Neuronal MCP-1 mediates microglia recruitment and neurodegeneration induced by the mild impairment of oxidative metabolism

Brain Pathology

Volumn 21, Issue 3, 2011, Pages 279-297

  Yang, Guang ^a   Meng, Ya ^a   Li, Wenxia ^a   Yong, Yue ^a   Fan, Zhiqin ^a   Ding, Hanqing ^a   Wei, Youzhen ^a   Luo, Jia ^a,b   Ke, Zun Ji ^a  

^a UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

chemokines; microglia activation; neurodegeneration; oxidative stress; thiamine deficiency

Indexed keywords

AMPROLIUM; ANTIOXIDANT; CD31 ANTIGEN; CD68 ANTIGEN; CELL MARKER; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1BETA; IONIZED CALCIUM BINDING ADAPTOR MOLECULE 1; LIPOCORTIN 5; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NEURON SPECIFIC NUCLEAR PROTEIN; NEUTRALIZING ANTIBODY; PYRITHIAMINE; RANTES; REACTIVE OXYGEN METABOLITE; THIAMINE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL SURVIVAL; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EMBRYO; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MALE; MICROGLIA; MOUSE; NERVE CELL CULTURE; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THALAMUS NUCLEUS; THALAMUS SUBMEDIAL NUCLEUS; THIAMINE DEFICIENCY;

ANIMALS; CELL DEATH; CHEMOKINE CCL2; CHEMOKINES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; NERVE DEGENERATION; NEURONS; OXIDATION-REDUCTION; POSTERIOR THALAMIC NUCLEI; REACTIVE OXYGEN SPECIES; THIAMINE DEFICIENCY;

EID: 79954615141     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/j.1750-3639.2010.00445.x     Document Type: Article

References (76)

1. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, et al, (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21: 383-421. (Pubitemid 30349107)
2. Allan SM, Rothwell NJ, (2001) Cytokines and acute neurodegeneration. Nat Rev Neurosci 2: 734-744. (Pubitemid 33674819)
3. Antony JM, van Marle G, Opii W, Butterfield DA, Mallet F, Yong VW, et al, (2004) Human endogenous retrovirus glycoprotein-mediated induction of redox reactants causes oligodendrocyte death and demyelination. Nat Neurosci 7: 1088-1095. (Pubitemid 41184449)
4. Banisadr G, Gosselin RD, Mechighel P, Kitabgi P, Rostene W, Parsadaniantz SM, (2005) Highly regionalized neuronal expression of monocyte chemoattractant protein-1 (MCP-1/CCL2) in rat brain: evidence for its colocalization with neurotransmitters and neuropeptides. J Comp Neurol 489: 275-292. (Pubitemid 41026230)
5. Benveniste EN, Nguyen VT, O'Keefe GM, (2001) Immunological aspects of microglia: relevance to Alzheimer's disease. Neurochem Int 39: 381-391. (Pubitemid 32907402)
6. Biber K, Neumann H, Inoue K, Boddeke HW, (2007) Neuronal "on" and "off" signals control microglia. Trends Neurosci 30: 596-602.
7. Bubber P, Ke ZJ, Gibson GE, (2004) Tricarboxylic acid cycle enzymes following thiamine deficiency. Neurochem Int 45: 1021-1028. (Pubitemid 39164927)
8. Butterworth RF, (2009) Thiamine deficiency-related brain dysfunction in chronic liver failure. Metab Brain Dis 24: 189-196.
9. Calingasan NY, Chun WJ, Park LC, Uchida K, Gibson GE, (1999) Oxidative stress is associated with region-specific neuronal death during thiamine deficiency. J Neuropathol Exp Neurol 58: 946-958. (Pubitemid 29441923)
10. Calingasan NY, Huang PL, Chun HS, Fabian A, Gibson GE, (2000) Vascular factors are critical in selective neuronal loss in an animal model of impaired oxidative metabolism. J Neuropathol Exp Neurol 59: 207-217. (Pubitemid 30143879)
11. Calingasan NY, Park LC, Calo LL, Trifiletti RR, Gandy SE, Gibson GE, (1998) Induction of nitric oxide synthase and microglial responses precede selective cell death induced by chronic impairment of oxidative metabolism. Am J Pathol 153: 599-610. (Pubitemid 28373670)
12. Cameron B, Landreth GE, (2010) Inflammation, microglia, and Alzheimer's disease. Neurobiol Dis 37: 503-509.
13. Chen YY, Chen G, Fan Z, Luo J, Ke ZJ, (2008) GSK3beta and endoplasmic reticulum stress mediate rotenone-induced death of SK-N-MC neuroblastoma cells. Biochem Pharmacol 76: 128-138.
14. D'Mello C, Le T, Swain MG, (2009) Cerebral microglia recruit monocytes into the brain in response to tumor necrosis factoralpha signaling during peripheral organ inflammation. J Neurosci 29: 2089-2102.
15. de Jong EK, Dijkstra IM, Hensens M, Brouwer N, van Amerongen M, Liem RS, et al, (2005) Vesicle-mediated transport and release of CCL21 in endangered neurons: a possible explanation for microglia activation remote from a primary lesion. J Neurosci 25: 7548-7557. (Pubitemid 41170612)
16. De Lella Ezcurra AL, Chertoff M, Ferrari C, Graciarena M, Pitossi F, (2010) Chronic expression of low levels of tumor necrosis factor-alpha in the substantia nigra elicits progressive neurodegeneration, delayed motor symptoms and microglia/macrophage activation. Neurobiol Dis 37: 630-640.
17. Deng YY, Lu J, Ling EA, Kaur C, (2009) Monocyte chemoattractant protein-1 (MCP-1) produced via NF-kappaB signaling pathway mediates migration of amoeboid microglia in the periventricular white matter in hypoxic neonatal rats. Glia 57: 604-621.
18. Fenoglio C, Galimberti D, Lovati C, Guidi I, Gatti A, Fogliarino S, et al, (2004) MCP-1 in Alzheimer's disease patients: A-2518G polymorphism and serum levels. Neurobiol Aging 25: 1169-1173. (Pubitemid 39094019)
19. Flugel A, Hager G, Horvat A, Spitzer C, Singer GM, Graeber MB, et al, (2001) Neuronal MCP-1 expression in response to remote nerve injury. J Cereb Blood Flow Metab 21: 69-76. (Pubitemid 32016841)
20. Frank-Cannon TC, Alto LT, McAlpine FE, Tansey MG, (2009) Does neuroinflammation fan the flame in neurodegenerative diseases? Mol Neurodegener 4: 47.
21. Frankin KBJ, Paxinos G, (2001) The Mouse Brain in Stereotaxic Coordinates, 2nd edn. Academic Press: San Diego, CA.
22. Fukui H, Moraes CT, (2008) The mitochondrial impairment, oxidative stress and neurodegeneration connection: reality or just an attractive hypothesis? Trends Neurosci 31: 251-256.
23. Gao YJ, Zhang L, Samad OA, Suter MR, Yasuhiko K, Xu ZZ, et al, (2009) JNK-induced MCP-1 production in spinal cord astrocytes contributes to central sensitization and neuropathic pain. J Neurosci 29: 4096-4108.
24. Gibson GE, Blass JP, (2007) Thiamine-dependent processes and treatment strategies in neurodegeneration. Antioxid Redox Signal 9: 1605-1619. (Pubitemid 47462965)
25. Gibson GE, Huang HM, (2004) Mitochondrial enzymes and endoplasmic reticulum calcium stores as targets of oxidative stress in neurodegenerative diseases. J Bioenerg Biomembr 36: 335-340. (Pubitemid 39619837)
26. Hazell AS, Butterworth RF, (2009) Update of cell damage mechanisms in thiamine deficiency: focus on oxidative stress, excitotoxicity and inflammation. Alcohol Alcohol 44: 141-147.
27. Hickman SE, Allison EK, El Khoury J, (2008) Microglial dysfunction and defective beta-amyloid clearance pathways in aging Alzheimer's disease mice. J Neurosci 28: 8354-8360.
28. Jiang W, Desjardins P, Butterworth RF, (2009) Cerebral inflammation contributes to encephalopathy and brain edema in acute liver failure: protective effect of minocycline. J Neurochem 109: 485-493.
29. Jiang W, Desjardins P, Butterworth RF, (2009) Direct evidence for central proinflammatory mechanisms in rats with experimental acute liver failure: protective effect of hypothermia. J Cereb Blood Flow Metab 29: 944-952.
30. Jung H, Toth PT, White FA, Miller RJ, (2008) Monocyte chemoattractant protein-1 functions as a neuromodulator in dorsal root ganglia neurons. J Neurochem 104: 254-263. (Pubitemid 350265055)
31. Karuppagounder SS, Shi Q, Xu H, Gibson GE, (2007) Changes in inflammatory processes associated with selective vulnerability following mild impairment of oxidative metabolism. Neurobiol Dis 26: 353-362. (Pubitemid 46561338)
32. Kauppinen TM, Higashi Y, Suh SW, Escartin C, Nagasawa K, Swanson RA, (2008) Zinc triggers microglial activation. J Neurosci 28: 5827-5835.
33. Ke ZJ, Calingasan NY, DeGiorgio LA, Volpe BT, Gibson GE, (2005) CD40-CD40L interactions promote neuronal death in a model of neurodegeneration due to mild impairment of oxidative metabolism. Neurochem Int 47: 204-215. (Pubitemid 40848683)
34. Ke ZJ, Calingasan NY, Karuppagounder SS, DeGiorgio LA, Volpe BT, Gibson GE, (2005) CD40L deletion delays neuronal death in a model of neurodegeneration due to mild impairment of oxidative metabolism. J Neuroimmunol 164: 85-92. (Pubitemid 40826765)
35. Ke ZJ, DeGiorgio LA, Volpe BT, Gibson GE, (2003) Reversal of thiamine deficiency-induced neurodegeneration. J Neuropathol Exp Neurol 62: 195-207. (Pubitemid 36176954)
36. Ke ZJ, Gibson GE, (2004) Selective response of various brain cell types during neurodegeneration induced by mild impairment of oxidative metabolism. Neurochem Int 45: 361-369. (Pubitemid 38625626)
37. Khoury JE, Luster AD, (2008) Mechanisms of microglia accumulation in Alzheimer's disease: therapeutic implications. Trends Pharmacol Sci 29: 626-632.
38. Koistinaho M, Koistinaho J, (2005) Interactions between Alzheimer's disease and cerebral ischemia-focus on inflammation. Brain Res 48: 240-250. (Pubitemid 40585755)
39. Landreth GE, (2009) Microglia in central nervous system diseases. J Neuroimmune Pharmacol 4: 369-370.
40. Lee JK, Tran T, Tansey MG, (2009) Neuroinflammation in Parkinson's disease. J Neuroimmune Pharmacol 4: 419-429.
41. Lu B, Rutledge BJ, Gu L, Fiorillo J, Lukacs NW, Kunkel SL, et al, (1998) Abnormalities in monocyte recruitment and cytokine expression in monocyte chemoattractant protein 1-deficient mice. J Exp Med 187: 601-608. (Pubitemid 28093362)
42. Ludwig J, Binder A, Steinmann J, Wasner G, Baron R, (2008) Cytokine expression in serum and cerebrospinal fluid in non-inflammatory polyneuropathies. J Neurol Neurosurg Psychiatry 79: 1268-1273.
43. Luo J, Lindstrom CL, Donahue A, Miller MW, (2001) Differential effects of ethanol on the expression of cyclo-oxygenase in cultured cortical astrocytes and neurons. J Neurochem 76: 1354-1363. (Pubitemid 32198240)
44. Mahad DJ, Ransohoff RM, (2003) The role of MCP-1 (CCL2) and CCR2 in multiple sclerosis and experimental autoimmune encephalomyelitis (EAE). Semin Immunol 15: 23-32. (Pubitemid 36092176)
45. McGeer PL, McGeer E, (2004) Immunotherapy for Alzheimer's disease. Sci Aging Knowledge Environ 2004: pe29.
46. Mhatre M, Floyd RA, Hensley K, (2004) Oxidative stress and neuroinflammation in Alzheimer's disease and amyotrophic lateral sclerosis: common links and potential therapeutic targets. J Alzheimers Dis 6: 147-157. (Pubitemid 38560250)
47. Muessel MJ, Berman NE, Klein RM, (2000) Early and specific expression of monocyte chemoattractant protein-1 in the thalamus induced by cortical injury. Brain Res 870: 211-221. (Pubitemid 30408423)
48. Nakazawa T, Hisatomi T, Nakazawa C, Noda K, Maruyama K, She H, et al, (2007) Monocyte chemoattractant protein 1 mediates retinal detachment-induced photoreceptor apoptosis. Proc National Acad Sci U S A 104: 2425-2430. (Pubitemid 46391413)
49. Nishimura M, Kuno S, Mizuta I, Ohta M, Maruyama H, Kaji R, Kawakami H, (2003) Influence of monocyte chemoattractant protein 1 gene polymorphism on age at onset of sporadic Parkinson's disease. Mov Disord 18: 953-955. (Pubitemid 37021174)
50. Orr CF, Rowe DB, Halliday GM, (2002) An inflammatory review of Parkinson's disease. Prog Neurobiol 68: 325-340. (Pubitemid 36071510)
51. Park LC, Zhang H, Gibson GE, (2001) Co-culture with astrocytes or microglia protects metabolically impaired neurons. Mech Ageing Dev 123: 21-27. (Pubitemid 32972255)
52. Puntambekar S, Doose J, Carson M, (2008) Central nervous system diseases and inflammation. In: Microglia: A CNS-Specific Tissue Macrophage, Chapter 1., Lane, Th.E., Carson, M., Bergmann, C., Wyss-Coray, T, (ed.), pp. 1-12. Springer: New York.
53. Ransohoff RM, Hamilton TA, Tani M, Stoler MH, Shick HE, Major JA, et al, (1993) Astrocyte expression of mRNA encoding cytokines IP-10 and JE/MCP-1 in experimental autoimmune encephalomyelitis. FASEB J 7: 592-600. (Pubitemid 23120908)
54. Rappert A, Bechmann I, Pivneva T, Mahlo J, Biber K, Nolte C, et al, (2004) CXCR3-dependent microglial recruitment is essential for dendrite loss after brain lesion. J Neurosci 24: 8500-8509. (Pubitemid 39313773)
55. Rojo AI, Innamorato NG, Martin-Moreno AM, De Ceballos ML, Yamamoto M, Cuadrado A, (2010) Nrf2 regulates microglial dynamics and neuroinflammation in experimental Parkinson's disease. Glia 58: 588-598.
56. Rostene W, Kitabgi P, Parsadaniantz SM, (2007) Chemokines: a new class of neuromodulator? Nat Rev 8: 895-903.
57. Shaftel SS, Carlson TJ, Olschowka JA, Kyrkanides S, Matousek SB, O'Banion MK, (2007) Chronic interleukin-1beta expression in mouse brain leads to leukocyte infiltration and neutrophil-independent blood brain barrier permeability without overt neurodegeneration. J Neurosci 27: 9301-9309. (Pubitemid 47358197)
58. Shi Q, Karuppagounder SS, Xu H, Pechman D, Chen H, Gibson GE, (2007) Responses of the mitochondrial alpha-ketoglutarate dehydrogenase complex to thiamine deficiency may contribute to regional selective vulnerability. Neurochem Int 50: 921-931. (Pubitemid 46962817)
59. Tansey MG, Wyss-Coray T, (2008) Cytokines in CNS Inflammation and Disease. In: Central nervous system diseases and inflammation., Lane, Th.E., Carson, M., Bergmann, C., Wyss-Coray, T, (ed.), pp. 59-106. Springer: New York.
60. Tanuma N, Sakuma H, Sasaki A, Matsumoto Y, (2006) Chemokine expression by astrocytes plays a role in microglia/macrophage activation and subsequent neurodegeneration in secondary progressive multiple sclerosis. Acta Neuropathol 112: 195-204.
61. Thacker MA, Clark AK, Bishop T, Grist J, Yip PK, Moon LD, et al, (2009) CCL2 is a key mediator of microglia activation in neuropathic pain states. Eur J Pain 13: 263-272.
62. Todd KG, Butterworth RF, (1999) Early microglial response in experimental thiamine deficiency: an immunohistochemical analysis. Glia 25: 190-198. (Pubitemid 29032774)
63. Van Der Voorn P, Tekstra J, Beelen RH, Tensen CP, Van Der Valk P, De Groot CJ, (1999) Expression of MCP-1 by reactive astrocytes in demyelinating multiple sclerosis lesions. Am J Pathol 154: 45-51. (Pubitemid 29031610)
64. Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA, (2005) Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 57: 67-81. (Pubitemid 40053317)
65. Viola A, Luster AD, (2008) Chemokines and their receptors: drug targets in immunity and inflammation. Ann Rev Pharmacol Toxicol 48: 171-197. (Pubitemid 351756361)
66. Voskuhl RR, Peterson RS, Song B, Ao Y, Morales LB, Tiwari-Woodruff S, Sofroniew MV, (2009) Reactive astrocytes form scar-like perivascular barriers to leukocytes during adaptive immune inflammation of the CNS. J Neurosci 29: 11511-11522.
67. Wang HK, Park UJ, Kim SY, Lee JH, Kim SU, Gwag BJ, Lee YB, (2008) Free radical production in CA1 neurons induces MIP-1alpha expression, microglia recruitment, and delayed neuronal death after transient forebrain ischemia. J Neurosci 28: 1721-1727. (Pubitemid 351287047)
68. Wang JY, Wen LL, Huang YN, Chen YT, Ku MC, (2006) Dual effects of antioxidants in neurodegeneration: direct neuroprotection against oxidative stress and indirect protection via suppression of glia-mediated inflammation. Curr Pharm Des 12: 3521-3533.
69. Wang X, Fan Z, Wang B, Luo J, Ke ZJ, (2007) Activation of double-stranded RNA-activated protein kinase by mild impairment of oxidative metabolism in neurons. J Neurochem 103: 2380-2390. (Pubitemid 350173586)
70. Wang X, Wang B, Fan Z, Shi X, Ke ZJ, Luo J, (2007) Thiamine deficiency induces endoplasmic reticulum stress in neurons. Neuroscience 144: 1045-1056. (Pubitemid 46013979)
71. Xia Z, Dudek H, Miranti CK, Greenberg ME, (1996) Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J Neurosci 16: 5425-5436. (Pubitemid 26277871)
72. Yamashita N, Hoshida S, Otsu K, Taniguchi N, Kuzuya T, Hori M, (2000) The involvement of cytokines in the second window of ischaemic preconditioning. Br J Pharmacol 131: 415-422.
73. Zhang J, Shi XQ, Echeverry S, Mogil JS, De Koninck Y, Rivest S, (2007) Expression of CCR2 in both resident and bone marrow-derived microglia plays a critical role in neuropathic pain. J Neurosci 27: 12396-12406. (Pubitemid 350085465)
74. Zhang Q, Ding H, Li W, Fan Z, Sun A, Luo J, Ke ZJ, (2009) Senescence accelerated mouse strain is sensitive to neurodegeneration induced by mild impairment of oxidative metabolism. Brain Res 1264: 111-118.
75. Zhang Q, Yang G, Li W, Fan Z, Sun A, Luo J, Ke ZJ, (2009) Thiamine deficiency increases beta-secretase activity and accumulation of beta-amyloid peptides. Neurobiol Aging; doi:10.1016/j.neurobiolaging.2009.01.005 [Epub ahead of print].
76. Zhao F, Cai T, Liu M, Zheng G, Luo W, Chen J, (2009) Manganese induces dopaminergic neurodegeneration via microglial activation in a rat model of manganism. Toxicol Sci 107: 156-164.