Microglial Activation Mediates Noradrenergic Locus Coeruleus Neurodegeneration via Complement Receptor 3 in a Rotenone-Induced Parkinson’s Disease Mouse Model

References

• Nistico R, Mehdawy B, Piccirilli S, et al. Paraquat- and rotenone-induced models of Parkinson’s disease. Int J Immunopathol Pharmacol. 2011;24(2):313–322. doi:10.1177/039463201102400205
   PubMed Web of Science ®Google Scholar
• Tanner CM, Kamel F, Ross GW, et al. Rotenone, paraquat, and Parkinson’s disease. Environ Health Perspect. 2011;119(6):866–872. doi:10.1289/ehp.1002839
   PubMed Web of Science ®Google Scholar
• Zaitone SA, Ahmed E, Elsherbiny NM, et al. Caffeic acid improves locomotor activity and lessens inflammatory burden in a mouse model of rotenone-induced nigral neurodegeneration: relevance to Parkinson’s disease therapy. Pharmacol Rep. 2019;71(1):32–41. doi:10.1016/j.pharep.2018.08.004
   PubMed Web of Science ®Google Scholar
• Tapias V, McCoy JL, Greenamyre JT. Phenothiazine normalizes the NADH/NAD(+) ratio, maintains mitochondrial integrity and protects the nigrostriatal dopamine system in a chronic rotenone model of Parkinson’s disease. Redox Biol. 2019;24:101164. doi:10.1016/j.redox.2019.101164
   PubMed Web of Science ®Google Scholar
• Betarbet R, Sherer TB, MacKenzie G, et al. Chronic systemic pesticide exposure reproduces features of Parkinson’s disease. Nat Neurosci. 2000;3(12):1301–1306. doi:10.1038/81834
   PubMed Web of Science ®Google Scholar
• Braak H, Ghebremedhin E, Rüb U, et al. Stages in the development of Parkinson’s disease-related pathology. Cell Tissue Res. 2004;318(1):121–134. doi:10.1007/s00441-004-0956-9
   PubMed Web of Science ®Google Scholar
• Zarow C, Lyness SA, Mortimer JA, et al. Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch Neurol. 2003;60(3):337–341. doi:10.1001/archneur.60.3.337
   PubMedGoogle Scholar
• Hou L, Sun F, Sun W, et al. Lesion of the locus coeruleus damages learning and memory performance in paraquat and maneb-induced mouse Parkinson’s disease model. Neuroscience. 2019;419:129–140. doi:10.1016/j.neuroscience.2019.09.006
   PubMed Web of Science ®Google Scholar
• Song S, Wang Q, Jiang L, et al. Noradrenergic dysfunction accelerates LPS-elicited inflammation-related ascending sequential neurodegeneration and deficits in non-motor/motor functions. Brain Behav Immun. 2019;81:374–387. doi:10.1016/j.bbi.2019.06.034
   PubMed Web of Science ®Google Scholar
• Subhramanyam CS, Wang C, Hu Q, et al. Microglia-mediated neuroinflammation in neurodegenerative diseases. Semin Cell Dev Biol. 2019;94:112–120. doi:10.1016/j.semcdb.2019.05.004
   PubMed Web of Science ®Google Scholar
• Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 2007;8(1):57–69. doi:10.1038/nrn2038
   PubMed Web of Science ®Google Scholar
• O’Neill E, Harkin A. Targeting the noradrenergic system for anti-inflammatory and neuroprotective effects: implications for Parkinson’s disease. Neural Regen Res. 2018;13(8):1332–1337. doi:10.4103/1673-5374.235219
   PubMed Web of Science ®Google Scholar
• Hou L, Zhang C, Wang K, et al. Paraquat and maneb co-exposure induces noradrenergic locus coeruleus neurodegeneration through NADPH oxidase-mediated microglial activation. Toxicology. 2017;380:1–10. doi:10.1016/j.tox.2017.02.009
   PubMed Web of Science ®Google Scholar
• Song S, Jiang L, Oyarzabal EA, et al. Loss of brain norepinephrine elicits neuroinflammation-mediated oxidative injury and selective caudo-rostral neurodegeneration. Mol Neurobiol. 2019;56(4):2653–2669. doi:10.1007/s12035-018-1235-1
   PubMed Web of Science ®Google Scholar
• Zhang C, Hou L, Yang J, et al. 2,5-Hexanedione induces dopaminergic neurodegeneration through integrin α(M)β2/NADPH oxidase axis-mediated microglial activation. Cell Death Dis. 2018;9(2):60. doi:10.1038/s41419-017-0091-7
   PubMedGoogle Scholar
• Gao HM, Liu B, Zhang W, et al. Critical role of microglial NADPH oxidase-derived free radicals in the in vitro MPTP model of Parkinson’s disease. FASEB J. 2003;17(13):1954–1956. doi:10.1096/fj.03-0109fje
   PubMedGoogle Scholar
• Wu XF, Block ML, Zhang W, et al. The role of microglia in paraquat-induced dopaminergic neurotoxicity. Antioxid Redox Signal. 2005;7(5–6):654–661. doi:10.1089/ars.2005.7.654
   PubMed Web of Science ®Google Scholar
• Chen X, Liu Z, Cao BB, et al. TGF-β1 neuroprotection via inhibition of microglial activation in a rat model of Parkinson’s disease. J Neuroimmune Pharmacol. 2017;12(3):433–446. doi:10.1007/s11481-017-9732-y
   PubMed Web of Science ®Google Scholar
• Che Y, Hou L, Sun F, et al. Taurine protects dopaminergic neurons in a mouse Parkinson’s disease model through inhibition of microglial M1 polarization. Cell Death Dis. 2018;9(4):435. doi:10.1038/s41419-018-0468-2
   PubMedGoogle Scholar
• De Miranda BR, Rocha EM, Bai Q, et al. Astrocyte-specific DJ-1 overexpression protects against rotenone-induced neurotoxicity in a rat model of Parkinson’s disease. Neurobiol Dis. 2018;115:101–114. doi:10.1016/j.nbd.2018.04.008
   PubMed Web of Science ®Google Scholar
• Zhou F, Wu JY, Sun XL, et al. Iptakalim alleviates rotenone-induced degeneration of dopaminergic neurons through inhibiting microglia-mediated neuroinflammation. Neuropsychopharmacology. 2007;32(12):2570–2580. doi:10.1038/sj.npp.1301381
   PubMed Web of Science ®Google Scholar
• Rosetti F, Mayadas TN. The many faces of Mac-1 in autoimmune disease. Immunol Rev. 2016;269(1):175–193. doi:10.1111/imr.12373
   PubMed Web of Science ®Google Scholar
• Das S, Mishra KP, Ganju L, et al. Intranasally delivered small interfering RNA-mediated suppression of scavenger receptor Mac-1 attenuates microglial phenotype switching and working memory impairment following hypoxia. Neuropharmacology. 2018;137:240–255. doi:10.1016/j.neuropharm.2018.05.002
   PubMed Web of Science ®Google Scholar
• Zhang J, Malik A, Choi HB, et al. Microglial CR3 activation triggers long-term synaptic depression in the hippocampus via NADPH oxidase. Neuron. 2014;82(1):195–207. doi:10.1016/j.neuron.2014.01.043
   PubMed Web of Science ®Google Scholar
• Liberatore GT, Jackson-Lewis V, Vukosavic S, et al. Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat Med. 1999;5(12):1403–1409. doi:10.1038/70978
   PubMed Web of Science ®Google Scholar
• Wang Q, Qian L, Chen SH, et al. Post-treatment with an ultra-low dose of NADPH oxidase inhibitor diphenyleneiodonium attenuates disease progression in multiple Parkinson’s disease models. Brain. 2015;138(Pt 5):1247–1262. doi:10.1093/brain/awv034
   PubMedGoogle Scholar
• Hou L, Bao X, Zang C, et al. Integrin CD11b mediates alpha-synuclein-induced activation of NADPH oxidase through a Rho-dependent pathway. Redox Biol. 2018;14:600–608. doi:10.1016/j.redox.2017.11.010
   PubMed Web of Science ®Google Scholar
• Hou L, Wang K, Zhang C, et al. Complement receptor 3 mediates NADPH oxidase activation and dopaminergic neurodegeneration through a Src-Erk-dependent pathway. Redox Biol. 2018;14:250–260. doi:10.1016/j.redox.2017.09.017
   PubMed Web of Science ®Google Scholar
• Elmore MR, Najafi AR, Koike MA, et al. Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron. 2014;82(2):380–397. doi:10.1016/j.neuron.2014.02.040
   PubMed Web of Science ®Google Scholar
• Khatri DK, Juvekar AR. Neuroprotective effect of curcumin as evinced by abrogation of rotenone-induced motor deficits, oxidative and mitochondrial dysfunctions in mouse model of Parkinson’s disease. Pharmacol Biochem Behav. 2016;150–151:39–47. doi:10.1016/j.pbb.2016.09.002
   PubMed Web of Science ®Google Scholar
• Mitra S, Chakrabarti N, Dutta SS, et al. Gender-specific brain regional variation of neurons, endogenous estrogen, neuroinflammation and glial cells during rotenone-induced mouse model of Parkinson’s disease. Neuroscience. 2015;292:46–70. doi:10.1016/j.neuroscience.2014.12.052
   PubMed Web of Science ®Google Scholar
• Sharma N, Jamwal S, Kumar P. Beneficial effect of antidepressants against rotenone induced Parkinsonism like symptoms in rats. Pathophysiology. 2016;23(2):123–134. doi:10.1016/j.pathophys.2016.03.002
   PubMedGoogle Scholar
• Groh J, Klein D, Berve K, et al. Targeting microglia attenuates neuroinflammation-related neural damage in mice carrying human PLP1 mutations. Glia. 2019;67(2):277–290. doi:10.1002/glia.23539
   PubMed Web of Science ®Google Scholar
• Manso Y, Holland PR, Kitamura A, et al. Minocycline reduces microgliosis and improves subcortical white matter function in a model of cerebral vascular disease. Glia. 2018;66(1):34–46. doi:10.1002/glia.23190
   PubMed Web of Science ®Google Scholar
• Czirr E, Castello NA, Mosher KI, et al. Microglial complement receptor 3 regulates brain Abeta levels through secreted proteolytic activity. J Exp Med. 2017;214(4):1081–1092. doi:10.1084/jem.20162011
   PubMed Web of Science ®Google Scholar
• Hou L, Sun F, Huang R, et al. Inhibition of NADPH oxidase by apocynin prevents learning and memory deficits in a mouse Parkinson’s disease model. Redox Biol. 2019;22:101134. doi:10.1016/j.redox.2019.101134
   PubMed Web of Science ®Google Scholar
• Hou L, Qu X, Qiu X, et al. Integrin CD11b mediates locus coeruleus noradrenergic neurodegeneration in a mouse Parkinson’s disease model. J Neuroinflammation. 2020;17(1):148. doi:10.1186/s12974-020-01823-3
   PubMed Web of Science ®Google Scholar
• Zhang W, Wang T, Qin L, et al. Neuroprotective effect of dextromethorphan in the MPTP Parkinson’s disease model: role of NADPH oxidase. FASEB J. 2004;18(3):589–591. doi:10.1096/fj.03-0983fje
   PubMedGoogle Scholar
• Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates. 2nd ed. San Diego: Academic Press; 2001.
   Google Scholar
• Wang Q, Chu CH, Qian L, et al. Substance P exacerbates dopaminergic neurodegeneration through neurokinin-1 receptor-independent activation of microglial NADPH oxidase. J Neurosci. 2014;34(37):12490–12503. doi:10.1523/JNEUROSCI.2238-14.2014
   PubMed Web of Science ®Google Scholar
• Okubo H, Nakatsu Y, Sakoda H, et al. Mosapride citrate improves nonalcoholic steatohepatitis with increased fecal lactic acid bacteria and plasma glucagon-like peptide-1 level in a rodent model. Am J Physiol Gastrointest Liver Physiol. 2015;308(2):G151–G158. doi:10.1152/ajpgi.00198.2014
   PubMed Web of Science ®Google Scholar
• Hou L, Huang R, Sun F, et al. NADPH oxidase regulates paraquat and maneb-induced dopaminergic neurodegeneration through ferroptosis. Toxicology. 2019;417:64–73. doi:10.1016/j.tox.2019.02.011
   PubMed Web of Science ®Google Scholar
• Hou L, Yang J, Li S, et al. Glibenclamide attenuates 2,5-hexanedione-induced neurotoxicity in the spinal cord of rats through mitigation of NLRP3 inflammasome activation, neuroinflammation and oxidative stress. Toxicol Lett. 2020;331:152–158. doi:10.1016/j.toxlet.2020.06.002
   PubMed Web of Science ®Google Scholar
• Zhang D, Li S, Hou L, et al. Microglial activation contributes to cognitive impairments in rotenone-induced mouse Parkinson’s disease model. J Neuroinflammation. 2021;18(1):4. doi:10.1186/s12974-020-02065-z
   PubMed Web of Science ®Google Scholar
• Mao XY, Zhou HH, Jin WL. Ferroptosis induction in pentylenetetrazole kindling and pilocarpine-induced epileptic seizures in mice. Front Neurosci. 2019;13:721. doi:10.3389/fnins.2019.00721
   PubMed Web of Science ®Google Scholar
• Gassmann M, Grenacher B, Rohde B, et al. Quantifying western blots: pitfalls of densitometry. Electrophoresis. 2009;30(11):1845–1855. doi:10.1002/elps.200800720
   PubMed Web of Science ®Google Scholar
• Lee JM, Kim TW, Park SS, et al. Treadmill exercise improves motor function by suppressing purkinje cell loss in parkinson disease rats. Int Neurourol J. 2018;22(Suppl 3):S147–S155. doi:10.5213/inj.1836226.113
   PubMedGoogle Scholar
• Javed H, Azimullah S, Abul Khair SB, et al. Neuroprotective effect of nerolidol against neuroinflammation and oxidative stress induced by rotenone. BMC Neurosci. 2016;17(1):58. doi:10.1186/s12868-016-0293-4
   PubMed Web of Science ®Google Scholar
• Ojha S, Javed H, Azimullah S, et al. Neuroprotective potential of ferulic acid in the rotenone model of Parkinson’s disease. Drug Des Devel Ther. 2015;9:5499–5510. doi:10.2147/DDDT.S90616
   PubMed Web of Science ®Google Scholar
• Verma DK, Singh DK, Gupta S, et al. Minocycline diminishes the rotenone induced neurotoxicity and glial activation via suppression of apoptosis, nitrite levels and oxidative stress. Neurotoxicology. 2018;65:9–21. doi:10.1016/j.neuro.2018.01.006
   PubMed Web of Science ®Google Scholar
• Sun C, Wang Y, Mo M, et al. Minocycline protects against rotenone-induced neurotoxicity correlating with upregulation of Nurr1 in a Parkinson’s disease rat model. Biomed Res Int. 2019;2019:6843265. doi:10.1155/2019/6843265
   PubMed Web of Science ®Google Scholar
• Maiguel D, Faridi MH, Wei C, et al. Small molecule-mediated activation of the integrin CD11b/CD18 reduces inflammatory disease. Sci Signal. 2011;4(189):ra57. doi:10.1126/scisignal.2001811
   PubMed Web of Science ®Google Scholar
• Budni J, Garcez ML, de Medeiros J, et al. The anti-inflammatory role of minocycline in Alzheimer s disease. Curr Alzheimer Res. 2016;13(12):1319–1329. doi:10.2174/1567205013666160819124206
   PubMed Web of Science ®Google Scholar
• Liang YJ, Feng SY, Qi YP, et al. Contribution of microglial reaction to increased nociceptive responses in high-fat-diet (HFD)-induced obesity in male mice. Brain Behav Immun. 2019;80:777–792. doi:10.1016/j.bbi.2019.05.026
   PubMed Web of Science ®Google Scholar
• Sriram K, Miller DB, O’Callaghan JP. Minocycline attenuates microglial activation but fails to mitigate striatal dopaminergic neurotoxicity: role of tumor necrosis factor-alpha. J Neurochem. 2006;96(3):706–718. doi:10.1111/j.1471-4159.2005.03566.x
   PubMed Web of Science ®Google Scholar
• Kumar V, Singh BK, Chauhan AK, et al. Minocycline rescues from zinc-induced nigrostriatal dopaminergic neurodegeneration: biochemical and molecular interventions. Mol Neurobiol. 2016;53(5):2761–2777. doi:10.1007/s12035-015-9137-y
   PubMed Web of Science ®Google Scholar
• Yang X, Ren H, Wood K, et al. Depletion of microglia augments the dopaminergic neurotoxicity of MPTP. FASEB J. 2018;32(6):3336–3345. doi:10.1096/fj.201700833RR
   PubMed Web of Science ®Google Scholar
• Sosna J, Philipp S, Albay R 3rd, et al. Early long-term administration of the CSF1R inhibitor PLX3397 ablates microglia and reduces accumulation of intraneuronal amyloid, neuritic plaque deposition and pre-fibrillar oligomers in 5XFAD mouse model of Alzheimer’s disease. Mol Neurodegener. 2018;13(1):11. doi:10.1186/s13024-018-0244-x
   PubMedGoogle Scholar
• Gao F, Chen D, Hu Q, et al. Rotenone directly induces BV2 cell activation via the p38 MAPK pathway. PLoS One. 2013;8(8):e72046. doi:10.1371/journal.pone.0072046
   PubMed Web of Science ®Google Scholar
• Wang J, Lai S, Li G, et al. Microglial activation contributes to depressive-like behavior in dopamine D3 receptor knockout mice. Brain Behav Immun. 2020;83:226–238. doi:10.1016/j.bbi.2019.10.016
   PubMed Web of Science ®Google Scholar
• Du Y, Ma Z, Lin S, et al. Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson’s disease. Proc Natl Acad Sci U S A. 2001;98(25):14669–14674. doi:10.1073/pnas.251341998
   PubMed Web of Science ®Google Scholar
• Sherer TB, Betarbet R, Kim JH, et al. Selective microglial activation in the rat rotenone model of Parkinson’s disease. Neurosci Lett. 2003;341(2):87–90. doi:10.1016/S0304-3940(03)00172-1
   PubMed Web of Science ®Google Scholar
• Shaikh SB, Nicholson LF. Effects of chronic low dose rotenone treatment on human microglial cells. Mol Neurodegener. 2009;4(1):55. doi:10.1186/1750-1326-4-55
   PubMedGoogle Scholar
• Hong S, Beja-Glasser VF, Nfonoyim BM, et al. Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science. 2016;352(6286):712–716. doi:10.1126/science.aad8373
   PubMed Web of Science ®Google Scholar
• Van der Jeugd A, Ahmed T, Burnouf S, et al. Hippocampal tauopathy in tau transgenic mice coincides with impaired hippocampus-dependent learning and memory, and attenuated late-phase long-term depression of synaptic transmission. Neurobiol Learn Mem. 2011;95(3):296–304. doi:10.1016/j.nlm.2010.12.005
   PubMed Web of Science ®Google Scholar
• Subramaniam SR, Federoff HJ. Targeting microglial activation states as a therapeutic avenue in Parkinson’s disease. Front Aging Neurosci. 2017;9:176. doi:10.3389/fnagi.2017.00176
   PubMed Web of Science ®Google Scholar
• Yan A, Liu Z, Song L, et al. Idebenone alleviates neuroinflammation and modulates microglial Polarization in LPS-stimulated BV2 cells and MPTP-induced Parkinson’s disease mice. Front Cell Neurosci. 2018;12:529. doi:10.3389/fncel.2018.00529
   PubMed Web of Science ®Google Scholar
• Hou L, Che Y, Sun F, et al. Taurine protects noradrenergic locus coeruleus neurons in a mouse Parkinson’s disease model by inhibiting microglial M1 polarization. Amino Acids. 2018;50(5):547–556. doi:10.1007/s00726-018-2547-1
   PubMed Web of Science ®Google Scholar
• Suo J, Zhang C, Wang P, et al. Allyl sulfide counteracts 1-bromopropane-induced neurotoxicity by inhibiting neuroinflammation and oxidative stress. Toxicol Sci. 2019;167(2):397–407. doi:10.1093/toxsci/kfy240
   PubMed Web of Science ®Google Scholar
• Wang Y, Liu J, Chen M, et al. The novel mechanism of rotenone-induced alpha-synuclein phosphorylation via reduced protein phosphatase 2A activity. Int J Biochem Cell Biol. 2016;75:34–44. doi:10.1016/j.biocel.2016.03.007
   PubMed Web of Science ®Google Scholar
• Hou L, Zhang L, Hong JS, et al. Nicotinamide adenine dinucleotide phosphate oxidase and neurodegenerative diseases: mechanisms and therapy. Antioxid Redox Signal. 2020;33(5):374–393. doi:10.1089/ars.2019.8014
   PubMed Web of Science ®Google Scholar
• Pal R, Monroe TO, Palmieri M, et al. Rotenone induces neurotoxicity through Rac1-dependent activation of NADPH oxidase in SHSY-5Y cells. FEBS Lett. 2014;588(3):472–481. doi:10.1016/j.febslet.2013.12.011
   PubMed Web of Science ®Google Scholar
• Taetzsch T, Block ML. Pesticides, microglial NOX2, and Parkinson’s disease. J Biochem Mol Toxicol. 2013;27(2):137–149. doi:10.1002/jbt.21464
   PubMed Web of Science ®Google Scholar
• Gao HM, Zhou H, Zhang F, Wilson BC, Kam W, Hong JS. HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration. J Neurosci. 2011;31(3):1081–1092. doi:10.1523/JNEUROSCI.3732-10.2011
   PubMed Web of Science ®Google Scholar