The prospects of minocycline in multiple sclerosis

Journal of Neuroimmunology

Volumn 235, Issue 1-2, 2011, Pages 1-8

  Chen, Xiaohong ^a   Ma, Xiaomeng ^a   Jiang, Ying ^a   Pi, Rongbiao ^a   Liu, Yingying ^a   Ma, Lili ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

Experimental autoimmune encephalomyelitis; Minocycline; Multiple sclerosis

Indexed keywords

ATORVASTATIN; BETA1A INTERFERON; GLATIRAMER; GLUCOCORTICOID; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; INTERFERON BETA SERINE; METHYLPREDNISOLONE; MINOCYCLINE; PLACEBO; PREDNISONE;

ABNORMAL LABORATORY RESULT; ADD ON THERAPY; ALLERGIC ENCEPHALOMYELITIS; BEDTIME DOSAGE; BRAIN INFARCTION; BRAIN ISCHEMIA; DISEASE ACTIVITY; DISEASE SEVERITY; DIZZINESS; DRUG DOSE REDUCTION; DRUG EFFECT; DRUG EFFICACY; DRUG INDUCED HEADACHE; DRUG MECHANISM; DRUG MEGADOSE; DRUG SAFETY; HUMAN; IMMUNOPATHOGENESIS; INJECTION SITE REACTION; MICROGLIA; MORNING DOSAGE; MULTIPLE SCLEROSIS; NAUSEA; NERVE CELL STIMULATION; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; OPTIMAL DRUG DOSE; PRIORITY JOURNAL; REVIEW; SINGLE DRUG DOSE; T LYMPHOCYTE; TREATMENT DURATION; TREATMENT RESPONSE;

ANIMALS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; MICROGLIA; MINOCYCLINE; MULTIPLE SCLEROSIS;

EID: 79958004172     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2011.04.006     Document Type: Review

References (92)

1. Antel J.P., Miron V.E. Central nervous system effects of current and emerging multiple sclerosis-directed immuno-therapies. Clin. Neurol. Neurosurg. 2008, 110:951-957.
2. Aronson A.L. Pharmacotherapeutics of the newer tetracyclines. J. Am. Vet. Med. Assoc. 1980, 176:1061-1068.
3. Blum D., Chtarto A., Tenenbaum L., Brotchi J., Levivier M. Clinical potential of minocycline for neurodegenerative disorders. Neurobiol. Dis. 2004, 17:359-366.
4. Bonelli R.M., Heuberger C., Reisecker F. Minocycline for Huntington's disease: an open label study. Neurology 2003, 60:883-884.
5. Brundula V., Rewcastle N.B., Metz L.M., Bernard C.C., Yong V.W. Targeting leukocyte MMPs and transmigration-minocycline as a potential therapy for multiple sclerosis. Brain 2002, 125:1297-1308.
6. Buljevac D., Verkooyen R.P., Jacobs B.C., Hop W., van Der Zwaan L.A., van Doorn P.A., Hintzen R.Q. Chlamydia pneumoniae and the risk for exacerbation in multiple sclerosis patients. Ann. Neurol. 2003, 54:828-831.
7. Chen X.H., Hu X.Q., Zou Y., Pi R.B., Liu M., Wang T.Q., Zheng X.P., Lin M.D., Liu P.Q., Tao L. Combined treatment with minocycline and prednisone attenuates experimental autoimmune encephalomyelitis in C57 BL/6 mice. J. Neuroimmunol. 2009, 210:22-29.
8. Chen X., Pi R., Liu M., Ma X., Jiang Y., Liu Y., Mao X., Hu X. Combination of methylprednisolone and minocycline synergistically improves experimental autoimmune encephalomyelitis in C57 BL/6 mice. J. Neuroimmunol. 2010, 226:104-109.
9. Conway D., Cohen J.A. Combination therapy in multiple sclerosis. Lancet Neurol. 2010, 9:299-308.
10. Diem R., Sattler M.B., Merkler D., Demmer I., Maier K., Stadelmann C., Ehrenreich H., Bahr M. Combined therapy with methylprednisolone and erythropoietin in a model of multiple sclerosis. Brain 2005, 128:375-385.
11. Dowdell K.C., Gienapp I.E., Stuckman S., Wardrop R.M., Whitacre C.C. Neuroendocrine modulation of chronic relapsing experimental autoimmune encephalomyelitis: a critical role for the hypothalamic-pituitary-adrenal axis. J. Neuroimmunol. 1999, 100:243-251.
12. Fan L.W., Pang Y., Lin S., Rhodes P.G., Cai Z. Minocycline attenuates lipopolysaccharide-induced white matter injury in the neonatal rat brain. Neuroscience 2005, 133:159-168.
13. Gabler W.L., Smith J., Tsukuda N. Comparison of doxycycline and a chemically modified tetracycline inhibition of leukocyte functions. Res. Commun. Chem. Pathol. Pharmacol. 1992, 78:151-160.
14. Giuliani F., Fu S.A., Metz L.M., Yong V.W. Effective combination of minocycline and interferon-beta in a model of multiple sclerosis. J. Neuroimmunol. 2005, 165:83-91.
15. Giuliani F., Metz L.M., Wilson T., Fan Y., Bar-Or A., Yong V.W. Additive effect of the combination of glatiramer acetate and minocycline in a model of MS. J. Neuroimmunol. 2005, 158:213-221.
16. Golub L.M., Ramamurthy N., McNamara T.F., Gomes B., Wolff M., Casino A., Kapoor A., Zambon J., Ciancio S., Schneir M., Perry H. Tetracyclines inhibit tissue collagenase activity-a new mechanism in the treatment of periodontal-disease. J. Periodontal Res. 1984, 19:651-655.
17. Gonsette R.E. Neurodegeneration in multiple sclerosis: the role of oxidative stress and excitotoxicity. J. Neurol. Sci. 2008, 274:48-53.
18. Good M.L., Hussey D.L. Minocycline: stain devil?. Br. J. Dermatol. 2003, 149:237-239.
19. Gordon P.H., Moore D.H., Miller R.G., Florence J.M., Verheijde J.L., Doorish C., Hilton J.F., Spitalny G.M., MacArthur R.B., Mitsumoto H., Neville H.E., Boylan K., Mozaffar T., Belsh J.M., Ravits J., Bedlack R.S., Graves M.C., McCluskey L.F., Barohn R.J., Tandan R., Western A.L.S.S.G. Efficacy of minocycline in patients with amyotrophic lateral sclerosis: a phase III randomised trial. Lancet Neurol. 2007, 6:1045-1053.
20. Gutteridge J.M.C. Iron and oxygen radicals in brain. Ann. Neurol. 1992, 32:S16-S21.
21. Haranaga S., Ikejim H., Yamaguchi H., Friedman H., Yamamoto Y. Analysis of Chlamydia pneumoniae growth in cells by reverse transcription-PCR targeted to bacterial gene transcripts. Clin. Diagn. Lab. Immunol. 2002, 9:313-319.
22. Hardmeier M., Wagenpfeil S., Freitag P., Fisher E., Rudick R.A., Kooijmans M., Clanet M., Radue E.W., Kappos L., European I.-a.R.M.S. Rate of brain atrophy in relapsing MS decreases during treatment with IFN beta-1a. Neurology 2005, 64:236-240.
23. Hohlfeld R. Biotechnological agents for the immunotherapy of multiple sclerosis-principles, problems and perspectives. Brain 1997, 120:865-916.
24. Hu W., Metselaar J., Ben L.H., Cravens P.D., Singh M.P., Frohman E.M., Eagar T.N., Racke M.K., Kieseier B.C., Stuve O. PEG minocycline-liposomes ameliorate CNS autoimmune disease. PLoS One 2009, 4:e4151.
25. Jordan J., Fernandez-Gomez J., Ramos M., Ikuta I., Aguirre N., Galindo F. Minocycline and cytoprotection: shedding new light on a shadowy controversy. Curr. Drug Deliv. 2007, 4:225-231.
26. Kalish R.S., Koujak S. Minocycline inhibits antigen processing for presentation to human T cells: additive inhibition with chloroquine at therapeutic concentrations. Clin. Immunol. 2004, 3:270-277.
27. Kieseier B.C., Wiendl H., Hemmer B., Hartung H.P. Treatment and treatment trials in multiple sclerosis. Curr. Opin. Neurol. 2007, 20:286-293.
28. Kim H.S., Suh Y.H. Minocycline and neurodegenerative diseases. Behav. Brain Res. 2009, 196:168-179.
29. Kim S.S., Kong P.J., Kim B.S., Sheen D.H., Nam S.Y., Chun W. Inhibitory action of minocycline on lipopolysaccharide-induced release of nitric oxide and prostaglandin E2 in BV2 microglial cells. Arch. Pharm. Res. 2004, 27:314-318.
30. Kloppenburg M., Verweij C.L., Miltenburg A.M.M., Verhoeven A.J., Daha M.R., Dijkmans B.A.C., Breedveld F.C. The influence of tetracyclines on T cell activation. Clin. Exp. Immunol. 1995, 102:635-641.
31. Kloppenburg M., Brinkman B.M.N., DeRooijDijk H.H., Miltenburg A.M.M., Daha M.R., Breedveld F.C., Dijkmans B.A.C., Verweij C.L. The tetracycline derivative minocycline differentially affects cytokine production by monocytes and T lymphocytes. Antimicrob. Agents Chemother. 1996, 40:934-940.
32. Kraus R.L., Pasieczny R., Lariosa-Willingham K., Turner M.S., Jiang A., Trauger J.W. Antioxidant properties of minocycline: neuroprotection in an oxidative stress assay and direct radical-scavenging activity. J. Neurochem. 2005, 94:819-827.
33. Levine S.M., Chakrabarty A. The role of iron in the pathogenesis of experimental allergic encephalomyelitis and multiple sclerosis. Ann. N.Y. Acad. Sci. 2004, 1012:252-266.
34. Liu S.H., Xue M.Z., Yong V.W. Identification of heme oxygenase-1 as a novel target of neuroprotection by minocycline in human neurons. J. Neuroimmunol. 2008, 203:246.
35. Lu F.M., Selak M., O'Connor J., Croul S., Lorenzana C., Butunoi C., Kalman B. Oxidative damage to mitochondrial DNA and activity of mitochondrial enzymes in chronic active lesions of multiple sclerosis. J. Neurol. Sci. 2000, 177:95-103.
36. Luccanini I., Ballerini C., Blagioli T., Biamonte F., Bellucci A., Rosi M.C., Grossi C., Massacesi L., Casamenti F. Combined treatment with atorvastatin and minocycline suppresses severity of EAE. Exp. Neurol. 2008, 211:214-226.
37. Maier K., Merkler D., Gerber J., Taheri N., Kuhnert A.V., Williams S.K., Neusch C., Bahr M., Diem R. Multiple neuroprotective mechanisms of minocycline in autoimmune CNS inflammation. Neurobiol. Dis. 2007, 25:514-525.
38. Mansson R., Hansson M.J., Morota S., Uchino H., Ekdahl C.T., Elmer E. Re-evaluation of mitochondrial permeability transition as a primary neuroprotective target of minocycline. Neurobiol. Dis. 2007, 25:198-205.
39. Mehindate K., Sahlas D.J., Frankel D., Mawal Y., Liberman A., Corcos J., Dion S., Schipper H.M. Proinflammatory cytokines promote glial heme oxygenase-1 expression and mitochondrial iron deposition: implications for multiple sclerosis. J. Neurochem. 2001, 77:1386-1395.
40. Metz L.M., Zhang Y.Y., Yeung M., Party D.G., Bell R.B., Stoian C.A., Yong V.W., Patten S.B., Duquette P., Antel J.P., Mitchell J.R. Minocycline reduces gadolinium-enhancing magnetic resonance imaging lesions in multiple sclerosis. Ann. Neurol. 2004, 55:756.
41. Metz L.M., Li D., Traboulsee A., Myles M.L., Duquette P., Godin J., Constantin M., Yong V.W., Investigators G.A.M.S. Glatiramer acetate in combination with minocycline in patients with relapsing-remitting multiple sclerosis: results of a Canadian, multicenter, double-blind, placebo-controlled trial. Mult. Scler. 2009, 15:1183-1194.
42. Nelissen I., Martens E., Van Den Steen P.E., Proost P., Ronsse I., Opdenakker G. Gelatinase B/matrix metalloproteinase-9 cleaves interferon-beta and is a target for immunotherapy. Brain 2003, 126:1371-1381.
43. Nessler S., Dodel R., Bittner A., Reuss S., Du Y.S., Hemmer B., Sommer N. Effect a minocycline in experimental autoimmune encephalomyelitis. Ann. Neurol. 2002, 52:689-690.
44. Neuhaus O., Farina C., Wekerle H., Hohlfeld R. Mechanisms of action of glatiramer acetate in multiple sclerosis. Neurology 2001, 56:702-708.
45. Neuhaus O., Strasser-Fuchs S., Fazekas F., Kieseier B.C., Niederwieser G., Hartung H.P., Archelos J.J. Statins as immunomodulators-comparison with interferon-beta 1b in MS. Neurology 2002, 59:990-997.
46. Nikodemova M., Watters J.J., Jackson S.J., Yang S.K., Duncan I.D. Minocycline down-regulates MHC II expression in microglia and macrophages through inhibition of IRF-1 and protein kinase C (PKC) (alpha/beta II). J. Biol. Chem. 2007, 282:15208-15216.
47. Nikodemova M., Lee J., Fabry Z., Duncan I.D. Minocycline attenuates experimental autoimmune encephalomyelitis in rats by reducing T cell infiltration into the spinal cord. J. Neuroimmunol. 2010, 219:33-37.
48. Paemen L., Martens E., Norga K., Masure S., Roets E., Hoogmartens J., Opdenakker G. The gelatinase inhibitory activity of tetracyclines and chemically modified tetracycline analogues as measured by a novel microtiter assay for inhibitors. Biochem. Pharmacol. 1996, 52:105-111.
49. Paintlia A.S., Paindia M.K., Singh I., Singh A.K. Combined medication of lovastatin with rolipram suppresses severity of experimental autoimmune encephalomyelitis. Exp. Neurol. 2008, 214:168-180.
50. Perlmutter L.J., Darvish M. Possible relationship of Chlamydia to multiple sclerosis. Med. Hypotheses 1983, 12:95-98.
51. Peterson J.W., Bo L., Mork S., Chang A., Trapp B.D. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann. Neurol. 2001, 50:389-400.
52. Popovic N., Schubart A., Goetz B.D., Zhang S.C., Linington C., Duncan I.D. Inhibition of autoimmune encephalomyelitis by a tetracycline. Ann. Neurol. 2002, 51:215-223.
53. Power C., Scot Henry S., Del Bigio M.R., Larsen P.H., Corbett D., Imai Y., Yong V.W., Peeling J. Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann. Neurol. 2003, 53:731-742.
54. Pozzilli C., Marinelli F., Romano S., Bagnato F. Corticosteroids treatment. J. Neurol. Sci. 2004, 223:47-51.
55. Pujol J., Junque C., Vendrell P., Grau J.M., Martivilalta J.L., Olive C., Gili J. Biological significance of iron-related magnetic-resonance-imaging changes in the brain. Arch. Neurol. 1992, 49:711-717.
56. Raivich G., Banati R. Brain microglia and blood-derived macrophages: molecular profiles and functional roles in multiple sclerosis and animal models of autoimmune demyelinating disease. Brain Res. Rev. 2004, 46:261-281.
57. Rovaris M., Filippi M. Interventions for the prevention of brain atrophy in multiple sclerosis-current status. CNS Drugs 2003, 17:563-575.
58. Ruggieri M., Pica C., Lia A., Zimatore G.B., Modesto M., Di Liddo E., Specchio L.M., Livrea P., Trojano M., Avolio C. Combination treatment of Glatiramer Acetate and Minocycline affects phenotype expression of blood monocyte-derived dendritic cells in Multiple Sclerosis patients. J. Neuroimmunol. 2008, 197:140-146.
59. Saivin S., Houin G. Clinical pharmacokinetics of doxycycline and minocycline. Clin. Pharmacokinet. 1988, 15:355-366.
60. Sela M., Teitelbaum D. Glatiramer acetate in the treatment of multiple sclerosis. Expert Opin. Pharmacother. 2001, 2:1149-1165.
61. Sorensen P.S., Mellgren S.I., Svenningsson A., Elovaara I., Frederiksen J.L., Beiske A.J., Myhr K.M., Seaard L.V., Olsen I.C., Sandberg-Wollheim M. NORdic, trial of oral Methylprednisolone as add-on therapy to Interferon beta-1a for treatment of relapsing-remitting Multiple Sclerosis (NORMIMS study): a randomised, placebo-controlled trial. Lancet Neurol. 2009, 8:519-529.
62. Sriram S., Stratton C.W., Yao S., Tharp A., Ding L., Bannan J.D., Mitchell W.M. Chlamydia pneumoniae infection of the central nervous system in multiple sclerosis. Ann. Neurol. 1999, 46:6-14.
63. Stahnke T., Stadelmann C., Netzler A., Bruck W., Richter-Landsberg C. Differential upregulation of heme oxygenase-1 (HSP32) in glial cells after oxidative stress and in demyelinating disorders. J. Mol. Neurosci. 2007, 32:25-37.
64. Stanislaus R., Pahan K., Singh A.K., Singh I. Amelioration of experimental allergic encephalomyelitis in Lewis rats by lovastatin. Neurosci. Lett. 1999, 269:71-74.
65. Stanislaus R., Singh A.K., Singh I. Lovastatin treatment decreases mononuclear cell infiltration into the CNS of Lewis rats with experimental allergic encephalomyelitis. J. Neurosci. Res. 2001, 66:155-162.
66. Stanislaus R., Gilg A.G., Singh A.K., Singh I. Immunomodulation of experimental autoimmune encephalomyelitis in the Lewis rats by Lovastatin. Neurosci. Lett. 2002, 333:167-170.
67. Stirling D.P., Khodarahmi K., Liu J., McPhail L.T., McBride C.B., Steeves J.D., Ramer M.S., Tetzlaff W. Minocycline treatment reduces delayed oligodendrocyte death, attenuates axonal dieback, and improves functional outcome after spinal cord injury. J. Neurosci. 2004, 24:2182-2190.
68. Stone M., Fortin P.R., Pacheco-Tena C., Inman R.D. Should tetracycline treatment be used more extensively for rheumatoid arthritis? Metaanalysis demonstrates clinical benefit with reduction in disease activity. J. Rheumatol. 2003, 30:2112-2122.
69. Sturkenboom M., Meier C.R., Jick H., Stricker B.H.C. Minocycline and lupuslike syndrome in acne patients. Arch. Intern. Med. 1999, 159:493-497.
70. Suzuki H., Sugimura Y., Iwama S., Nobuaki O., Nagasaki H., Arima H., Sawada M., Oiso Y. Minocycline prevents osmotic demyelination syndrome by inhibiting the activation of microglia. J. Am. Soc. Nephrol. 2010, 2:2090-2098.
71. Tikka T.M., Koistinaho J.E. Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. J. Immunol. 2001, 166:7527-7533.
72. Tikka T., Fiebich B.L., Goldsteins G., Keinanen R., Koistinaho J. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J. Neurosci. 2001, 21:2580-2588.
73. Tischner D., Reichardt H.M. Glucocorticoids in the control of neuroinflammation. Mol. Cell. Endocrinol. 2007, 275:62-70.
74. Tourbah A., Lyon-Caen O. Interferons in multiple sclerosis: ten years' experience. Biochimie 2007, 89:899-902.
75. Trapp B.D., Ransohoff R.M., Fisher E., Rudick R.A. Neurodegeneration in multiple sclerosis: relationship to neurological disability. Neuroscientist 1999, 5:48-57.
76. Tselis A., Perumal J., Caon C., Hreha S., Ching W., Din M., Van Stavern G., Khan O. Treatment of corticosteroid refractory optic neuritis in multiple sclerosis patients with intravenous immunoglobulin. Eur. J. Neurol. 2008, 15:1163-1167.
77. Tullman M.J., Lublin F.D. Combination therapy in multiple sclerosis. Curr. Neurol. Neurosci. Rep. 2005, 5:245-248.
78. Virley D.J. Developing therapeutics for the treatment of multiple sclerosis. NeuroRx 2005, 2:638-649.
79. Wang X., Zhu S., Drozda M., Zhang W.H., Stavrovskaya I.G., Cattaneo E., Ferrante R.J., Kristal B.S., Friedlander R.M. Minocycline inhibits caspase-independent and -dependent mitochondrial cell death pathways in models of Huntington's disease. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:10483-10487.
80. Wilkins A., Nikodemova M., Compston A., Duncan I. Minocycline attenuates nitric oxide-mediated neuronal and axonal destruction in vitro. Neuron Glia Biol. 2004, 1:297-305.
81. Wu D.C., Jackson-Lewis V., Vila M., Tieu K., Teismann P., Vadseth C., Choi D.K., Ischiropoulos H., Przedborski S. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 2002, 22:1763-1771.
82. Xue M.Z., Mikliaeva E.I., Casha S., Zygun D., Demchuk A., Yong V.W. Improving outcomes of neuroprotection by minocycline guides from cell culture and intracerebral hemorrhage in mice. Am. J. Pathol. 2010, 176:1193-1202.
83. Yamaguchi H., Haranaga S., Widen R., Friedman H., Yamamoto Y. Chlamydia pneumoniae infection induces differentiation of monocytes into macrophages. Infect. Immun. 2002, 70:2392-2398.
84. Yong V.W. Differential mechanisms of action of interferon-beta and glatiramer acetate in MS. Neurology 2002, 59:802-808.
85. Yong V.W. Prospects for neuroprotection in multiple sclerosis. Front. Biosci. 2004, 9:864-872.
86. Yong V.W., Power C., Forsyth P., Edwards D.R. Metalloproteinases in biology and pathology of the nervous system. Nat. Rev. Neurosci. 2001, 2:502-511.
87. Yong V.W., Wells J., Giuliani F., Casha S., Power C., Metz L.M. The promise of minocycline in neurology. Lancet Neurol. 2004, 3:744-751.
88. Youssef S., Stuve O., Patarroyo J.C., Ruiz P.J., Radosevich J.L., Hur E.M., Bravo M., Mitchell D.J., Sobel R.A., Steinman L., Zamvil S.S. The HMG-CoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease. Nature 2002, 420:78-84.
89. Yrjanheikki J., Keinanen R., Pellikka M., Hokfelt T., Koistinaho J. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:15769-15774.
90. Zabad R.K., Metz L.M., Todoruk T.R., Zhang Y., Mitchel J.R., Yeung M., Patry D.G., Bell R.B., Yong V.W. The clinical response to minocycline in multiple sclerosis is accompanied by beneficial immune changes: a pilot study. Mult. Scler. 2007, 13:517-526.
91. Zhang Y., Metz L.M., Yong V.W., Bell R.B., Yeung M., Patry D.G., Mitchell J.R. Pilot study of minocycline in relapsing-remitting multiple sclerosis. Can. J. Neurol. Sci. 2008, 35:185-191.
92. Zhang Y., Metz L.M., Yong V.W., Mitchell J.R. 3 T deep gray matter T2 hypointensity correlates with disability over time in stable relapsing-remitting multiple sclerosis: a 3-year pilot study. J. Neurol. Sci. 2010, 297:76-81.