Downregulation of miR-7116-5p in microglia by MPP+ sensitizes TNF-α production to induce dopaminergic neuron damage

GLIA

Volumn 65, Issue 8, 2017, Pages 1251-1263

  He, Qian ^a,b   Wang, Qing ^a,b   Yuan, Chao ^c   Wang, Yizheng ^a  

^a Institute of Neuroscience   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c Department of Pharmacology   (China)

Author keywords

microRNA; neuroinflammation; organic cation transporter 3; Parkinson's disease

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; 1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; MICRORNA; MICRORNA 7116 5P; ORGANIC CATION TRANSPORTER 3; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CD11B ANTIGEN; DOPAMINE RECEPTOR STIMULATING AGENT; GLIAL FIBRILLARY ACIDIC PROTEIN; MIRN712 MICRORNA, MOUSE; OCTAMER TRANSCRIPTION FACTOR 4; POU5F1 PROTEIN, MOUSE; TRITIUM;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOPAMINERGIC NERVE CELL; DOWN REGULATION; GENE EXPRESSION; MALE; MICROGLIA; MOUSE; MPTP-INDUCED PARKINSONISM; NERVOUS SYSTEM INFLAMMATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; VENTRAL MESENCEPHALON; ANIMAL; C57BL MOUSE; CELL CULTURE; DEPENDOPARVOVIRUS; DRUG EFFECTS; GENETICS; METABOLISM; NEWBORN; TRANSGENIC MOUSE; TRANSPORT AT THE CELLULAR LEVEL;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL TRANSPORT; CD11B ANTIGEN; CELLS, CULTURED; DEPENDOVIRUS; DOPAMINE AGENTS; DOPAMINERGIC NEURONS; DOWN-REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MICRORNAS; OCTAMER TRANSCRIPTION FACTOR-3; TRITIUM; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85019636622     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.23153     Document Type: Article

References (52)

1. Asci R, Vallefuoco F, Andolfo I, Bruno M, De Falco L, & Iolascon A. 2013. Trasferrin receptor 2 gene regulation by microRNA 221 in SH-SY5Y cells treated with MPP(+) as Parkinson's disease cellular model. Neuroscience Research, 77, 121–127.
2. Ballard PA, Tetrud JW, & Langston JW. 1985. Permanent human parkinsonism due to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP): Seven cases. Neurology, 35, 949–956.
3. Barcia C, Sanchez Bahillo A, Fernandez-Villalba E, Bautista V, Poza YPM, Fernandez-Barreiro A, … Herrero MT. 2004. Evidence of active microglia in substantia nigra pars compacta of parkinsonian monkeys 1 year after MPTP exposure. Glia, 46, 402–409.
4. Bezard E, Gross CE, Fournier MC, Dovero S, Bloch B, & Jaber M. 1999. Absence of MPTP-induced neuronal death in mice lacking the dopamine transporter. Experimental Neurology, 155, 268–273.
5. Blum D, Torch S, Lambeng N, Nissou M, Benabid AL, Sadoul R, & Verna JM. 2001. Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: Contribution to the apoptotic theory in Parkinson's disease. Progress in Neurobiology, 65, 135–172.
6. Boka G, Anglade P, Wallach D, Javoy-Agid F, Agid Y, & Hirsch EC. 1994. Immunocytochemical analysis of tumor necrosis factor and its receptors in Parkinson's disease. Neuroscience Letters, 172, 151–154.
7. Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, & Braak E. 2003. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging, 24, 197–211.
8. Brochard V, Combadiere B, Prigent A, Laouar Y, Perrin A, Beray-Berthat V, Bonduelle O, Alvarez-Fischer D, Callebert J, Launay JM, et al. 2009. Infiltration of CD4+ lymphocytes into the brain contributes to neurodegeneration in a mouse model of Parkinson disease. Journal of Clinical Investigation, 119, 182–192.
9. Cardo LF, Coto E, Ribacoba R, Menendez M, Moris G, Suarez E, & Alvarez V. 2014. MiRNA profile in the substantia nigra of Parkinson's disease and healthy subjects. Journal of Molecular Neuroscience, 54, 830–836.
10. Cui M, Aras R, Christian WV, Rappold PM, Hatwar M, Panza J, Jackson-Lewis V, Javitch JA, Ballatori N, Przedborski S, et al. 2009. The organic cation transporter-3 is a pivotal modulator of neurodegeneration in the nigrostriatal dopaminergic pathway. Proceedings of the National Academy of the Sciences United States of America, 106, 8043–8048.
11. Di Monte DA, Wu EY, & Langston JW. 1992. Role of astrocytes in MPTP metabolism and toxicity. Annals of the New York Academy of Sciences, 648, 219–228.
12. Fearnley JM, & Lees AJ. 1991. Ageing and Parkinson's disease: Substantia nigra regional selectivity. Brain, 114, 2283–2301.
13. Ferger B, Leng A, Mura A, Hengerer B, & Feldon J. 2004. Genetic ablation of tumor necrosis factor-alpha (TNF-alpha) and pharmacological inhibition of TNF-synthesis attenuates MPTP toxicity in mouse striatum. Journal of Neurochemistry, 89, 822–833.
14. Forloni G, Mangiarotti F, Angeretti N, Lucca E, & De Simoni MG. 1997. Beta-amyloid fragment potentiates IL-6 and TNF-alpha secretion by LPS in astrocytes but not in microglia. Cytokine, 9, 759–762.
15. Gainetdinov RR, Fumagalli F, Jones SR, & Caron MG. 1997. Dopamine transporter is required for in vivo MPTP neurotoxicity: Evidence from mice lacking the transporter. Journal of Neurochemistry, 69, 1322–1325.
16. Gao X, Chen H, Schwarzschild MA, & Ascherio A. 2011. Use of ibuprofen and risk of Parkinson disease. Neurology, 76, 863–869.
17. Gerhard A, Pavese N, Hotton G, Turkheimer F, Es M, Hammers A, … Brooks DJ. 2006. In vivo imaging of microglial activation with [11C](R)-PK11195 PET in idiopathic Parkinson's disease. Neurobiology of Disease, 21, 404–412.
18. Guan Y, Yao H, Wang J, Sun K, Cao L, & Wang Y. 2015. NF-kappaB-DICER-miRs axis regulates TNF-alpha expression in responses to endotoxin stress. International Journal of Biological Sciences, 11, 1257–1268.
19. Heikkila RE, Manzino L, Cabbat FS, & Duvoisin RC. 1984. Protection against the dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine by monoamine oxidase inhibitors. Nature, 311, 467–469.
20. Hirsch EC, & Hunot S. 2009. Neuroinflammation in Parkinson's disease: A target for neuroprotection? The Lancet Neurology, 8, 382–397.
21. Kanaan NM, Kordower JH, & Collier TJ. 2008. Age and region-specific responses of microglia, but not astrocytes, suggest a role in selective vulnerability of dopamine neurons after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure in monkeys. Glia, 56, 1199–1214.
22. Kim YS, Choi DH, Block ML, Lorenzl S, Yang L, Kim YJ, Sugama S, Cho BP, Hwang O, Browne SE, et al. 2007. A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation. FASEB Journal, 21, 179–187.
23. Langston JW, Forno LS, Tetrud J, Reeves AG, Kaplan JA, & Karluk D. 1999. Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure. Annals of Neurology, 46, 598–605.
24. Langston JW, Irwin I, Langston EB, & Forno LS. 1984. 1-Methyl-4-phenylpyridinium ion (MPP+): Identification of a metabolite of MPTP, a toxin selective to the substantia nigra. Neuroscience Letters, 48, 87–92.
25. Liberatore GT, Jackson-Lewis V, Vukosavic S, Mandir AS, Vila M, McAuliffe WG, … Przedborski S. 1999. Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nature Medicine, 5, 1403–1409.
26. Liu T, Clark RK, McDonnell PC, Young PR, White RF, Barone FC, & Feuerstein GZ. 1994. Tumor necrosis factor-alpha expression in ischemic neurons. Stroke, 25, 1481–1488.
27. Main BS, Zhang M, Brody KM, Ayton S, Frugier T, Steer D, … Taylor JM. 2016. Type-1 interferons contribute to the neuroinflammatory response and disease progression of the MPTP mouse model of Parkinson's disease. Glia, 64, 1590–1604.
28. Martin HL, Santoro M, Mustafa S, Riedel G, Forrester JV, & Teismann P. 2016. Evidence for a role of adaptive immune response in the disease pathogenesis of the MPTP mouse model of Parkinson's disease. Glia, 64, 386–395.
29. McGeer PL, Itagaki S, Boyes BE, & McGeer EG. 1988. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology, 38, 1285–1291.
30. McGeer PL, & McGeer EG. 2007. NSAIDs and Alzheimer disease: Epidemiological, animal model and clinical studies. Neurobiol Aging, 28, 639–647.
31. Mogi M, Harada M, Kondo T, Riederer P, Inagaki H, Minami M, & Nagatsu T. 1994a. Interleukin-1 beta, interleukin-6, epidermal growth factor and transforming growth factor-alpha are elevated in the brain from parkinsonian patients. Neuroscience Letters, 180, 147–150.
32. Mogi M, Harada M, Riederer P, Narabayashi H, Fujita K, & Nagatsu T. 1994b. Tumor necrosis factor-alpha (TNF-alpha) increases both in the brain and in the cerebrospinal fluid from parkinsonian patients. Neuroscience Letters, 165, 208–210.
33. Nishimura M, Mizuta I, Mizuta E, Yamasaki S, Ohta M, Kaji R, & Kuno S. 2001. Tumor necrosis factor gene polymorphisms in patients with sporadic Parkinson's disease. Neuroscience Letters, 311, 1–4.
34. Niu M, Xu R, Wang J, Hou B, & Xie A. 2016. MiR-133b ameliorates axon degeneration induced by MPP(+) via targeting RhoA. Neuroscience, 325, 39–49.
35. Ouchi Y, Yoshikawa E, Sekine Y, Futatsubashi M, Kanno T, Ogusu T, & Torizuka T. 2005. Microglial activation and dopamine terminal loss in early Parkinson's disease. Annals of Neurology, 57, 168–175.
36. Reines SA, Block GA, Morris JC, Liu G, Nessly ML, Lines CR, … Baranak CC. 2004. Rofecoxib: No effect on Alzheimer's disease in a 1-year, randomized, blinded, controlled study. Neurology, 62, 66–71.
37. Saijo K, Winner B, Carson CT, Collier JG, Boyer L, Rosenfeld MG, … Glass CK. 2009. A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell, 137, 47–59.
38. Sauer H, Rosenblad C, & Bjorklund A. 1995. Glial cell line-derived neurotrophic factor but not transforming growth factor beta 3 prevents delayed degeneration of nigral dopaminergic neurons following striatal 6-hydroxydopamine lesion. Proceedings of the National Academy of the Sciences United States of America, 92, 8935–8939.
39. Scharf S, Mander A, Ugoni A, Vajda F, & Christophidis N. 1999. A double-blind, placebo-controlled trial of diclofenac/misoprostol in Alzheimer's disease. Neurology, 53, 197–201.
40. Shang T, Uihlein AV, Van Asten J, Kalyanaraman B, & Hillard CJ. 2003. 1-Methyl-4-phenylpyridinium accumulates in cerebellar granule neurons via organic cation transporter 3. Journal of Neurochemistry, 85, 358–367.
41. Shao W, Zhang SZ, Tang M, Zhang XH, Zhou Z, Yin YQ, Zhou QB, Huang YY, Liu YJ, Wawrousek E, et al. 2013. Suppression of neuroinflammation by astrocytic dopamine D2 receptors via alphaB-crystallin. Nature, 494, 90–94.
42. Simon LS. 1999. Role and regulation of cyclooxygenase-2 during inflammation. American Journal of Medicine, 106, 37S–42S.
43. Sriram K, Matheson JM, Benkovic SA, Miller DB, Luster MI, & O'Callaghan JP. 2002. Mice deficient in TNF receptors are protected against dopaminergic neurotoxicity: Implications for Parkinson's disease. FASEB Journal, 16, 1474–1476.
44. Sriram K, Matheson JM, Benkovic SA, Miller DB, Luster MI, & O'Callaghan JP. 2006. Deficiency of TNF receptors suppresses microglial activation and alters the susceptibility of brain regions to MPTP-induced neurotoxicity: Role of TNF-alpha. FASEB Journal, 20, 670–682.
45. Tili E, Michaille JJ, Cimino A, Costinean S, Dumitru CD, Adair B, Fabbri M, Alder H, Liu CG, Calin GA, et al. 2007. Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. Journal of Immunology, 179, 5082–5089.
46. Ungerstedt U. 1968. 6-Hydroxy-dopamine induced degeneration of central monoamine neurons. European Journal of Pharmacology, 5, 107–110.
47. Vane JR, Mitchell JA, Appleton I, Tomlinson A, Bishop-Bailey D, Croxtall J, & Willoughby DA. 1994. Inducible isoforms of cyclooxygenase and nitric-oxide synthase in inflammation. Proceedings of the National Academy of the Sciences United States of America, 91, 2046–2050.
48. Wang T, Zhang W, Pei Z, Block M, Wilson B, Reece JM, … Hong JS. 2006. Reactive microgliosis participates in MPP+-induced dopaminergic neurodegeneration: Role of 67 kDa laminin receptor. FASEB Journal, 20, 906–915.
49. Winter J, Jung S, Keller S, Gregory RI, & Diederichs S. 2009. Many roads to maturity: MicroRNA biogenesis pathways and their regulation. Nature Cell Biology, 11, 228–234.
50. Wu DC, Jackson-Lewis V, Vila M, Tieu K, Teismann P, Vadseth C, … Przedborski S. 2002. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. Journal of Neuroscience, 22, 1763–1771.
51. Zhang C, Ge X, Liu Q, Jiang M, Li MW, & Li H. 2015. MicroRNA-mediated non-cell-autonomous regulation of cortical radial glial transformation revealed by a Dicer1 knockout mouse model. Glia, 63, 860–876.
52. Zhang L, Dong LY, Li YJ, Hong Z, & Wei WS. 2012. The microRNA miR-181c controls microglia-mediated neuronal apoptosis by suppressing tumor necrosis factor. Journal of Neuroinflammation, 9, 211.