Targeting neuro-inflammatory cytokines and oxidative stress by minocycline attenuates quinolinic-acid-induced huntington's disease-like symptoms in rats

Neurotoxicity Research

Volumn 22, Issue 4, 2012, Pages 310-320

  Kalonia, Harikesh ^a   Mishra, Jitendriya ^a   Kumar, Anil ^a  

^a PANJAB UNIVERSITY   (India)

Author keywords

Minocycline; Neurotoxicity; Oxidative stress; Proinflammatory cytokines; Quinolinic acid

Indexed keywords

CATALASE; INTERLEUKIN 6; MINOCYCLINE; NITRITE; QUINOLINIC ACID; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; HUNTINGTON CHOREA; LIPID PEROXIDATION; LOCOMOTION; MALE; MORNING DOSAGE; MOTOR COORDINATION; MOTOR DYSFUNCTION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; ROTAROD TEST; WEIGHT REDUCTION;

ANALYSIS OF VARIANCE; ANIMALS; BODY WEIGHT; CATALASE; CYTOKINES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; HUNTINGTON DISEASE; LIPID PEROXIDATION; MALE; MINOCYCLINE; MOTOR ACTIVITY; NITRITES; OXIDATIVE STRESS; PSYCHOMOTOR PERFORMANCE; QUINOLINIC ACIDS; RATS; RATS, WISTAR; ROTAROD PERFORMANCE TEST; STATISTICS AS TOPIC; SUPEROXIDE DISMUTASE;

ANIMALIA; RATTUS;

EID: 84870297389     PISSN: 10298428     EISSN: 14763524     Source Type: Journal    
DOI: 10.1007/s12640-012-9315-x     Document Type: Article

References (82)

1. Amin AR, Attur MG, Thakker GD et al (1996) A novel mechanism of action of tetracyclines: effects on nitric oxide synthases. Proc Natl Acad Sci USA 93:14014-14019
2. Amori L, Wu HQ, Marinozzi M et al (2009) Specific inhibition of kynurenate synthesis enhances extracellular dopamine levels in the rodent striatum. Neuroscience 159:196-203
3. Appel SH (2009) CD4? T cells mediate cytotoxicity in neurodegenerative diseases. J Clin Invest 119:13-15
4. Beal MF (1995) Aging, energy and oxidative stress in neurodegenerative diseases. Ann Neurol 38:357-366
5. Beal MF (2000) Energetics in the pathogenesis of neurodegenerative diseases. Trends Neurosci 23:298-304
6. Beal MF, Kowall NW, Ellison DW et al (1986) Replication of the neurochemical characteristics of Huntington's disease by quinolinic acid. Nature 321:168-171
7. Bizat N, Hermel JM, Boyer F et al (2003) Calpain is a major cell death effector in selective striatal degeneration induced in vivo by 3-nitropropionate: implications for Huntington's disease. J Neurosci 23:5020-5030
8. Blum D, Hourez R, Galas MC et al (2003) Adenosine receptors and Huntington's disease: implications for pathogenesis and therapeutics. Lancet Neurol 2:366-374
9. Blum D, Chtarto A, Tenenbaum L et al (2004) Clinical potential of minocycline for neurodegenerative disorders. Neurobiol Dis 17:359-366
10. Braidy N, Grant R, Adams S et al (2009) Mechanism for quinolinic acid cytotoxicity in human astrocytes and neurons. Neurotox Res 16:77-86
11. Brouillet E, Conde F, Beal MF et al (1999) Replicating Huntington's disease phenotype in experimental animals. Prog Neurobiol 59:427-468
12. Browne SE, Beal MF (2002) Toxin-induced mitochondrial dysfunction. Int Rev Neurobiol 53:243-279
13. Cai ZY, Yan Y, Sun SQ et al (2008) Minocycline attenuates cognitive impairment and restrains oxidative stress in the hippocampus of rats with chronic cerebral hypoperfusion. Neurosci Bull 24: 305-313
14. Cai ZY, Yan Y, Chen R (2010) Minocycline reduces astrocytic reactivation and neuroinflammation in the hippocampus of a vascular cognitive impairment rat model. Neurosci Bull 26: 28-36
15. Cha JH (2000) Transcriptional dysregulation in Huntington's disease. Trends Neurosci 23:387-392
16. Chen M, Ona VO, Li M et al (2000) Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat Med 6:797-801
17. Chu LS, Fang SH, Zhou Y et al (2010) Minocycline inhibits 5-lipoxygenase expression and accelerates functional recovery in chronic phase of focal cerebral ischemia in rats. Life Sci 86:170-177
18. Diguet E, Fernagut PO, Wei X et al (2004) Deleterious effects of minocycline in animal models of Parkinson's disease and Huntington's disease. Eur J Neurosci 19:3266-3276
19. Dong XX, Wang Y, Qin ZH (2009) Molecular mechanisms of excitotoxicity and their relevance to pathogenesis of neurodegenerative diseases. Acta Pharmacol Sin 30:379-387
20. Du Y, Ma Z, Lin S et al (2001) Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. Proc Natl Acad Sci USA 98:14669-14674
21. Eikelenboom P, Veerhuis R, Scheper W et al (2006) The significance of neuroinflammation in understanding Alzheimer's disease. J Neural Transm 113:1685-1695
22. Estrada Sánchez AM, Mejía-Toiber J, Massieu L (2008) Excitotoxic neuronal death and the pathogenesis of Huntington's disease. Arch Med Res 39:265-276
23. Gafni J, Ellerby LM (2002) Calpain activation in Huntington's disease. J Neurosci 22:4842-4849
24. Gafni J, Hermel E, Young JE et al (2004) Inhibition of calpain cleavage of Huntingtin reduces toxicity: accumulation of calpain/caspase fragments in the nucleus. J Biol Chem 279:20211-20220
25. Ganzella M, Jardim FM, Boeck CR et al (2006) Time course of oxidative events in the hippocampus following intracerebroventricular infusion of quinolinic acid in mice. Neurosci Res 55:397-402
26. Garcia-Martinez EM, Sanz-Blasco S, Karachitos A et al (2010) Mitochondria and calcium flux as targets of neuroprotection caused by minocycline in cerebellar granule cells. Biochem Pharmacol 79:239-250
27. Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177:751-766
28. Green LC, Wagner DA, Glogowski J et al (1982) Analysis of nitrate, nitrite, and (15 N) nitrate in biological fluids. Ann Biochem 126: 131-138
29. Gunawardena S, Her LS, Brusch RG et al (2003) Disruption of axonal transport by loss of Huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 40:25-40
30. Hardingham GE (2009) Coupling of the NMDA receptor to neuroprotective and neurodestructive events. Biochem Soc Trans 37: 1147-1160
31. He Y, Appel S, Le W (2001) Minocycline inhibits microglial activation and protects nigral cells after 6-hydroxydopamine injection into mouse striatum. Brain Res 909:187-193
32. Homsi S, Federico F, Croci N et al (2009) Minocycline effects on cerebral edema: relations with inflammatory and oxidative stress markers following traumatic brain injury in mice. Brain Res 1291:122-132
33. Jiang W, Desjardins P, Butterworth RF (2009) Minocycline attenuates oxidative/nitrosative stress and cerebral complications of acute liver failure in rats. Neurochem Int 55:601-605
34. Kalonia H, Kumar P, Nehru B et al (2009a) Neuroprotective effect of MK-801 against intra-striatal quinolinic acid induced behavioral, oxidative stress and cellular alterations in rats. Indian J Exp Biol 47:880-892
35. Kalonia H, Kumar P, Kumar A et al (2009b) Effects of caffeic acid, rofecoxib and their combination against quinolinic acid-induced behavioral alterations and disruption in glutathione redox status. Neurosci Bull 25:343-352
36. Kalonia H, Kumar P, Kumar A et al (2010) Protective effect of rofecoxib and nimesulide against intra-striatal quinolinic acidinduced behavioral, oxidative stress and mitochondrial dysfunctions in rats. Neurotoxicology 31:195-203
37. Kono Y (1978) Generation of superoxide radical during autooxidation of hydroxylamine and an assay of superoxide dismutase. Arch Biochem Biophysics 186:189-195
38. Kulkarni SK (1999) Hand book of experimental pharmacology, 3rd edn. Vallabh Prakashan, Delhi
39. Leblhuber F, Walli J, Jellinger K et al (1998) Activated immune system in patients with Huntington's disease. Clin Chem Lab Med 36:747-750
40. Lim D, Fedrizzi L, Tartari M et al (2008) Calcium homeostasis and mitochondrial dysfunction in striatal neurons of Huntington disease. J Biol Chem 283:5780-5789
41. Lin CH, Lin YF, Chang MC et al (2001) Advanced glycosylation end products induce nitric oxide synthase expression in C6 glioma cells: involvement of a p38 MAP kinase-dependent mechanism. Life Sci 69:2503-2515
42. Liu XD, Wang JJ, Sun L et al (2009) Involvement of medullary dorsal horn glial cell activation in mediation of masseter mechanical allodynia induced by experimental tooth movement. Arch Oral Biol 54:1143-1150
43. Luck H (1971) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press, New York
44. Mattson MP (2003) Excitotoxic and excitoprotective mechanisms: abundant targets for the prevention and treatment of neurodegenerative disorders. Neuromol Med 3:65-94
45. McGeer PL, McGeer EG (2004) Inflammation and the degenerative diseases of aging. Ann N Y Acad Sci 1035:104-116
46. Milakovic T, Quintanilla RA, Johnson GV (2006) Mutant Huntingtin expression induces mitochondrial calcium handling defects in clonal striatal cells: functional consequences. J Biol Chem 281: 34785-34795
47. Minghetti L, Greco A, Potenza RL et al (2007) Effects of the adenosine A2A receptor antagonist SCH 58621 on cyclooxygenase- 2 expression, glial activation, and brain-derived neurotrophic factor availability in a rat model of striatal neurodegeneration. J Neuropathol Exp Neurol 66:363-371
48. Mishra MK, Ghosh D, Duseja R et al (2009) Antioxidant potential of minocycline in Japanese encephalitis virus infection in murine neuroblastoma cells: correlation with membrane fluidity and cell death. Neurochem Int 54:464-470
49. Panov AV, Gutekunst CA, Leavitt BR et al (2002) Early mitochondrial calcium defects in Huntington's disease are a direct effect of polyglutamines. Nat Neurosci 5:731-736
50. Pavese N, Gerhard A, Tai YF et al (2006) Microglial activation correlates with severity in Huntington disease: a clinical and PET study. Neurology 66:1638-1643
51. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, 6th edn. Academic Press, San Diego
52. Rossato JI, Zeni G, Mello CF et al (2002) Ebselen blocks the quinolinic acid-induced production of thiobarbituric acid reactive species but does not prevent the behavioral alterations produced by intra-striatal quinolinic acid administration in the rat. Neurosci Lett 318:137-140
53. Sanchez Mejia RO, Ona VO, Li M et al (2001) Minocycline reduces traumatic brain injury-mediated caspase-1 activation, tissue damage, and neurological dysfunction. Neurosurgery 48:1393-1401
54. Sapp E, Kegel KB, Aronin N et al (2001) Early and progressive accumulation of reactive microglia in the Huntington disease brain. J Neuropathol Exp Neurol 60:161-172
55. Sattler R, Tymianski M (2001) Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Mol Neurobiol 24:107-129
56. Scarabelli TM, Stephanou A, Pasini E et al (2004) Minocycline inhibits caspase activation and reactivation, increases the ratio of XIAP to smac/DIABLO, and reduces the mitochondrial leakage of cytochrome c and smac/DIABLO. J Am Coll Cardiol 43: 865-874
57. Smith DL, Woodman B, Mahal A et al (2003) Minocycline and doxycycline are not beneficial in a model of Huntington's disease. Ann Neurol 54:186-196
58. Song C, Zhang Y, Parsons CG et al (2003) Expression of polyglutamine- expanded Huntingtin induces tyrosine phosphorylation of N-methyl-d-aspartate receptors. J Biol Chem 278:33364-33369
59. Stolp HB, Dziegielewska KM (2009) Review: role of developmental inflammation and blood-brain barrier dysfunction in neurodevelopmental and neurodegenerative diseases. Neuropathol Appl Neurobiol 35:132-146
60. Szebenyi G, Morfini GA, Babcock A et al (2003) Neuropathogenic forms of Huntingtin and androgen receptor inhibit fast axonal transport. Neuron 40:41-52
61. Tai YF, Pavese N, Gerhard A et al (2007) Microglial activation in presymptomatic Huntington's disease gene carriers. Brain 130: 1759-1766
62. Tang TS, Tu H, Chan EY et al (2003) Huntingtin and huntingtin associated protein 1 influence neuronal calcium signaling mediated by inositol-(1,4,5) triphosphate receptor type 1. Neuron 39:227-239
63. Tang M, Alexander H, Clark RS et al (2010) Minocycline reduces neuronal death and attenuates microglial response after pediatric asphyxial cardiac arrest. J Cereb Blood Flow Metab 30:119-129
64. Tikka TM, Koistinaho JE (2001) Minocycline provides neuroprotection against N-methyl-d-aspartate neurotoxicity by inhibiting microglia. J Immunol 166:7527-7533
65. Tikka T, Fiebich BL, Goldsteins G et al (2001) Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 21:2580-2588
66. Tikka TM, Vartiainen NE, Goldsteins G et al (2002) Minocycline prevents neurotoxicity induced by cerebrospinal fluid from patients with motor neurone disease. Brain 125:722-731
67. Tsuji M, Wilson MA, Lange MS et al (2004) Minocycline worsens hypoxic-ischemic brain injury in a neonatal mouse model. Exp Neurol 189:58-65
68. Turmaine M, Raza A, Mahal A et al (2000) Nonapoptotic neurodegeneration in a transgenic mouse model of Huntington's disease. Proc Natl Acad Sci USA 97:8093-8097
69. Tzeng SF, Hsiao HY, Mak OT (2005) Prostaglandins and cyclooxygenases in glial cells during brain inflammation. Curr Drug Targets Inflamm Allergy 4:335-340
70. Wang X, Zhu S, Drozda M et al (2003) Minocycline inhibits caspaseindependent and -dependent mitochondrial cell death pathways in models of Huntington's disease. Proc Natl Acad Sci USA 100:10483-10487
71. Wang J, Wei Q, Wang CY et al (2004) Minocycline up-regulates Bcl- 2 and protects against cell death in the mitochondria. J Biol Chem 279:19948-19954
72. Wang X, Gao X, Zhang X et al (2006) The negative cell cycle regulator, Tob (transducer of ErbB-2), is involved in motor skill learning. Biochem Biophy Res Comm 340:1023-1027
73. Wellington CL, Ellerby LM, Leavitt BR et al (2003) Huntingtin proteolysis in Huntington disease. Clin Neurosci Res 3:129-139
74. Wills ED (1966) Mechanisms of lipid peroxide formation in animal tissues. Biochem J 99:667-676
75. Wu DC, Jackson-Lewis V, Vila M et al (2002) Blockade of microglial activation is neuroprotective in the 1-methyl-4- phenyl-1,2,3,6- tetrahydropyridine mouse model of Parkinson disease. J Neurosci 22:1763-1771
76. Yang L, Sugama S, Chirichigno JW et al (2003) Minocycline enhances MPTP toxicity to dopaminergic neurons. J Neurosci Res 74:278-285
77. Yrjanheikki J, Keinanen R, Pellikka M et al (1998) Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci USA 95:15769-15774
78. Yrjanheikki J, Tikka T, Keinanen R et al (1999) A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci USA 96:13496-13500
79. Zeron MM, Hansson O, Chen N et al (2002) Increased sensitivity to N-methyl-d-aspartate receptor-mediated excitotoxicity in a mouse model of Huntington's disease. Neuron 33:849-860
80. Zhu S, Stavrovskaya IG, Drozda M et al (2002) Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 417:74-78
81. Zilka N, Stozicka Z, Kovac A et al (2009) Human misfolded truncated tau protein promotes activation of microglia and leukocyte infiltration in the transgenic rat model of tauopathy. J Neuroimmunol 209:16-25
82. Zuccato C, Tartari M, Crotti A et al (2003) Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes. Nat Genet 35:76-83