Minocycline: Neuroprotective mechanisms in Parkinson's disease

Current Pharmaceutical Design

Volumn 10, Issue 6, 2004, Pages 679-686

  Thomas, M ^a   Le, W D ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Apoptosis; Caspase; Dopamine; Microglia; Minocycline; Neuroprotection; Parkinson's disease; Tetracycline derivatives

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; CASPASE; CASPASE INHIBITOR; CEP 1347; CMT 8; DOXYCYCLINE; MINOCYCLINE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MIXED LINEAGE LEUKEMIA PROTEIN; NEUROPROTECTIVE AGENT; NITRIC OXIDE SYNTHASE; OXIDOPAMINE; TETRACYCLINE DERIVATIVE; UNCLASSIFIED DRUG;

APOPTOSIS; AUTOIMMUNE DISEASE; AUTONOMIC NERVOUS SYSTEM; BRADYKINESIA; BRAIN CORTEX; CELL ACTIVATION; CLINICAL FEATURE; CLINICAL TRIAL; COGNITIVE DEFECT; CRANIAL NERVE; DISABILITY; DISEASE SEVERITY; DOSE RESPONSE; DRUG MECHANISM; DRUG SAFETY; DRUG TOLERABILITY; ENZYME INHIBITION; EVIDENCE BASED MEDICINE; HEPATITIS; HUMAN; HUNTINGTON CHOREA; HYPERSENSITIVITY; INFLAMMATION; LEWY BODY; LOCUS CERULEUS; LUPUS VULGARIS; MEYNERT BASAL NUCLEUS; MICROGLIA; MOUSE; MUSCLE RIGIDITY; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PATHOPHYSIOLOGY; PNEUMONIA; PRIORITY JOURNAL; RAPHE NUCLEUS; REVIEW; SUBSTANTIA NIGRA; TREMOR; VASCULITIS;

ANIMALS; ANTIPARKINSON AGENTS; APOPTOSIS; CLINICAL TRIALS; HUMANS; MINOCYCLINE; MITOCHONDRIA; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PARKINSON DISEASE;

EID: 1442326012     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/1381612043453162     Document Type: Review

References (96)

1. Lang AE, Lozano AM. Parkinson's disease. First of two parts. N Engl J Med 1998; 339: 1044-53.
2. Hoehn MM, Yahr MD. Parkinsonism: onset, progression, and mortality 1967. Neurology 1998; 50: 318-34.
3. Polymeropoulos MH, Lavedan C, Leroy E et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's Disease. Science 1997; 276: 2045-47.
4. Kitada T, Asakawa S, Hattori N et al. Mutations in the Parkin gene causes autosomal recessive juvenile Parkinsonism. Nature 1998; 392: 605-8.
5. Mouradian AM. Recent advances in the genetics and pathogenesis of Parkinson disease. Neurology 2002; 58: 179-85.
6. Olanow CW, Tatton WG, Jenner P. Mechanisms of cell death in Parkinson's disease. In: Jankovic J, Tolosa E, Eds. Parkinson's Disease and Movement Disorders, 4th edition, Lippincott Williams and Wilkins, Philadephia, PA 2002.
7. Togo T, Iseki E, Marui W, Akiyama H, Uéda K and Kosaka K. Glial involvement in the degeneration process of Lewy body-bearing neurons and the degradation process of Lewy bodies in brains of dementia with Lewy bodies. J Neurol Sci 2001; 184: 71-5.
8. Wakabayashi K, Hayashi S, Yoshimoto M, Kudo H, Takahashi H. NACP/a-synuclein-positive filamentous inclusions in astrocytes and oligodendrocytes of Parkinson's disease brains. Acta Neuropathol. 2000; 99: 14-20.
9. Lang-Rollin I, Rideout H, Stefanis L. Ubiquitinated inclusions and neuronal cell death. Histol Histopathol 2003; 18: 509-17.
10. McNaught KS, Olanow CW, Halliwell B, Isacson O, Jenner P. Failure of the ubiquitin-proteasome system in Parkinson's disease. Nat Rev Neurosci 2001; 2: 589-94.
11. McNaught KS, Belizaire R, Isacson O, Jenner P, Olanow CW. Altered proteasomal function in sporadic Parkinson's disease. Exp Neurol 2003; 179: 38-46.
12. Ryu EJ, Harding HP, Angelastro JM, Vitolo OV, Ron D, Greene LA. Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson's disease.J Neurosci 2002; 22: 10690-8.
13. Greene JC, Whitworth AJ, Kuo I, Andrews LA, Feany MB, Pallanck LJ. Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc Natl Acad Sci USA 2003; 100: 4078-83.
14. Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, Greenamyre JT. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat Neurosci 2000; 3: 1301-6.
15. Sherer TB, Betarbet R, Stout AK, Lund S, Baptista M, Panov AV, Cookson MR, Greenamyre JT. An in vitro model of Parkinson's disease: linking mitochondrial impairment to altered alpha-synuclein metabolism and oxidative damage. J Neurosci 2002; 22: 7006-15
16. Olanow CW, Jenner P, Beal F. Neurodegeneration and neuroprotection in Parkinson's disease. Suppl to Ann Neurol 1998; 44(3).
17. Kerr JFR, Wyllie AH, Currie AH. Apoptosis, a basic biological phenomenon with wider implications in tissue kinetics. Br J Cancer 1972; 26: 239-45
18. Wolozin B, Behl C. Mechanisms of neurodegenerative diseases. Part 1: Protein aggregates. Arch Neurol 2000; 57: 793-6.
19. Wolozin B, Behl C. Mechanisms of neurodegenerative diseases. Part 2: Control of cell death. Arch Neurol 2000; 57: 801-4.
20. Hartmann A, Mouatt-Prigent A, Faucheux BA, Agid Y, Hirsch EC. FADD: A link between TNF family receptors and caspases in Parkinson's disease. Neurology 2002; 58: 308-10
21. Furukawa K, Mattson M. The transcription factor NF-κB mediates increases in calcium currents and decreases in NMDA- and AMPA/Kainate- induced currents induced by tumor necrosis factor -α in hippocampal neurons. J Neurochem 1998; 70: 1876-86.
22. Wang X, Qin ZH, Leng Y, Wang Y, Jin X, Chase TN, Bennett MC. Prostaglandin A1 inhibits rotenone-induced apoptosis in SH-SY5Y cells. J Neurochem 2002; 83: 1094-102.
23. Kahns S, Lykkebo S, Jakobsen LD, Nielsen MS, Jensen PH. Caspase-mediated parkin cleavage in apoptotic cell death. J Biol Chem 2002; 277: 15303-8
24. Jellinger KA. Cell death mechanisms in neurodegeneration. J Cell Mol Med 2001; 5: 1-17.
25. Tatton NA. Increased caspase 3 and bax immunoreactivity accompany nuclear GAPDH translocation and neuronal apoptosis in Parkinson's disease. Exp Neurol 2000; 166: 29-43.
26. Mochizuki H, Goto K, Mori H, Mizuno Y. Histochemical detection of apoptosis in Parkinson's disease. J Neurol Sci 1996; 137: 120-3.
27. Friedlander RM. Role of caspase 1 in neurologic disease. Arch Neurol 2000; 57: 1273-6.
28. Mogi M, Togari A, Kondo T et al. Caspase activities and tumor necrosis factor receptor R1 (p55) level are elevated in the substantia nigra from parkinsonian brain. J Neural Transm 2000; 107: 335-41.
29. Boka G, Anglade P, Wallach D, Javoy-Agid F, Agid Y, Hirsch EC. Immunocytochemical analysis of tumor necrosis factor and its receptors in Parkinson' s disease. Neurosci Lett 1994; 172: 151-4.
30. Hartmann A, Hunot S, Michel PP et al. Caspase-3: A vulnerability factor and final effector in apoptotic death of dopaminergic neurons in Parkinson's disease. Proc Natl Acad Sci USA 2000; 97: 2875-80.
31. Dobrenis K. Microglia in cell culture and in transplantation therapy for central nervous system disease. Methods 1998; 16: 320-44.
32. Flugel A, Bradl M, Kreutzberg GW and Graeber MB. Transformation of donor-derived bone marrow precursors into host microglia during autoimmune CNS inflammation and during the retrograde response to axotomy. J Neurosci Res 2001; 66: 74-82.
33. Appel SH, Le WD, Tajti J, Haverkamp LJ, Engelhardt JI. Nigral damage and dopaminergic hypofunction in mesencephalon-immunized guinea pigs. Ann Neurol 1992; 32: 494-501.
34. Le WD, Engelhardt J, Xie WJ, Schneider L, Smith RG, Appel SH. Experimental autoimmune nigral damage in guinea pigs. J Neuroimmunol 1995; 57: 45-53.
35. Chen SD, Le WD, Xie WJ, Alexianu ME, Engelhart JI, Siklos L, Appel SH. Experimental destruction of substantia nigra initiated by Parkinson disease immunoglobulins. Arch Neurol 1998, 55: 1075-80.
36. Le WD, Rowe D, Xie WJ, Ortiz I, He Y, Appel SH. Microglial activation and dopaminergic cell injury: an in vitro model relevant to Parkinson's disease. 2001; 21; 8447-55
37. Grunblatt E, Mandel S and Youdim MB. Neuroprotective strategies in Parkinson's disease using the models of 6-hydroxydopamine and MPTP. Ann NY Acad Sci 2000; 899: 262-73.
38. Kurkowska-Jastrzebska I, Wronska A, Kohutnicka M, Czlonkowski A and Czlonkowska A. The inflammatory reaction following 1-methyl-4-phenyl-1,2,3, 6-tetrahydropyridine intoxication in mouse. Exp Neurol 1999; 156: 50-61.
39. Czlonkowski A and Czlonkowska A. MHC class II positive microglia and lymphocytic infiltration are present in the substantia nigra and striatum in mouse model of Parkinson's disease. Acta Neurobiol Exp 1999b 59: 1-8.
40. Du Y, Ma Z, Lin S, et al. Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. Proc Natl Acad Sci USA 2001; 98: 14669-74.
41. Liberatore GT, Jackson-Lewis V, Vukosavic S, et al. Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat Med 1999; 5: 1403-9.
42. Mogi, M., Harada M, Kondo T et al. Interleukin-1 beta, interleukin-6, epidermal growth factor and transforming growth factor-alpha are elevated in the brain from parkinsonian patients. Neurosci Lett 1994; 180: 147-50.
43. Le WD, Rowe DB, Jankovic J, Xie WJ, Appel SH. Effects of cerebrospinal fluid from patients with Parkinson disease on dopaminergic cells. Arch Neurol 1999; 56: 194-200.
44. Mirza B, Hadberg H, Thomsen P and Moos T. The absence of reactive astrocytosis is indicative of a unique inflammatory process in Parkinson's disease. Neuroscience 2000; 95: 425-32.
45. Shepherd CE, Thiel E, McCann H, Harding AJ and Halliday GM. Cortical inflammation in Alzheimer's disease but not Lewy body dementia. Arch Neurol 2000; 57: 817-22.
46. Broe M, Shepherd C, Milward E and Halliday G. Relationship between DNA fragmentation, morphological changes and neuronal loss in Alzheimer's disease and dementia with Lewy bodies. Acta Neuropathol 2001; 101: 616-24.
47. Clarke G, Collins RA, Leavitt BR, et al. A on e-hit model of cell death in inherited neuronal degenerations. Nature 2000; 406: 195-9.
48. Hardman CD, Henderson J, Finkelstein DI, Paxinos G, Horne MK and Halliday GM. Comparison of the basal ganglia in rats, marmosets, macaques, baboons and humans: volume and neuronal number for the output and internal relay and striatal modulating nuclei. J Comp Neurol 2002; 445: 238-55.
49. McGeer PL, Itagaki S, Akiyama H and McGeer EG. Rate of cell death in Parkinsonism indicates active neuropathological process. Ann Neurol 1988; 24: 574-6.
50. Czlonkowska A, Kohutnicka M, Kurkowska-Jastrzebska I, Czlonkowski A. Microglial reaction in MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) induced Parkinson's disease mice model. Neurodegeneration 1996; 5: 137-43.
51. Kohutnicka M, Lewandowska E, Kurkowska-Jastrzebska I, Czlonkowski A, Czlonkowska A. Microglial and astrocytic involvement in a murine model of Parkinson's disease induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Immunopharmacol 1988; 39: 167-80.
52. Akiyama H, McGeer P. Microglial response to 6-hydroxydopamine-induced substantia nigra lesions. Brain Res 1989; 489: 247-53.
53. He Y, Lee T, Leong SK. 6-Hydroxydopamine induced apoptosis of dopaminergic cells in the rat substantia nigra. Brain Res 2000; 858: 163-6.
54. Liu B, Du L, Hong JS. Naloxone protects rat dopaminergic neurons against inflammatory damage through inhibition of microglia activation and superoxide generation. J Pharmacol Exp Ther 2000; 293: 607-17.
55. Liberatore GT, Jackson-Lewis V, Vukosavic S. Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat Med 1999; 5: 1403-9.
56. Ryan M, Greenwald RA, Golub LM. Potential of tetracyclines to modify cartilage breakdown in osteoarthritis. Curr Opin Rheum. 1996; 8: 238-47.
57. Golub LM, Ramamurthy NS, Llavaneras A et al. A chemically modified non-microbial tetracycline (CMT-8) inhibits gingival matrix metalloproteinases, periodontal breakdown, and extra-oral bone loss in ovariectomized rats. Ann NY Acad Sci 1999; 878: 290-310.
58. Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan P.H, Koistinaho J. A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci USA 1999; 96: 13496-500.
59. Tikka TM, Koistinaho JE. Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. J Immunol 2001; 166: 7527-33.
60. Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 2001; 21: 2580-8.
61. Lin S, Zhang Y, Dodel R, Farlow MR, Paul SM, Du Y. Minocycline blocks nitric oxide-induced neurotoxicity by inhibition p38 MAP kinase in rat cerebellar granule neurons. Neurosci Lett 2001; 315: 61-4.
62. Arvin KL, Han BH, Du Y, et al. Minocycline markedly protects the neonatal brain against hypoxic-ischemic injury. Ann Neurol 2002; 52: 54-61.
63. Sanchez MRO, Ona VO, Li M, Friedlander RM. Minocycline reduces traumatic brain injury-mediated caspase-1 activation, tissue damage, and neurological dysfunction. Neurosurg 2001; 48: 1393-9.
64. Tikka T, Usenius T, Tenhunen M, Keinanen R, Koistinaho J. Tetracycline derivatives and ceftriaxone, a cephalosporin antibiotic, protect neurons against apoptosis induced by ionizing radiation. J Neurochem 2001; 78: 1409-14.
65. Tikka T, Fiebich B, Goldsteins G, Keinanen R, Koistinaho J. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J of Neurosci. 2001; 21: 2580-8.
66. He Y, Appel S, Le W. Minocycline inhibits microglial activation and protects nigral cells after 6-hydroxydopamine injection into mouse striatum. Brain Res 2001; 909: 187-93.
67. Do Y, Ma Z, Lin S, Dodel RC et al. Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. Proc Natl Acad Sci USA 2001; 98: 14669-74.
68. Amin AR, Patel RN, Thakker GD, Lowenstein CJ, Attur MG, Abramson SB. Post-transcriptional regulation of inducible nitric oxide synthase mRNA in murine macrophages by doxycycline and chemically modified tetracyclines. FEBS Lett 1997; 410: 259-64.
69. Lassus P, Opitz-Araya X, Lazebnik Y. Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science 2002; 297: 1352-4.
70. Zhu S, Stavrovskaya IG, Drodza M, et al. Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 2002; 417: 74-8.
71. Chen M, Ona VO, Li M, Ferrante RJ et al. Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat Med 2000; 6: 797-801.
72. Yamamoto A, Lucas JJ, Hen R. Reversal of neuropathology and motor dysfunction in a conditional model of Huntington's disease. Cell. 2000; 101: 57-66.
73. Van Den Bosch L, Tilkin P, Lemmens G, Robberecht W. Minocycline delays disease onset and mortality in a transgenic model of ALS. Neuroreport. 2002; 13: 1067-70.
74. Tikka TM, Vartiainen NE, Goldsteins G, et al. Minocycline prevents neurotoxicity induced by cerebrospinal fluid from patients with motor neuron disease. Brain. 2002; 125: 722-31.
75. Lin S, Wei X, Xu Y et al. Minocycline blocks 6-hydroxydopamine-induced neurotoxicity and free radical production in rat cerebellar granule neurons. Life Sci 2003; 72: 1635-41
76. Wu DC, Jackson-Lewis W, Vila M, et al. Blockade of microglial activation is neuroprotective in the 1-methy-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J Neurosci 2002; 22: 1763-71
77. Volbracht C, Fava E, Leist M, Nicotera P. Calpain inhibitors prevent nitric oxide-triggered excitotoxic apoptosis Neuroreport 2001; 12:3645-8.
78. Morita F, Wen TC, Tanaka J et al. Protective effect of a prosaposin-derived, 18-mer peptide on slowly progressive neuronal degeneration after brief ischemia. J Cereb Blood Flow Metab 2001; 21: 1295-302.
79. Alessandrini A, Namura S, Moskowitz M, Bonventre J. MEK1 protein kinase inhibition protects against damage resulting from focal cerebral ischemia. Proc Natl Acad Sci USA 1999; 96: 12866-9.
80. Bozyczko-Coyne D, O'Kane TM, Wu ZL, et al. CEP-1347/KT-7515, an inhibitor of SAPK/JNK pathway activation, promotes survival and blocks multiple events associated with Abeta-induced cortical neuron apoptosis. J Neurochem 2001; 77: 849-63.
81. Bilsland J, Harper S. Caspases and neuroprotection. Curr Opin Investig Drugs 2002; 3: 1745-52
82. Eberhardt O, Schulz JB. Apoptotic mechanisms and antiapoptotic therapy in the MPTP model of Parkinson's disease. Toxicol Lett 2003; 139: 135-51.
83. O'Dell JR, Blakely KW, Mallek JA, et al. Treatment of early seropositive rheumatoid arthritis: a two-year, double blind comparison of minocycline and hydroxychloroquine. Arthritis Rheum 2001; 44: 2235-41.
84. O'Dell JR, Paulsen G, Haire CE et al. Treatment of early seropositive rheumatoid arthritis with Minocycline. Four-year follow up of a double blind placebo controlled trial. Arthritis rheum 1999; 42: 1691-5.
85. Goulden V, Glass D, Cunliffe WJ. Safety of long-term high-dose minocycline in the treatment of acne. Br J Dermatol 1996; 134: 693-5.
86. Settgast AM, Groth T, Gertner E. Minocycline-induced central nervous system-pulmonary hypersensitivity syndrome. Int J Dermatol 2003; 42: 316-7.
87. Elkayam O, Yaron M, Caspi D. Minocycline-induced autoimmune syndromes: an overview. Semin Arthr Rheum. 1999; 28: 392-7.
88. Balestrero S, Ciambellotti A, parody A, Rebora A. Minocycline-induced lupus-like syndrome. Int'l J Dermatol, 2001; 40: 474-5.
89. Angulo JM, Sigal LH, Espinoza LR. Minocycline induced lupus and autoimmune hepatitis. J Rheumatol 1999; 26: 1420-1.
90. Weese-Mayer DE, Yang RJ, Mayer JR, Zaparackas Z. Minocycline and pseudotumor cerebri: The well known, but well-kept secret. Pediatrics. 2001; 108: 519-20.
91. Thomas M, Le WL, Jankovic J. Minocycline and other Tetracycline derivatives: A neuroprotective strategy in Parkinson's disease and Huntington's disease. Clin Neuropharm. 2003; 26: 1-7.
92. Denovan-Wright EM, Devarajan S, Dursun SM, Robertson HA. Maintained improvement with minocycline of a patient with advanced Huntington's disease. J Psychopharmacol 2002; 16: 393-4.
93. Bonelli RM, Heuberger C, Reisecker F. Minocycline in Huntington's disease: an open label study. Neurology. 2003; 60: 883-4.
94. Clausen T, Bullock R. Medical treatment and neuroprotection in traumatic brain injury. Curr Pharm Design 2001; 7(15): 1517-32.
95. Ito C. Analysis of overall gene expression induced by amphetamine and phencyclidine: novel targets for the treatment of drug psychosis and schizophrenia. Curr Pharm Design 2002; 8(2): 147-53.
96. Nikam SS, Meltzer LT. NR2B selective NMDA receptor antagonists. Curr Pharm Design 2002; 8(10): 845-55.