney disease: pathogenesis and therapeutic targets. Am J Pathol. 2021;191(2):256–265.
   PubMed Web of Science ®Google Scholar
• Mizukami T, Orihashi K, Herlambang B, et al. Sodium 4-phenylbutyrate protects against spinal cord ischemia by inhibition of endoplasmic reticulum stress. J Vasc Surg. 2010;52(6):1580–1586.
   PubMed Web of Science ®Google Scholar
• Amani H, Shahbazi MA, D’Amico C, Fontana F, Abbaszadeh S, Santos HA. Microneedles for painless transdermal immunotherapeutic applications. J Control Release. 2021;330:185–217.
   PubMed Web of Science ®Google Scholar
• Nan D, Jin H, Deng J, et al. Cilostazol ameliorates ischemia/reperfusion-induced tight junction disruption in brain endothelial cells by inhibiting endoplasmic reticulum stress. FASEB J. 2019;33(9):10152–10164.
   PubMed Web of Science ®Google Scholar
• Wang HF, Wang ZQ, Ding Y, et al. Endoplasmic reticulum stress regulates oxygen-glucose deprivation-induced parthanatos in human SH-SY5Y cells via improvement of intracellular ROS. CNS Neurosci Ther. 2018;24(1):29–38.
   PubMed Web of Science ®Google Scholar
• Lin Y, Zhang C, Xiang P, Shen J, Sun W, Yu H. Exosomes derived from HeLa cells break down vascular integrity by triggering endoplasmic reticulum stress in endothelial cells. J Extracell Vesicles. 2020;9(1):1722385.
   PubMed Web of Science ®Google Scholar
• Ruland J, Hartjes L. CARD-BCL-10-MALT1 signalling in protective and pathological immunity. Nat Rev Immunol. 2019;19(2):118–134.
   PubMed Web of Science ®Google Scholar
• Engelmann C, Haenold R. Transcriptional control of synaptic plasticity by transcription factor NF-κB. Neural Plast. 2016;2016:7027949.
   PubMed Web of Science ®Google Scholar
• Izumi K, Nishikori M, Yuan H, Otsuka Y, Nakao K, Takaori-Kondo A. Establishment and characterization of a MALT lymphoma cell line carrying an API2-MALT1 translocation. Genes Chromosomes Cancer. 2020;59(9):517–524.
   PubMed Web of Science ®Google Scholar
• Frakes AE, Dillin A. The UPR(ER): sensor and coordinator of organismal homeostasis. Mol Cell. 2017;66(6):761–771.
   PubMed Web of Science ®Google Scholar
• Fontan L, Yang C, Kabaleeswaran V, et al. MALT1 small molecule inhibitors specifically suppress ABC-DLBCL in vitro and in vivo. Cancer Cell. 2012;22(6):812–824.
   PubMed Web of Science ®Google Scholar
• Taira Y, Marsala M. Effect of proximal arterial perfusion pressure on function, spinal cord blood flow, and histopathologic changes after increasing intervals of aortic occlusion in the rat. Stroke. 1996;27(10):1850–1858.
   PubMed Web of Science ®Google Scholar
• Kerkhofs D, van Hagen BT, Milanova IV, et al. Pharmacological depletion of microglia and perivascular macrophages prevents Vascular Cognitive Impairment in Ang II-induced hypertension. Theranostics. 2020;10(21):9512–9527.
   PubMed Web of Science ®Google Scholar
• Zhang S, Hu L, Jiang J, et al. HMGB1/RAGE axis mediates stress-induced RVLM neuroinflammation in mice via impairing mitophagy flux in microglia. J Neuroinflammation. 2020;17(1):15.
   PubMed Web of Science ®Google Scholar
• Khachatryan Z, Haunschild J, von Aspern K, Borger MA, Etz CD. Ischemic spinal cord injury - experimental evidence and evolution of protective measures. Ann Thorac Surg. 2021;S0003–4975:21.
   Google Scholar
• Bramlett HM, Dietrich WD. Long-term consequences of traumatic brain injury: current status of potential mechanisms of injury and neurological outcomes. J Neurotrauma. 2015;32(23):1834–1848.
   PubMed Web of Science ®Google Scholar
• Dong W, Liu Y, Peng J, et al. The IRAK-1-BCL10-MALT1-TRAF6-TAK1 cascade mediates signaling to NF-kappaB from Toll-like receptor 4. J Biol Chem. 2006;281(36):26029–26040.
   PubMed Web of Science ®Google Scholar
• McAllister-Lucas LM, Ruland J, Siu K, et al. CARMA3/Bcl10/MALT1-dependent NF-kappaB activation mediates angiotensin II-responsive inflammatory signaling in nonimmune cells. Proc Natl Acad Sci U S A. 2007;104(1):139–144.
   PubMed Web of Science ®Google Scholar
• Markó L, Park JK, Henke N, et al. B-cell lymphoma/leukaemia 10 and angiotensin II-induced kidney injury. Cardiovasc Res. 2020;116(5):1059–1070.
   PubMed Web of Science ®Google Scholar
• Güler A, Sahin MA, Ucak A, et al. Protective effects of angiotensin II type-1 receptor blockade with olmesartan on spinal cord ischemia-reperfusion injury: an experimental study on rats. Ann Vasc Surg. 2010;24(6):801–808.
   PubMed Web of Science ®Google Scholar
• Li XQ, Lv HW, Wang ZL, Tan WF, Fang B, Ma H. MiR-27a ameliorates inflammatory damage to the blood-spinal cord barrier after spinal cord ischemia: reperfusion injury in rats by downregulating TICAM-2 of the TLR4 signaling pathway. J Neuroinflammation. 2015;12:25.
   PubMed Web of Science ®Google Scholar
• Li XQ, Lv HW, Tan WF, Fang B, Wang H, Ma H. Role of the TLR4 pathway in blood-spinal cord barrier dysfunction during the bimodal stage after ischemia/reperfusion injury in rats. J Neuroinflammation. 2014;11:62.
   PubMed Web of Science ®Google Scholar
• Wang L, Yao Y, He R, et al. Methane ameliorates spinal cord ischemia-reperfusion injury in rats: antioxidant, anti-inflammatory and anti-apoptotic activity mediated by Nrf2 activation. Free Radic Biol Med. 2017;103:69–86.
   PubMed Web of Science ®Google Scholar
• Mussbacher M, Salzmann M, Brostjan C, et al. Cell type-specific roles of NF-κB linking inflammation and thrombosis. Front Immunol. 2019;10:85.
   PubMed Web of Science ®Google Scholar
• Shih RH, Wang CY, Yang CM. NF-kappaB signaling pathways in neurological inflammation: a mini review. Front Mol Neurosci. 2015;8:77.
   PubMed Web of Science ®Google Scholar
• Wang D, Chen F, Fang B, et al. MiR-128-3p alleviates spinal cord ischemia/reperfusion injury associated neuroinflammation and cellular apoptosis via SP1 suppression in rat. Front Neurosci. 2020;14:609613.
   PubMed Web of Science ®Google Scholar
• Bhattacharya A, Kaushik DK, Lozinski BM, Yong VW. Beyond barrier functions: roles of pericytes in homeostasis and regulation of neuroinflammation. J Neurosci Res. 2020;98(12):2390–2405.
   PubMed Web of Science ®Google Scholar
• Mészáros Á, Molnár K, Nógrádi B, et al. Neurovascular inflammaging in health and disease. Cells. 2020;9(7):1614.
   PubMed Web of Science ®Google Scholar
• Ye LX, An NC, Huang P, et al. Exogenous platelet-derived growth factor improves neurovascular unit recovery after spinal cord injury. Neural Regen Res. 2021;16(4):765–771.
   PubMed Web of Science ®Google Scholar
• Yuan X, Wu Q, Wang P, et al. Exosomes derived from pericytes improve microcirculation and protect blood-spinal cord barrier after spinal cord injury in mice. Front Neurosci. 2019;13:319.
   PubMed Web of Science ®Google Scholar
• Rashid HO, Yadav RK, Kim HR, Chae HJ. ER stress: autophagy induction, inhibition and selection. Autophagy. 2015;11(11):1956–1977.
   PubMed Web of Science ®Google Scholar
• Senft D, Ronai ZA. UPR, autophagy, and mitochondria crosstalk underlies the ER stress response. Trends Biochem Sci. 2015;40(3):141–148.
   PubMed Web of Science ®Google Scholar
• Folch-Puy E, Panisello A, Oliva J, et al. Relevance of endoplasmic reticulum stress cell signaling in liver cold ischemia reperfusion injury. Int J Mol Sci. 2016;17(6):807.
   PubMed Web of Science ®Google Scholar
• Lin Y, Jiang M, Chen W, Zhao T, Wei Y. Cancer and ER stress: mutual crosstalk between autophagy, oxidative stress and inflammatory response. Biomed Pharmacother. 2019;118:109249.
   PubMed Web of Science ®Google Scholar
• Namgaladze D, Khodzhaeva V, Brüne B. ER-mitochondria communication in cells of the innate immune system. Cells. 2019;8(9):1088.
   PubMed Web of Science ®Google Scholar
• Sprenkle NT, Sims SG, Sánchez CL, Meares GP. Endoplasmic reticulum stress and inflammation in the central nervous system. Mol Neurodegener. 2017;12(1):42.
   PubMed Web of Science ®Google Scholar
• Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. 2012;13(2):89–102.
   PubMed Web of Science ®Google Scholar
• Liu LR, Liu JC, Bao JS, Bai QQ, Wang GQ. Interaction of microglia and astrocytes in the neurovascular unit. Front Immunol. 2020;11:1024.
   PubMed Web of Science ®Google Scholar
• Neuroimmunological I-KH. Implications of AQP4 in astrocytes. Int J Mol Sci. 2016;17(8):1306.
   PubMed Web of Science ®Google Scholar
• Sun XG, Duan H, Jing G, Wang G, Hou Y, Zhang M. Inhibition of TREM-1 attenuates early brain injury after subarachnoid hemorrhage via downregulation of p38MAPK/MMP-9 and preservation of ZO-1. Neuroscience. 2019;406:369–375.
   PubMed Web of Science ®Google Scholar
• Li XF, Zhang XJ, Zhang C, et al. Ulinastatin protects brain against cerebral ischemia/reperfusion injury through inhibiting MMP-9 and alleviating loss of ZO-1 and occludin proteins in mice. Exp Neurol. 2018;302:68–74.
   PubMed Web of Science ®Google Scholar
• Noble LJ, Donovan F, Igarashi T, Goussev S, Werb Z. Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events. J Neurosci. 2002;22(17):7526–7535.
   PubMed Web of Science ®Google Scholar
• Abbott NJ. Inflammatory mediators and modulation of blood-brain barrier permeability. Cell Mol Neurobiol. 2000;20(2):131–147.
   PubMed Web of Science ®Google Scholar
• Cohen-Salmon M, Slaoui L, Mazaré N, et al. Astrocytes in the regulation of cerebrovascular functions. Glia. 2021;69(4):817–841.
   PubMed Web of Science ®Google Scholar
• Yamanaka K, Sasaki N, Fujita Y, Kawamoto A, Hirata K, Okita Y. Impact of acquired and innate immunity on spinal cord ischemia and reperfusion injury. Gen Thorac Cardiovasc Surg. 2016;64(5):251–259.
   PubMed Web of Science ®Google Scholar
• Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci. 2001;21(8):2580–2588.
   PubMed Web of Science ®Google Scholar
• Matsumoto S, Matsumoto M, Yamashita A, et al. The temporal profile of the reaction of microglia, astrocytes, and macrophages in the delayed onset paraplegia after transient spinal cord ischemia in rabbits. Anesth Analg. 2003;96:6.
   Web of Science ®Google Scholar