Inflammatory effects of highly pathogenic H5N1 influenza virus infection in the CNS of mice

Journal of Neuroscience

Volumn 32, Issue 5, 2012, Pages 1545-1559

  Jang, Haeman ^a   Boltz, David ^a   McClaren, Jennifer ^a   Pani, Amar K ^a   Smeyne, Michelle ^a   Korff, Ane ^a   Webster, Robert ^a   Smeyne, Richard Jay ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYINDOLEACETIC ACID; COLONY STIMULATING FACTOR 1; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; DIHYDROXYPHENYLACETIC ACID; DOPAMINE; EOTAXIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HOMOVANILLIC ACID; INDOLEAMINE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; INTERLEUKIN 9; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; NORADRENALIN; RANTES; SEROTONIN; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN STEM; CELL COUNT; CELL LOSS; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; FEMALE; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; INFLAMMATION; INFLUENZA A (H5N1); MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SUBSTANTIA NIGRA; SUBSTANTIA NIGRA PARS COMPACTA;

ANIMALS; BRAIN; CENTRAL NERVOUS SYSTEM VIRAL DISEASES; CHICK EMBRYO; FEMALE; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA, HUMAN; MICE; MICE, INBRED C57BL;

EID: 84856637001     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5123-11.2012     Document Type: Article

References (76)

1. Appel SH, Beers DR, Henkel JS (2010) T cell-microglial dialogue in Parkinson's disease and amyotrophic lateral sclerosis: are we listening? Trends Immunol 31:7-17.
2. Baquet ZC, Williams D, Brody J, Smeyne RJ (2009) A comparison of modelbased (2D) and design-based (3D) stereological methods for estimating cell number in the substantia nigra pars compacta (SNpc) of the C57BL/6J Mouse. Neuroscience 161:1082-1090.
3. Bazzu G, Calia G, Puggioni G, Spissu Y, Rocchitta G, Debetto P, Grigoletto J, Zusso M, Migheli R, Serra PA, Desole MS, Miele E (2010) alpha- Synuclein- and MPTP-generated rodent models of Parkinson's disease and the study of extracellular striatal dopamine dynamics: a microdialysis approach. CNS Neurol Disord Drug Targets 9:482-490.
4. Boyd JD, Jang H, Shepherd KR, Faherty C, Slack S, Jiao Y, Smeyne RJ (2007) Response to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) differs in mouse strains and reveals a divergence in JNK signaling and COX-2 induction before loss of neurons in the substantia nigra pars compacta. Brain Res 1175:107-116.
5. Carr MW, Roth SJ, Luther E, Rose SS, Springer TA (1994) Monocyte chemoattractant protein 1 acts as a T-lymphocyte chemoattractant. Proc Natl Acad Sci U S A 91:3652-3656.
6. Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron 39:889-909.
7. de Jong MD (2008) H5N1 transmission and disease: observations from the frontlines. Pediatr Infect Dis J 27:S54-56.
8. Dickman MS (2001) von Economo encephalitis. Arch Neurol 58:1696-1698.
9. Dufour JH, Dziejman M, Liu MT, Leung JH, Lane TE, Luster AD (2002) IFN-gamma-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. J Immunol 168:3195-3204.
10. Dybing JK, Schultz-Cherry S, Swayne DE, Suarez DL, Perdue ML (2000) Distinct pathogenesis of Hong Kong-origin H5N1 viruses in mice compared with that of other highly pathogenic H5 avian influenza viruses. J Virol 74:1443-1450.
11. Faherty CJ, Xanthoudakis S, Smeyne RJ (1999) Caspase-3-dependent neuronal death in the hippocampus following kainic acid treatment. Brain Res Mol Brain Res 70:159-163.
12. Fernandez EJ, Lolis E (2002) Structure, function, and inhibition of chemokines. Annu Rev Pharmacol Toxicol 42:469-499.
13. Gao HM, Kotzbauer PT, Uryu K, Leight S, Trojanowski JQ, Lee VM (2008) Neuroinflammation and oxidation/nitration ofα-synuclein linked to dopaminergic neurodegeneration. J Neurosci 28:7687-7698.
14. Gehrmann J, Banati RB, Kreutzberg GW (1993) Microglia in the immune surveillance of the brain: human microglia constitutively express HLA-DR molecules. J Neuroimmunol 48:189-198.
15. Ghoshal A, Das S, Ghosh S, Mishra MK, Sharma V, Koli P, Sen E, Basu A (2007) Proinflammatory mediators released by activated microglia induces neuronal death in Japanese encephalitis. Glia 55:483-496.
16. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH (2010) Mechanisms underlying inflammation in neurodegeneration. Cell 140:918-934.
17. Gonçalves J, Baptista S, Martins T, Milhazes N, Borges F, Ribeiro CF, Malva JO, Silva AP (2010) Methamphetamine-induced neuroinflammation and neuronal dysfunction in the mice hippocampus: preventive effect of indomethacin. Eur J Neurosci 31:315-326.
18. Graeber MB, Streit WJ (2010) Microglia: biology and pathology. Acta Neuropathol 119:89-105.
19. Harry GJ, Kraft AD (2008) Neuroinflammation and microglia: considerations and approaches for neurotoxicity assessment. Expert Opin Drug Metab Toxicol 4:1265-1277.
20. Hayase Y, Tobita K (1997) Influenza virus and neurological diseases. Psychiatry Clin Neurosci 51:181-184.
21. Hayashi M, Luo Y, Laning J, Strieter RM, Dorf ME (1995) Production and function of monocyte chemoattractant protein-1 and other betachemokines in murine glial cells. J Neuroimmunol 60:143-150.
22. Hickey WF, Kimura H (1988) Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 239:290-292.
23. Hirsch EC, Breidert T, Rousselet E, Hunot S, Hartmann A, Michel PP (2003) The role of glial reaction and inflammation in Parkinson's disease. Ann N Y Acad Sci 991:214-228.
24. Hu LF, Lu M, Tiong CX, Dawe GS, Hu G, Bian JS (2010) Neuroprotective effects of hydrogen sulfide on Parkinson's disease rat models. Aging Cell 9:135-146.
25. Hu X, Zhang D, Pang H, Caudle WM, Li Y, Gao H, Liu Y, Qian L, Wilson B, Di Monte DA, Ali SF, Zhang J, Block ML, Hong JS (2008) Macrophage antigen complex-1 mediates reactive microgliosis and progressive dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. J Immunol 181:7194-7204.
26. Jang H, Boltz DA, Webster RG, Smeyne RJ (2009a) Viral parkinsonism. Biochim Biophys Acta 1792:714-721.
27. Jang H, Boltz D, Sturm-Ramirez K, Shepherd KR, Jiao Y, Webster R, Smeyne RJ (2009b) Highly pathogenic H5N1 influenza virus can enter the CNS and induce neuroinflammation and neurodegeneration. Proc Natl Acad Sci U S A 106:14063-14068.
28. Jenner P (1998) Oxidative mechanisms in nigral cell death in Parkinson's disease. Mov Dis 13 [Suppl 1]:24-34.
29. Jensen P, Smeyne R, Goldowitz D (2004) Analysis of cerebellar development in math1 null embryos and chimeras. J Neurosci 24:2202-2211.
30. Kim YS, Joh TH (2006) Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease. Exp Mol Med 38:333-347.
31. Klopfleisch R, Werner O, Mundt E, Harder T, Teifke JP (2006) Neurotropism of highly pathogenic avian influenza virus A/chicken/Indonesia/ 2003 (H5N1) in experimentally infected pigeons (Columbia livia f. domestica). Vet Pathol 43:463-470.
32. Korteweg C, Gu J (2008) Pathology, molecular biology, and pathogenesis of avian influenza A (H5N1) infection in humans. Am J Pathol 172:1155-1170.
33. Kuhn DM, Francescutti-Verbeem DM, Thomas DM (2006) Dopamine quinones activate microglia and induce a neurotoxic gene expression profile: relationship to methamphetamine-induced nerve ending damage. Ann N Y Acad Sci 1074:31-41.
34. Liu M, Cai T, Zhao F, Zheng G, Wang Q, Chen Y, Huang C, Luo W, Chen J (2009) Effect of microglia activation on dopaminergic neuronal injury induced by manganese, and its possible mechanism. Neurotox Res 16:42-49.
35. Mastroeni D, Grover A, Leonard B, Joyce JN, Coleman PD, Kozik B, Bellinger DL, Rogers J (2009) Microglial responses to dopamine in a cell culture model of Parkinson's disease. Neurobiol Aging 30:1805-1817.
36. McKeller RN, Fowler JL, Cunningham JJ, Warner N, Smeyne RJ, Zindy F, Skapek SX (2002) The Arf tumor suppressor gene promotes hyaloid vascular regression during mouse eye development. Proc Natl Acad SciUSA 99:3848-3853.
37. Menninger KA (1926) Influenza and schizophrenia. An analysis of postinfluenzal "dementia precox" as of 1918 and five years later. Am J Psych 5:469-529.
38. Menten P, Wuyts A, Van Damme J (2002) Macrophage inflammatory protein-1. Cytokine Growth Factor Rev 13:455-481.
39. Metcalf D (1985) The granulocyte-macrophage colony-stimulating factors. Science 229:16-22.
40. Minghetti L, Ajmone-Cat MA, De Berardinis MA, De Simone R (2005) Microglial activation in chronic neurodegenerative diseases: roles of apoptotic neurons and chronic stimulation. Brain Res Brain Res Rev 48:251-256.
41. Nishimura H, Itamura S, Iwasaki T, Kurata T, Tashiro M (2000) Characterization of human influenza A (H5N1) virus infection in mice: neuro-, pneumo- and adipotropic infection. J Gen Virol 81:2503-2510.
42. Opal SM, DePalo VA (2000) Anti-inflammatory cytokines. Chest 117:1162-1172.
43. Parent M, Parent A (2010) Substantia nigra and Parkinson's disease: a brief history of their long and intimate relationship. Can J Neurol Sci 37:313-319.
44. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. San Diego: Academic.
45. Peng J, Stevenson FF, Oo ML, Andersen JK (2009) Iron-enhanced paraquatmediated dopaminergic cell death due to increased oxidative stress as a consequence of microglial activation. Free Radic Biol Med 46:312-320.
46. Perry VH, Newman TA, Cunningham C (2003) The impact of systemic infection on the progression of neurodegenerative disease. Nat Rev Neurosci 4:103-112.
47. Persidsky Y, Ghorpade A, Rasmussen J, Limoges J, Liu XJ, Stins M, Fiala M, Way D, Kim KS, Witte MH, Weinand M, Carhart L, Gendelman HE (1999) Microglial and astrocyte chemokines regulate monocyte migration through the blood-brain barrier in human immunodeficiency virus-1 encephalitis. Am J Pathol 155:1599-1611.
48. Raivich G (2005) Like cops on the beat: the active role of resting microglia. Trends Neurosci 28:571-573.
49. Ravenholt RT, Foege WH (1982) 1918 influenza, encephalitis lethargica, parkinsonism. Lancet 320:860-864.
50. Reed LJ, Muench H (1938) A simple method of estimating 50 per cent endpoints. Am J Hygiene 27:493-497.
51. Reynolds AD, Stone DK, Mosley RL, Gendelman HE (2009) Nitrated {alpha}-synuclein-induced alterations in microglial immunity are regulated by CD4+ T cell subsets. J Immunol 182:4137-4149.
52. Rigoni M, Shinya K, Toffan A, Milani A, Bettini F, Kawaoka Y, Cattoli G, Capua I (2007) Pneumo- and neurotropism of avian origin Italian highly pathogenic avian influenza H7N1 isolates in experimentally infected mice. Virology 364:28-35.
53. Rimmelzwaan GF, van Riel D, Baars M, Bestebroer TM, van Amerongen G, Fouchier RA, Osterhaus AD, Kuiken T (2006) Influenza A virus (H5N1) infection in cats causes systemic disease with potential novel routes of virus spread within and between hosts. Am J Pathol 168:176-183.
54. Robinson TE, Mocsary Z, Camp DM, Whishaw IQ (1994) Time course of recovery of extracellular dopamine following partial damage to the nigrostriatal dopamine system. J Neurosci 14:2687-2696.
55. Rojo AI, Innamorato NG, Martín-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. Sanchez-Guajardo V, Febbraro F, Kirik D, Romero-Ramos M (2010) Microglia acquire distinct activation profiles depending on the degree of alpha-synuclein neuropathology in a rAAV based model of Parkinson's disease. PLoS One 5:e8784.
57. Sejvar JJ, Uyeki TM (2010) Neurologic complications of 2009 influenza A (H1N1): heightened attention on an ongoing question. Neurology 74:1020-1021.
58. Simard AR, Rivest S (2004) Bone marrow stem cells have the ability to populate the entire CNS into fully differentiated parenchymal microglia. FASEB J 18:998-1000.
59. Smeyne M, Smeyne RJ (2002) Method for culturing postnatal substantia nigra as an in vitro model of experimental Parkinson's disease. Brain Res Brain Res Protoc 9:105-111.
60. Smeyne M, Boyd J, Raviie Shepherd K, Jiao Y, Pond BB, Hatler M, Wolf R, Henderson C, Smeyne RJ (2007) GSTpi expression mediates dopaminergic neuron sensitivity in experimental parkinsonism. Proc Natl Acad Sci U S A 104:1977-1982.
61. Smith DJ, Stevens ME, Sudanagunta SP, Bronson RT, Makhinson M, Watabe AM, O'Dell TJ, Fung J, Weier HU, Cheng JF, Rubin EM (1997) Functional screening of 2 Mb of human chromosome 21q22.2 in transgenic mice implicates minibrain in learning defects associated with Down syndrome. Nat Genet 16:28-36.
62. Smith TS, Parker WD Jr, Bennett JP Jr (1994) L-dopa increases nigral production of hydroxyl radicals in vivo: potential L-dopa toxicity? Neuroreport 5:1009-1011.
63. Su X, Maguire-Zeiss KA, Giuliano R, Prifti L, Venkatesh K, Federoff HJ (2008) Synuclein activates microglia in a model of Parkinson's disease. Neurobiol Aging 29:1690-1701.
64. Tanaka H, Park CH, Ninomiya A, Ozaki H, Takada A, Umemura T, Kida H (2003) Neurotropism of the 1997 Hong Kong H5N1 influenza virus in mice. Vet Microbiol 95:1-13.
65. Tansey MG, Goldberg MS (2010) Neuroinflammation in Parkinson's disease: its role in neuronal death and implications for therapeutic intervention. Neurobiol Dis 37:510-518.
66. Taubenberger JK, Morens DM (2006) 1918 Influenza: the mother of all pandemics. Emerg Infect Dis 12:15-22.
67. Tumpey TM, Basler CF, Aguilar PV, Zeng H, Solórzano A, Swayne DE, Cox NJ, Katz JM, Taubenberger JK, Palese P, García-Sastre A (2005) Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310:77-80.
68. von Economo K (1917) Encephalitis lethargica. Wiener Klinische Wochenschrift 30:581-585.
69. Wang G, Zhang J, Li W, Xin G, Su Y, Gao Y, Zhang H, Lin G, Jiao X, Li K (2008) Apoptosis and proinflammatory cytokine responses of primary mouse microglia and astrocytes induced by human H1N1 and avian H5N1 influenza viruses. Cell Mol Immunol 5:113-120.
70. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
71. Yao L, Korteweg C, Hsueh W, Gu J (2008) Avian influenza receptor expression in H5N1-infected and noninfected human tissues. FASEB J 22:733-740.
72. Yokota S, Imagawa T, Miyamae T, Ito S, Nakajima S, Nezu A, Mori M (2000) Hypothetical pathophysiology of acute encephalopathy and encephalitis related to influenza virus infection and hypothermia therapy. Pediatr Int 42:197-203.
73. Yokoyama H, Takagi S, Watanabe Y, Kato H, Araki T (2008) Role of reactive nitrogen and reactive oxygen species againstMPTPneurotoxicity in mice. J Neural Transm 115:831-842.
74. Yong VW, Marks S (2010) The interplay between the immune and central nervous systems in neuronal injury. Neurology 74 [Suppl 1]:9-16.
75. Yuen KY, Wong SS (2005) Human infection by avian influenza A H5N1. Hong Kong Med J 11:189-199.
76. Zhang W, Wang T, Pei Z, Miller DS, Wu X, Block ML, Wilson B, Zhang W, Zhou Y, Hong JS, Zhang J (2005) Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson's disease. FASEB J 19:533-542.