A novel role of microglial NADPH oxidase in mediating extra-synaptic function of norepinephrine in regulating brain immune homeostasis

GLIA

Volumn 63, Issue 6, 2015, Pages 1057-1072

  Jiang, Lulu ^a,b   Chen, Shih Heng ^b   Chu, Chun Hsien ^b   Wang, Shi Jun ^b   Oyarzabal, Esteban ^b   Wilson, Belinda ^b   Sanders, Virginia ^c   Xie, Keqin ^a   Wang, Qingshan ^b   Hong, Jau Shyong ^b  

^a SHANDONG UNIVERSITY   (China)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

DSP 4; Extra synaptic; Neurodegeneration; Neurotransmitter; Volume transmission

Indexed keywords

2 BROMO N (2 CHLOROETHYL) N ETHYLBENZYLAMINE; ADRENERGIC RECEPTOR; BETA 2 ADRENERGIC RECEPTOR; LIPOPOLYSACCHARIDE; NORADRENALIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SUPEROXIDE; BENZYLAMINE DERIVATIVE; NEUROTRANSMITTER UPTAKE INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN IMMUNE HOMEOSTASIS; CELL CULTURE; CELL MEMBRANE; CELL SURVIVAL; CONTROLLED STUDY; DEGENERATIVE DISEASE; DOPAMINERGIC NERVE CELL; FEMALE; GLIA; HOMEOSTASIS; IN VIVO STUDY; MALE; MESENCEPHALON; MICROGLIA; MOUSE; NERVE CELL; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NEUROTOXICITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; STEREOCHEMISTRY; SUBSTANTIA NIGRA; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; CHLOROCEBUS AETHIOPS; COCULTURE; COS 1 CELL LINE; DRUG EFFECTS; ENZYMOLOGY; FISCHER 344 RAT; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; BENZYLAMINES; BRAIN; CELL LINE; CELL SURVIVAL; CERCOPITHECUS AETHIOPS; COCULTURE TECHNIQUES; COS CELLS; DOPAMINERGIC NEURONS; HOMEOSTASIS; LIPOPOLYSACCHARIDES; MALE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICROGLIA; NADPH OXIDASE; NEUROTRANSMITTER UPTAKE INHIBITORS; NOREPINEPHRINE; RATS, INBRED F344; RECEPTORS, ADRENERGIC, BETA-2;

EID: 84927961442     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22801     Document Type: Article

References (76)

1. Abercrombie ED, Zigmond MJ. 1989. Partial injury to central noradrenergic neurons: Reduction of tissue norepinephrine content is greater than reduction of extracellular norepinephrine measured by microdialysis. J Neurosci 9:4062-4067.
2. Alexander RW, Williams LT, Lefkowitz RJ. 1975. Identification of cardiac beta-adrenergic receptors by (minus) [3H]alprenolol binding. Proc Natl Acad Sci U.S.A 72:1564-1568.
3. Antelman SM, Caggiula AR. 1993. Norepinephrine-dopamine interactions: One step beyond. In: M Briley, M Marien, editors. Noradrenergic mechanisms in Parkinson's disease. Boca Raton: CRC Press. 127-139.
4. Baloyannis SJ, Costa V, Baloyannis IS. 2006. Morphological alterations of the synapses in the locus coeruleus in Parkinson's disease. J Neurol Sci 248:35-41.
5. Block ML, Hong JS. 2005. Microglia and inflammation-mediated neurodegeneration: Multiple triggers with a common mechanism. Prog Neurobiol 76:77-98.
6. Block ML, Zecca L, Hong JS. 2007. Microglia-mediated neurotoxicity: Uncovering the molecular mechanisms. Nature Rev Neurosci 8:57-69.
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. Bylund DB. 2007. Characterization of adrenoceptors. Curr Protoc Pharmacol 36:1.5: 1.5.1-1.5.18.
9. Bylund DB, Snyder SH. 1976. Beta adrenergic receptor binding in membrane preparations from mammalian brain. Mol Pharmacol 12:568-580.
10. Castaneda-Hernandez GC, Bach-y-Rita P. 2003. Volume transmission and pain perception. Sci World J 3:677-683.
11. Cheepsunthorn P, Radov L, Menzies S, Reid J, Connor JR. 2001. Characterization of a novel brain-derived microglial cell line isolated from neonatal rat brain. GLIA 35:53-62.
12. Chen SH, Oyarzabal EA, Hong JS. 2013. Preparation of rodent primary cultures for neuron-glia, mixed glia, enriched microglia, and reconstituted cultures with microglia. Methods Mol Biol 1041:231-240.
13. Collingridge GL, James TA, MacLeod NK. 1979. Neurochemical and electrophysiological evidence for a projection from the locus coeruleus to the substantia nigra [proceedings]. J Physiol 290:44P.
14. Cunningham C. 2013. Microglia and neurodegeneration: The role of systemic inflammation. GLIA 61:71-90.
15. Daw NW, Videen TO, Parkinson D, Rader RK. 1985. DSP-4 (N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine) depletes noradrenaline in kitten visual cortex without altering the effects of monocular deprivation. J Neurosci 5:1925-1933.
16. Dello Russo C, Boullerne AI, Gavrilyuk V, Feinstein DL. 2004. Inhibition of microglial inflammatory responses by norepinephrine: Effects on nitric oxide and interleukin-1 beta production. J Neuroinflammation 1:9.
17. Deupree JD, Kennedy RH. 1979. Stereospecific (--)-[3H]norepinephrine binding to bovine hypothalamus. Possible identification of the catecholamine uptake site in synaptic vesicles. Biochimi Biophysica Acta 582:470-485.
18. Farmer P, Pugin J. 2000. Beta-adrenergic agonists exert their "anti-inflammatory" effects in monocytic cells through the IkappaB/NF-kappaB pathway. Am J Physiol Lung Cell Mol Physiol 279:L675-L882.
19. Flierl MA, Rittirsch D, Nadeau BA, Sarma JV, Day DE, Lentsch AB, Huber-Lang MS, Ward PA. 2009. Upregulation of phagocyte-derived catecholamines augments the acute inflammatory response. PloS one 4:e4414.
20. Fornai F, Bassi L, Torracca MT, Alessandri MG, Scalori V, Corsini GU. 1996. Region- and neurotransmitter-dependent species and strain differences in DSP-4-induced monoamine depletion in rodents. Neurodegeneration 5:241-249.
21. Fritschy JM, Grzanna R. 1989. Immunohistochemical analysis of the neurotoxic effects of DSP-4 identifies two populations of noradrenergic axon terminals. Neuroscience 30:181-197.
22. Fuxe K, Borroto-Escuela DO, Romero-Fernandez W, Diaz-Cabiale Z, Rivera A, Ferraro L, Tanganelli S, Tarakanov AO, Garriga P, Narvaez JA, Cirula F, Guescini M, Agnati LF. 2012. Extrasynaptic neurotransmission in the modulation of brain function. Focus on the striatal neuronal-glial networks. Front Physiol 3:136.
23. Gao HM, Zhang F, Zhou H, Kam W, Wilson B, Hong JS. 2011a. Neuroinflammation and α-synuclein dysfunction potentiate each other, driving chronic progression of neurodegeneration in a mouse model of Parkinson's disease. Environ Health Perspect 119:807.
24. Gao HM, Hong JS, Zhang W, Liu B. 2002. Distinct role for microglia in rotenone-induced degeneration of dopaminergic neurons. J Neurosci 22:782-790.
25. Gendelman HE. 2002. Neural immunity: Friend or foe? J Neurovirol 8:474-479.
26. Gresch PJ, Sved AF, Zigmond MJ, Finlay JM. 1995. Local influence of endogenous norepinephrine on extracellular dopamine in rat medial prefrontal cortex. J Neurochem 65:111-116.
27. Heneka MT, Nadrigny F, Regen T, Martinez-Hernandez A, Dumitrescu-Ozimek L, Terwel D, Jardanhazi-Kurutz D, Walter J, Kirchhoff F, Hanisch UK Kummer MP. 2010. Locus ceruleus controls Alzheimer's disease pathology by modulating microglial functions through norepinephrine. Proc Natl Acad Sci U.S.A 107:6058-6063.
28. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S. 1998. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 57:1-9.
29. Jaim-Etcheverry G, Zieher LM. 1980. DSP-4: A novel compound with neurotoxic effects on noradrenergic neurons of adult and developing rats. Brain Res 188:513-523.
30. Jing FC, Chen H, Li CL. 2007. Rapid determination of dopamine and its metabolites during in vivo cerebral microdialysis by routine high performance liquid chromatography with electrochemical detection. Biomed Environ Sci 20:317-320.
31. Jones BE, Moore RY. 1977. Ascending projections of the locus coeruleus in the rat. II. Autoradiographic study. Brain Res 127:25-53.
32. Jonsson G, Hallman H, Ponzio F, Ross S. 1981. DSP4 (N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine)--a useful denervation tool for central and peripheral noradrenaline neurons. Eur J Pharmacol 72:173-188.
33. Kin NW, Sanders VM. 2006. It takes nerve to tell T and B cells what to do. J Leukoc Biol 79:1093-1104.
34. Kohm AP, Sanders VM. 2001. Norepinephrine and beta 2-adrenergic receptor stimulation regulate CD4+ T and B lymphocyte function in vitro and in vivo. Pharmacol Rev 53:487-525.
35. Koshkin V, Lotan O, Pick E. 1996. The cytosolic component p47(phox) is not a sine qua non participant in the activation of NADPH oxidase but is required for optimal superoxide production. J Biol Chem 271:30326-30329.
36. Liu B, Du L, Hong JS. 2000. Naloxone protects rat dopaminergic neurons against inflammatory damage through inhibition of microglia activation and superoxide generation. J Pharmacol Exp Ther 293:607-617.
37. Liu B, Hong JS. 2003. Primary rat mesencephalic neuron-glia, neuron-enriched, microglia-enriched, and astroglia-enriched cultures. Methods Mol Med 79:387-395.
38. Liu J, Mori A. 1993. Monoamine metabolism provides an antioxidant defense in the brain against oxidant- and free radical-induced damage. Arch Biochem Biophys 302:118-127.
39. Liu Y, Qin L, Wilson B, Wu X, Qian L, Granholm AC, Crews FT, Hong JS. 2008. Endotoxin induces a delayed loss of TH-IR neurons in substantia nigra and motor behavioral deficits. Neurotoxicology 29:864-870.
40. Mechawar N, Watkins KC, Descarries L. 2002. Ultrastructural features of the acetylcholine innervation in the developing parietal cortex of rat. J Comp Neurol 443:250-258.
41. Mizrahi A, Berdichevsky Y, Ugolev Y, Molshanski-Mor S, Nakash Y, Dahan I, Alloul N, Gorzalczany Y, Sarfstein R, Hirshberg M, Pick E. 2006. Assembly of the phagocyte NADPH oxidase complex: chimeric constructs derived from the cytosolic components as tools for exploring structure-function relationships. J Leukoc Biol 79:881-895.
42. Mori K, Ozaki E, Zhang B, Yang L, Yokoyama A, Takeda I, Maeda N, Sakanaka M, Tanaka J. 2002. Effects of norepinephrine on rat cultured microglial cells that express alpha1, alpha2, beta1 and beta2 adrenergic receptors. Neuropharmacology 43:1026-1034.
43. Mosley RL, Hutter-Saunders JA, Stone DK, Gendelman HE. 2012. Inflammation and adaptive immunity in Parkinson's disease. CSH Perspect Med 2:a009381.
44. Phani S, Loike JD, Przedborski S. 2012. Neurodegeneration and inflammation in Parkinson's disease. Parkinsonism Rel Disord 18 Suppl 1:S207-S209.
45. Qian L, Block ML, Wei SJ, Lin CF, Reece J, Pang H, Wilson B, Hong JS, Flood PM. 2006. Interleukin-10 protects lipopolysaccharide-induced neurotoxicity in primary midbrain cultures by inhibiting the function of NADPH oxidase. J Pharmacol Exp Ther 319:44-52.
46. Qian L, Wei SJ, Zhang D, Hu X, Xu Z, Wilson B, El-Benna J, Hong JS, Flood PM. 2008b. Potent anti-inflammatory and neuroprotective effects of TGF-beta1 are mediated through the inhibition of ERK and p47phox-Ser345 phosphorylation and translocation in microglia. J Immunol 181:660-668.
47. Qian L, Wu HM, Chen SH, Zhang D, Ali SF, Peterson L, Wilson B, Lu RB, Hong JS, Flood PM. 2011. Beta2-adrenergic receptor activation prevents rodent dopaminergic neurotoxicity by inhibiting microglia via a novel signaling pathway. J Immunol 186:4443-4454.
48. Qin L, Liu Y, Cooper C, Liu B, Wilson B, Hong JS. 2002. Microglia enhance beta-amyloid peptide-induced toxicity in cortical and mesencephalic neurons by producing reactive oxygen species. J Neurochem 83:973-983.
49. Qin L, Liu Y, Hong JS, Crews FT. 2013. NADPH oxidase and aging drive microglial activation, oxidative stress, and dopaminergic neurodegeneration following systemic LPS administration. Glia 61:855-868.
50. Qin L, Liu Y, Wang T, Wei SJ, Block ML, Wilson B, Liu B, Hong JS. 2004. NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia. J Biol Chem 279:1415-1421.
51. Qin L, Wu X, Block ML, Liu Y, Breese GR, Hong JS, Knapp DJ, Crews FT. 2007. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55:453-462.
52. Regan JW, Kobilka TS, Yang-Feng TL, Caron MG, Lefkowitz RJ, Kobilka BK. 1988. Cloning and expression of a human kidney cDNA for an alpha 2-adrenergic receptor subtype. Proc Natl Acad Sci U.S.A 85:6301-6305.
53. Robertson SD, Plummer NW, de Marchena J, Jensen P. 2013. Developmental origins of central norepinephrine neuron diversity. Nature Neurosci 16:1016-1023.
54. Robinson GB, Fluharty SJ, Zigmond MJ, Sclabassi RJ, Berger TW. 1993. Recovery of hippocampal dentate granule cell responsiveness to entorhinal cortical input following norepinephrine depletion. Brain Res 614:21-28.
55. Ross SB. 1976. Long-term effects of N-2-chlorethyl-N-ethyl-2-bromobenzylamine hydrochloride on noradrenergic neurones in the rat brain and heart. Br J Pharmacol 58:521-527.
56. Sanders VM. 1998. The role of norepinephrine and beta-2-adrenergic receptor stimulation in the modulation of Th1, Th2, and B lymphocyte function. Adv Exp Med Biology 437:269-278.
57. Sanders VM, Straub RH. 2002. Norepinephrine, the beta-adrenergic receptor, and immunity. Brain Behavi Immun 16:290-332.
58. Sara SJ. 2009. The locus coeruleus and noradrenergic modulation of cognition. Nature Rev Neurosci 10:211-223.
59. Schwinn DA, Lomasney JW, Lorenz W, Szklut PJ, Fremeau RT Jr, Yang-Feng TL, Caron MG, Lefkowitz RJ, Cotecchia S. 1990. Molecular cloning and expression of the cDNA for a novel alpha 1-adrenergic receptor subtype. J Biol Chem 265:8183-8189.
60. Severn A, Rapson NT, Hunter CA, Liew FY. 1992. Regulation of tumor necrosis factor production by adrenaline and beta-adrenergic agonists. J Immunol 148:3441-3445.
61. Strader CD, Sigal IS, Register RB, Candelore MR, Rands E, Dixon RA. 1987. Identification of residues required for ligand binding to the beta-adrenergic receptor. Proc Natl Acad Sci U.S.A 84:4384-4388.
62. Straub RH, Gunzler C, Miller LE, Cutolo M, Scholmerich J, Schill S. 2002. Anti-inflammatory cooperativity of corticosteroids and norepinephrine in rheumatoid arthritis synovial tissue in vivo and in vitro. FASEB I 16:993-1000.
63. Suh CI, Stull ND, Li XJ, Tian W, Price MO, Grinstein S, Yaffe MB, Atkinson S, Dinauer MC. 2006. The phosphoinositide-binding protein p40phox activates the NADPH oxidase during FcgammaIIA receptor-induced phagocytosis. J Exp Med 203:1915-1925.
64. Taylor CP. 1997. Mechanisms of action of gabapentin. Rev. Neurol 153 Suppl 1:S39-S45.
65. Troadec JD, Marien M, Darios F, Hartmann A, Ruberg M, Colpaert F, Michel PP. 2001. Noradrenaline provides long-term protection to dopaminergic neurons by reducing oxidative stress. J Neurochem 79:200-210.
66. Troadec JD, Marien M, Mourlevat S, Debeir T, Ruberg M, Colpaert F, Michel PP. 2002. Activation of the mitogen-activated protein kinase (ERK(1/2)) signaling pathway by cyclic AMP potentiates the neuroprotective effect of the neurotransmitter noradrenaline on dopaminergic neurons. Mol Pharmacol 62:1043-1052.
67. van der Poll T, Jansen J, Endert E, Sauerwein HP, van Deventer SJ. 1994. Noradrenaline inhibits lipopolysaccharide-induced tumor necrosis factor and interleukin 6 production in human whole blood. Infect Immun 62:2046-2050.
68. Vargova L, Sykova E. 2008. Extracellular space diffusion and extrasynaptic transmission. Physiol Res57 Suppl 3:S89-S99.
69. Wang Q, Chu CH, Oyarzabal E, Jiang L, Chen SH, Wilson B, Qian L, Hong JS. 2014a. Subpicomolar diphenyleneiodonium inhibits microglial NADPH oxidase with high specificity and shows great potential as a therapeutic agent for neurodegenerative diseases. Glia 62:2034-2043.
70. Wang Q, Chu CH, Qian L, Chen SH, Wilson B, Oyarzabal E, Jiang L, Ali S, Robinson B, Kim HC, Hong JS. 2014b. Substance P exacerbates dopaminergic neurodegeneration through neurokinin-1 receptor-independent activation of microglial NADPH oxidase. J Neurosci 34:12490-12503.
71. Wang Q, Shin EJ, Nguyen XK, Li Q, Bach JH, Bing G, Kim WK, Kim HC, Hong JS. 2012a. Endogenous dynorphin protects against neurotoxin-elicited nigrostriatal dopaminergic neuron damage and motor deficits in mice. J Neuroinflammation 9:124.
72. Wang Q, Zhou H, Gao H, Chen SH, Chu CH, Wilson B, Hong JS. 2012b. Naloxone inhibits immune cell function by suppressing superoxide production through a direct interaction with gp91phox subunit of NADPH oxidase. J Neuroinflammation 9:32.
73. Wang T, Qin L, Liu B, Liu Y, Wilson B, Eling TE, Langenbach R, Taniura S, Hong JS. 2004. Role of reactive oxygen species in LPS-induced production of prostaglandin E2 in microglia. J Neurochem 88:939-947.
74. Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, O'Donnell J, Christensen DJ, Nicholson C, Iliff JJ, Takano T, Deane R, Nedergaard M. 2013. Sleep drives metabolite clearance from the adult brain. Science 342:373-377.
75. Zamah AM, Delahunty M, Luttrell LM, Lefkowitz RJ. 2002. Protein kinase A-mediated phosphorylation of the beta 2-adrenergic receptor regulates its coupling to Gs and Gi. Demonstration in a reconstituted system. J Biol Chem 277:31249-31256.
76. Zarow C, Lyness SA, Mortimer JA, Chui HC. 2003. Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch Neurol 60:337-341.