Protein kinase Cδ upregulation in microglia drives neuroinflammatory responses and dopaminergic neurodegeneration in experimental models of Parkinson's disease

Neurobiology of Disease

Volumn 93, Issue , 2016, Pages 96-114

  Gordon, Richard ^a,b   Singh, Neeraj ^a   Lawana, Vivek ^a   Ghosh, Anamitra ^a   Harischandra, Dilshan S ^a   Jin, Huajun ^a   Hogan, Colleen ^a   Sarkar, Souvarish ^a   Rokad, Dharmin ^a   Panicker, Nikhil ^a   Anantharam, Vellareddy ^a   Kanthasamy, Anumantha G ^a   Kanthasamy, Arthi ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Dopaminergic degeneration; Microglial activation; Neuroinflammation; NF B; Oxidative stress; Parkinson's disease; PKC delta; PKC ; Synuclein

Indexed keywords

ALPHA SYNUCLEIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; NITRIC OXIDE; PROTEIN KINASE C GAMMA; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; PROTEIN KINASE C DELTA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE ASSOCIATION; DOPAMINERGIC SYSTEM; ENZYME LOCALIZATION; EXPERIMENTAL PARKINSONISM; IN VIVO STUDY; MALE; MESENCEPHALON; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; UPREGULATION; ANIMAL; CYTOLOGY; DOPAMINERGIC NERVE CELL; DRUG EFFECTS; INFLAMMATION; KNOCKOUT MOUSE; METABOLISM; NERVE DEGENERATION; PARKINSON DISEASE; PATHOLOGY; THEORETICAL MODEL;

ANIMALS; DOPAMINERGIC NEURONS; INFLAMMATION; LIPOPOLYSACCHARIDES; MESENCEPHALON; MICE, KNOCKOUT; MICROGLIA; MODELS, THEORETICAL; NERVE DEGENERATION; PARKINSON DISEASE; PROTEIN KINASE C-DELTA; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; UP-REGULATION;

EID: 84968813298     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2016.04.008     Document Type: Article

References (102)

1. Almodovar A.J., et al. Genomic structure and genetic drift in C57BL/6 congenic metabolic mutant mice. Mol. Genet. Metab. 2013, 110:396-400.
2. Anantharam V., et al. Caspase-3-dependent proteolytic cleavage of protein kinase Cdelta is essential for oxidative stress-mediated dopaminergic cell death after exposure to methylcyclopentadienyl manganese tricarbonyl. J. Neurosci. 2002, 22:1738-1751.
3. Appel S.H., et al. T cell-microglial dialogue in Parkinson's disease and amyotrophic lateral sclerosis: are we listening?. Trends Immunol. 2010, 31:7-17.
4. Ay M., et al. Molecular cloning, epigenetic regulation, and functional characterization of Prkd1 gene promoter in dopaminergic cell culture models of Parkinson's disease. J. Neurochem. 2015, 135:402-415.
5. Beitz J.M. Parkinson's disease: a review. Front. Biosci. (Schol. Ed.) 2014, 6:65-74.
6. Benner E.J., et al. Therapeutic immunization protects dopaminergic neurons in a mouse model of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9435-9440.
7. Bey E.A., et al. Protein kinase C delta is required for p47phox phosphorylation and translocation in activated human monocytes. J. Immunol. 2004, 173:5730-5738.
8. Bhatt K.H., et al. Protein kinase Cdelta and protein tyrosine kinase regulate peptidoglycan-induced nuclear factor-kappaB activation and inducible nitric oxide synthase expression in mouse peritoneal macrophages in vitro. Mol. Immunol. 2010, 47:861-870.
9. Bijlsma R., et al. Genetic and environmental stress, and the persistence of populations. EXS 1997, 83:193-207.
10. Block M.L., et al. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 2007, 8:57-69.
11. Bohnen N.I., et al. Extra-nigral pathological conditions are common in Parkinson's disease with freezing of gait: an in vivo positron emission tomography study. Mov. Disord. 2014, 29:1118-1124.
12. Boza-Serrano A., et al. The role of Galectin-3 in alpha-synuclein-induced microglial activation. Acta Neuropathol. Commun. 2014, 2:156.
13. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
14. Brochard V., et al. Infiltration of CD4+ lymphocytes into the brain contributes to neurodegeneration in a mouse model of Parkinson disease. J. Clin. Invest. 2009, 119:182-192.
15. Brown G.C., Neher J.J. Microglial phagocytosis of live neurons. Nat. Rev. Neurosci. 2014, 15:209-216.
16. Brown D.T., et al. Random genetic drift determines the level of mutant mtDNA in human primary oocytes. Am. J. Hum. Genet. 2001, 68:533-536.
17. Burguillos M.A., et al. Caspase signalling controls microglia activation and neurotoxicity. Nature 2011, 472:319-324.
18. Carpenter A.C., Alexander J.S. Endothelial PKC delta activation attenuates neutrophil transendothelial migration. Inflamm. Res. 2008, 57:216-229.
19. Czlonkowska A., et al. Microglial reaction in MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) induced Parkinson's disease mice model. Neurodegeneration 1996, 5:137-143.
20. Das K.C., et al. Thiol modulation of TNF alpha and IL-1 induced MnSOD gene expression and activation of NF-kappa B. Mol. Cell. Biochem. 1995, 148:45-57.
21. Deb D.K., et al. Activation of protein kinase C delta by IFN-gamma. J. Immunol. 2003, 171:267-273.
22. Du Y., et al. Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:14669-14674.
23. Fellner L., et al. Toll-like receptor 4 is required for alpha-synuclein dependent activation of microglia and astroglia. Glia 2013, 61:349-360.
24. Fontayne A., et al. Phosphorylation of p47phox sites by PKC alpha, beta II, delta, and zeta: effect on binding to p22phox and on NADPH oxidase activation. Biochemistry 2002, 41:7743-7750.
25. Furuya T., et al. Caspase-11 mediates inflammatory dopaminergic cell death in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson's disease. J. Neurosci. 2004, 24:1865-1872.
26. Ghosh A., et al. Selective inhibition of NF-kappaB activation prevents dopaminergic neuronal loss in a mouse model of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:18754-18759.
27. Ghosh A., et al. Selective inhibition of NF-kappaB activation prevents dopaminergic neuronal loss in a mouse model of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:18754-18759.
28. Ghosh A., et al. Neuroprotection by a mitochondria-targeted drug in a Parkinson's disease model. Free Radic. Biol. Med. 2010, 49:1674-1684.
29. Ghosh A., et al. The peptidyl-prolyl isomerase Pin1 up-regulation and proapoptotic function in dopaminergic neurons: relevance to the pathogenesis of Parkinson disease. J. Biol. Chem. 2013, 288:21955-21971.
30. Ginnan R., et al. PKC-delta mediates activation of ERK1/2 and induction of iNOS by IL-1beta in vascular smooth muscle cells. Am. J. Phys. Cell Physiol. 2006, 290:C1583-C1591.
31. Glass C.K., et al. Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140:918-934.
32. Gomel R., et al. The localization of protein kinase Cdelta in different subcellular sites affects its proapoptotic and antiapoptotic functions and the activation of distinct downstream signaling pathways. Mol. Cancer Res. 2007, 5:627-639.
33. Gordon R., et al. A simple magnetic separation method for high-yield isolation of pure primary microglia. J. Neurosci. Methods 2011, 194:287-296.
34. Gordon R., et al. Proteolytic activation of proapoptotic kinase protein kinase Cdelta by tumor necrosis factor alpha death receptor signaling in dopaminergic neurons during neuroinflammation. J. Neuroinflammation 2012, 9:82.
35. Hanrott K., et al. Differential activation of PKC delta in the substantia nigra of rats following striatal or nigral 6-hydroxydopamine lesions. Eur. J. Neurosci. 2008, 27:1086-1096.
36. Harischandra D.S., et al. Role of proteolytic activation of protein kinase Cdelta in the pathogenesis of prion disease. Prion. 2014, 8:143-153.
37. Harischandra D.S., et al. alpha-Synuclein protects against manganese neurotoxic insult during the early stages of exposure in a dopaminergic cell model of Parkinson's disease. Toxicol. Sci. 2015, 143:454-468.
38. Hayden M.S., Ghosh S. Signaling to NF-kappaB. Genes Dev. 2004, 18:2195-2224.
39. Hirsch E.C., Hunot S. Neuroinflammation in Parkinson's disease: a target for neuroprotection?. Lancet Neurol. 2009, 8:382-397.
40. Hirsch E.C., et al. Neuroinflammation in Parkinson's disease. Parkinsonism Relat. Disord. 2012, 18(Suppl. 1):S210-S212.
41. Hirsch E.C., et al. Pathogenesis of Parkinson's disease. Mov. Disord. 2013, 28:24-30.
42. Hu X., et al. Macrophage antigen complex-1 mediates reactive microgliosis and progressive dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. J. Immunol. 2008, 181:7194-7204.
43. Humphries M.J., et al. Tyrosine phosphorylation regulates nuclear translocation of PKCdelta. Oncogene 2008, 27:3045-3053.
44. Hunot S., et al. Nuclear translocation of NF-kappaB is increased in dopaminergic neurons of patients with parkinson disease. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:7531-7536.
45. Hunter R.L., et al. Inflammation induces mitochondrial dysfunction and dopaminergic neurodegeneration in the nigrostriatal system. J. Neurochem. 2007, 100:1375-1386.
46. Inoguchi T., et al. Protein kinase C-dependent increase in reactive oxygen species (ROS) production in vascular tissues of diabetes: role of vascular NAD(P)H oxidase. J. Am. Soc. Nephrol. 2003, 14:S227-S232.
47. Jin H., et al. alpha-Synuclein negatively regulates protein kinase Cdelta expression to suppress apoptosis in dopaminergic neurons by reducing p300 histone acetyltransferase activity. J. Neurosci. 2011, 31:2035-2051.
48. Jin H., et al. Histone hyperacetylation up-regulates protein kinase Cdelta in dopaminergic neurons to induce cell death: relevance to epigenetic mechanisms of neurodegeneration in Parkinson disease. J. Biol. Chem. 2014, 289:34743-34767.
49. Jin H., et al. Targeted toxicants to dopaminergic neuronal cell death. Methods Mol. Biol. 2015, 1254:239-252.
50. Jongeneel C.V. Transcriptional regulation of the tumor necrosis factor alpha gene. Immunobiology 1995, 193:210-216.
51. Kanthasamy A.G., et al. Role of proteolytic activation of protein kinase Cdelta in oxidative stress-induced apoptosis. Antioxid. Redox Signal. 2003, 5:609-620.
52. Kaul S., et al. Caspase-3 dependent proteolytic activation of protein kinase C delta mediates and regulates 1-methyl-4-phenylpyridinium (MPP+)-induced apoptotic cell death in dopaminergic cells: relevance to oxidative stress in dopaminergic degeneration. Eur. J. Neurosci. 2003, 18:1387-1401.
53. Kaul S., et al. Tyrosine phosphorylation regulates the proteolytic activation of protein kinase Cdelta in dopaminergic neuronal cells. J. Biol. Chem. 2005, 280:28721-28730.
54. Kawai T., Akira S. Signaling to NF-kappaB by Toll-like receptors. Trends Mol. Med. 2007, 13:460-469.
55. Khwaja A., Tatton L. Caspase-mediated proteolysis and activation of protein kinase Cdelta plays a central role in neutrophil apoptosis. Blood 1999, 94:291-301.
56. Kilpatrick L.E., et al. Regulation of TNF-induced oxygen radical production in human neutrophils: role of delta-PKC. J. Leukoc. Biol. 2010, 87:153-164.
57. Kim Y.S., et al. A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation. FASEB J. 2007, 21:179-187.
58. Kim S., et al. Role of protein kinase Cdelta in paraquat-induced glial cell death. J. Neurosci. Res. 2008, 86:2062-2070.
59. Kim C., et al. Neuron-released oligomeric alpha-synuclein is an endogenous agonist of TLR2 for paracrine activation of microglia. Nat. Commun. 2013, 4:1562.
60. Lee J.K., et al. Regulator of G-protein signaling 10 promotes dopaminergic neuron survival via regulation of the microglial inflammatory response. J. Neurosci. 2008, 28:8517-8528.
61. Lee E.J., et al. Alpha-synuclein activates microglia by inducing the expressions of matrix metalloproteinases and the subsequent activation of protease-activated receptor-1. J. Immunol. 2010, 185:615-623.
62. Lema Tome C.M., et al. Inflammation and alpha-synuclein's prion-like behavior in Parkinson's disease-is there a link?. Mol. Neurobiol. 2013, 47:561-574.
63. Liberatore G.T., et al. Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat. Med. 1999, 5:1403-1409.
64. Mecklenbrauker I., et al. Regulation of B-cell survival by BAFF-dependent PKCdelta-mediated nuclear signalling. Nature 2004, 431:456-461.
65. Miyamoto A., et al. Increased proliferation of B cells and auto-immunity in mice lacking protein kinase Cdelta. Nature 2002, 416:865-869.
66. Moore D.J., et al. Molecular pathophysiology of Parkinson's disease. Annu. Rev. Neurosci. 2005, 28:57-87.
67. Murakami M., Hirano T. The molecular mechanisms of chronic inflammation development. Front. Immunol. 2012, 3:323.
68. Napetschnig J., Wu H. Molecular basis of NF-kappaB signaling. Annu. Rev. Biophys. 2013, 42:443-468.
69. Newton A.C. Protein kinase C: structure, function, and regulation. J. Biol. Chem. 1995, 270:28495-28498.
70. Nitti M., et al. PKC delta and NADPH oxidase in AGE-induced neuronal death. Neurosci. Lett. 2007, 416:261-265.
71. Obeso J.A., et al. Missing pieces in the Parkinson's disease puzzle. Nat. Med. 2010, 16:653-661.
72. Panicker N., et al. Fyn kinase regulates microglial neuroinflammatory responses in cell culture and animal models of Parkinson's disease. J. Neurosci. 2015, 35:10058-10077.
73. Przedborski S., et al. MPTP as a mitochondrial neurotoxic model of Parkinson's disease. J. Bioenerg. Biomembr. 2004, 36:375-379.
74. Qian L., et al. Microglia-mediated neurotoxicity is inhibited by morphine through an opioid receptor-independent reduction of NADPH oxidase activity. J. Immunol. 2007, 179:1198-1209.
75. Qin L., et al. NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia. J. Biol. Chem. 2004, 279:1415-1421.
76. Qin L., et al. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 2007, 55:453-462.
77. Ren J., et al. Protein kinase C-delta (PKCdelta) regulates proinflammatory chemokine expression through cytosolic interaction with the NF-kappaB subunit p65 in vascular smooth muscle cells. J. Biol. Chem. 2014, 289:9013-9026.
78. Rocha N.P., et al. Insights into neuroinflammation in Parkinson's disease: from biomarkers to anti-inflammatory based therapies. Biomed Res Int. 2015, 2015:628192.
79. Sadasivan S., et al. Methylphenidate exposure induces dopamine neuron loss and activation of microglia in the basal ganglia of mice. PLoS One 2012, 7.
80. Saijo K., et al. A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 2009, 137:47-59.
81. Saminathan H., et al. Environmental neurotoxic pesticide dieldrin activates a non receptor tyrosine kinase to promote PKCdelta-mediated dopaminergic apoptosis in a dopaminergic neuronal cell model. Neurotoxicology 2011, 32:567-577.
82. Schapira A.H. Neurobiology and treatment of Parkinson's disease. Trends Pharmacol. Sci. 2009, 30:41-47.
83. St-Denis A., et al. Protein kinase C-alpha modulates lipopolysaccharide-induced functions in a murine macrophage cell line. J. Biol. Chem. 1998, 273:32787-32792.
84. Sun F., et al. Proteasome inhibitor-induced apoptosis is mediated by positive feedback amplification of PKCdelta proteolytic activation and mitochondrial translocation. J. Cell. Mol. Med. 2008, 12:2467-2481.
85. Swindell W.R., Bouzat J.L. Selection and inbreeding depression: effects of inbreeding rate and inbreeding environment. Evolution 2006, 60:1014-1022.
86. Takahashi K., et al. Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2. J. Exp. Med. 2005, 201:647-657.
87. Tansey M.G., Goldberg M.S. Neuroinflammation in Parkinson's disease: its role in neuronal death and implications for therapeutic intervention. Neurobiol. Dis. 2010, 37:510-518.
88. Tepperman B.L., et al. Protein kinase C mediates lipopolysaccharide- and phorbol-induced nitric-oxide synthase activity and cellular injury in the rat colon. J. Pharmacol. Exp. Ther. 2000, 295:1249-1257.
89. Urrutia P.J., et al. The interplay between iron accumulation, mitochondrial dysfunction, and inflammation during the execution step of neurodegenerative disorders. Front. Pharmacol. 2014, 5:38.
90. Valera E., Masliah E. Immunotherapy for neurodegenerative diseases: focus on alpha-synucleinopathies. Pharmacol. Ther. 2013, 138:311-322.
91. Vancurova I., et al. NF-kappa B activation in tumor necrosis factor alpha-stimulated neutrophils is mediated by protein kinase Cdelta. Correlation to nuclear Ikappa Balpha. J. Biol. Chem. 2001, 276:19746-19752.
92. Vignali D.A. Multiplexed particle-based flow cytometric assays. J. Immunol. Methods 2000, 243:243-255.
93. Volpicelli-Daley L.A., et al. Addition of exogenous alpha-synuclein preformed fibrils to primary neuronal cultures to seed recruitment of endogenous alpha-synuclein to Lewy body and Lewy neurite-like aggregates. Nat. Protoc. 2014, 9:2135-2146.
94. Wallerstedt E., et al. Protein kinase C-δ is involved in the inflammatory effect of IL-6 in mouse adipose cells. Diabetologia 2010, 53:946-954.
95. Wen J., et al. Specific PKC isoforms regulate LPS-stimulated iNOS induction in murine microglial cells. J. Neuroinflammation 2011, 8:38.
96. Wie S.M., et al. Inhibiting tyrosine phosphorylation of protein kinase Cdelta (PKCdelta) protects the salivary gland from radiation damage. J. Biol. Chem. 2014, 289:10900-10908.
97. Wu D.C., et al. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 2002, 22:1763-1771.
98. Wu D.C., et al. NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:6145-6150.
99. Yang T.T., et al. Differential distribution and activation of microglia in the brain of male C57BL/6J mice. Brain Struct. Funct. 2013, 218:1051-1060.
100. Zhang W., et al. Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson's disease. FASEB J. 2005, 19:533-542.
101. Zhang D., et al. Neuroprotective effect of protein kinase C delta inhibitor rottlerin in cell culture and animal models of Parkinson's disease. J. Pharmacol. Exp. Ther. 2007, 322:913-922.
102. Zhang D., et al. Protein kinase C delta negatively regulates tyrosine hydroxylase activity and dopamine synthesis by enhancing protein phosphatase-2A activity in dopaminergic neurons. J. Neurosci. 2007, 27:5349-5362.