Repurposing an old drug to improve the use and safety of tissue plasminogen activator for acute ischemic stroke: Minocycline

Reviews in Neurological Diseases

Volumn 7, Issue SUPPL. 1, 2010, Pages

  Hess, David C ^a   Fagan, Susan C ^a,b  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Acute ischemic stroke; Minocycline; MMP 9; PARP 1; Tissue plasminogen activator

Indexed keywords

DOXYCYCLINE; GELATINASE B; MINOCYCLINE; POLY(ADENOSINE DIPHOSPHATE RIBOSE); TETRACYCLINE; TISSUE PLASMINOGEN ACTIVATOR; PLASMINOGEN ACTIVATOR;

ALLERGIC ENCEPHALOMYELITIS; ARTHRITIS; BRAIN ISCHEMIA; CLINICAL TRIAL; COMPUTER ASSISTED TOMOGRAPHY; DIFFUSION WEIGHTED IMAGING; DRUG HALF LIFE; DRUG INHIBITION; DRUG SAFETY; DRUG TOLERABILITY; HUMAN; NEUROPROTECTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PERIODONTAL DISEASE; RECANALIZATION; REVIEW; RHEUMATOID ARTHRITIS; ANIMAL; BRAIN; CLINICAL TRIAL (TOPIC); DRUG DEVELOPMENT; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; PROCEDURES; STROKE; TRENDS;

ANIMALS; BRAIN; CLINICAL TRIALS AS TOPIC; DRUG DISCOVERY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MATRIX METALLOPROTEINASE 9; MINOCYCLINE; PLASMINOGEN ACTIVATORS; STROKE;

EID: 77955599953     PISSN: 15452913     EISSN: None     Source Type: Journal    
DOI: 10.3909/rind7S1S0002     Document Type: Review

References (66)

1. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. N Engl J Med. 1995;333:1581-1587.
2. Reeves MJ, Arora S, Broderick JP, et al; Paul Coverdell Prototype Registries Writing Group. Acute stroke care in the US: results from 4 pilot prototypes of the Paul Coverdell National Acute Stroke Registry. Stroke. 2005;36:1232-1240.
3. Kleindorfer D, Xu Y, Moomaw CJ, et al. US geographic distribution of rt-PA utilization by hospital for acute ischemic stroke. Stroke. 2009;40:3580-3584.
4. Hacke W, Kaste M, Bluhmki E, et al. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med. 2008;359:1317-1329.
5. Del Zoppo GJ, Saver JL, Jauch EC, Adams HP Jr. Expansion of the time window for treatment of acute ischemic stroke with intravenous tissue plasminogen activator: a science advisory from the American Heart Association/American Stroke Association. Stroke. 2009;40:2945-2948.
6. Smith WS, Sung G, Starkman S, et al. Safety and efficacy of mechanical embolectomy in acute ischemic stroke: results of the MERCI trial. Stroke. 2005;36:1432-1438. (Pubitemid 40967507)
7. Bose A, Henkes H, Alfke K, et al. The Penumbra System: a mechanical device for the treatment of acute stroke due to thromboembolism. AJNR Am J Neuroradiol. 2008;29:1409-1413.
8. Soares BP, Chien JD, Wintermark M. MR and CT monitoring of recanalization, reperfusion, and penumbra salvage: everything that recanalizes does not necessarily reperfuse! Stroke. 2009;40:S24-S27.
9. De Silva DA, Fink JN, Christensen S, et al. Assessing reperfusion and recanalization as markers of clinical outcomes after intravenous thrombolysis in the echoplanar imaging thrombolytic evaluation trial (EPITHET). Stroke. 2009;40:2872-2874.
10. Ames A 3rd, Wright RL, Kowada M, et al. Cerebral ischemia. II. The no-reflow phenomenon. Am J Pathol. 1968;52:437-453.
11. del Zoppo GJ, Schmid-Schonbein GW, Mori E, et al. Polymorphonuclear leukocytes occlude capillaries following middle cerebral artery occlusion and reperfusion in baboons. Stroke. 1991;22:1276-1283.
12. Hallenbeck JM, Dutka AJ, Tanishima T, et al. Polymorphonuclear leukocyte accumulation in brain regions with low blood flow during the early postischemic period. Stroke. 1986;17:246-253. (Pubitemid 16125248)
13. Garcia JH, Liu KF, Yoshida Y, et al. Brain microvessels: factors altering their patency after the occlusion of a middle cerebral artery (Wistar rat). Am J Pathol. 1994;145:728-740. (Pubitemid 24285979)
14. Yemisci M, Gursoy-Ozdemir Y, Vural A, et al. Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery. Nat Med. 2009;15:1031-1037.
15. Astrup J, Symon L, Branston NM, Lassen NA. Cortical evoked potential and extracellular K+ and H+ at critical levels of brain ischemia. Stroke. 1977;8:51-57. (Pubitemid 8025387)
16. Molina CA, Saver JL. Extending reperfusion therapy for acute ischemic stroke: emerging pharmacological, mechanical, and imaging strategies. Stroke. 2005;36:2311-2320.
17. Wintermark M, Flanders AE, Velthuis B, et al. Perfusion-CT assessment of infarct core and penumbra: receiver operating characteristic curve analysis in 130 patients suspected of acute hemispheric stroke. Stroke. 2006;37:979-985.
18. Muir KW, Buchan A, von Kummer R, et al. Imaging of acute stroke. Lancet Neurol. 2006;5:755-768.
19. Alexandrov AV, Molina CA, Grotta JC, et al. Ultrasound-enhanced systemic thrombolysis for acute ischemic stroke. N Engl J Med. 2004;351:2170-2178. (Pubitemid 39507629)
20. Nicole O, Docagne F, Ali C, et al. The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling. Nat Med. 2001;7:59-64.
21. Brown DL, Barsan WG, Lisabeth LD, et al. Survey of emergency physicians about recombinant tissue plasminogen activator for acute ischemic stroke. Ann Emerg Med. 2005;46:56-60. (Pubitemid 40916897)
22. Projan SJ. Preclinical pharmacology of GAR- 936, a novel glycylcycline antibacterial agent. Pharmacotherapy. 2000;20:219S-223S; discussion 224S-228S.
23. Leyden JJ, McGinley KJ, Kligman AM. Tetracycline and minocycline treatment. Arch Dermatol. 1982;118:19-22.
24. Tilley BC, Alarcon GS, Heyse SP, et al. Minocycline in rheumatoid arthritis. A 48-week, double-blind, placebo-controlled trial. MIRA trial group. Ann Intern Med. 1995;122:81-89.
25. Yrjanheikki J, Keinanen R, Pellikka M, et al. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci U S A. 1998;95:15769-15774. (Pubitemid 29018775)
26. Yrjanheikki J, Tikka T, Keinanen R, et al. A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci U S A. 1999;96:13496-13500.
27. Wang CX, Yang T, Noor R, Shuaib A. Delayed minocycline but not delayed mild hypothermia protects against embolic stroke. BMC Neurol. 2002;2:2. (Pubitemid 38729088)
28. Wang CX, Yang T, Shuaib A. Effects of minocycline alone and in combination with mild hypothermia in embolic stroke. Brain Res. 2003;963:327-329. (Pubitemid 36126315)
29. Nagel S, Su Y, Horstmann S, et al. Minocycline and hypothermia for reperfusion injury after focal cerebral ischemia in the rat: effects on BBB breakdown and MMP expression in the acute and subacute phase. Brain Res. 2008;1188:198-206. (Pubitemid 350296055)
30. Yenari MA, Xu L, Tang XN, et al. Microglia potentiate damage to blood-brain barrier constituents: improvement by minocycline in vivo and in vitro. Stroke. 2006;37:1087-1093.
31. Fagan SC, Edwards DJ, Borlongan CV, et al. Optimal delivery of minocycline to the brain: implication for human studies of acute neuroprotection. Exp Neurol. 2004;186:248-251.
32. Xu L, Fagan SC, Waller JL, et al. Low dose intravenous minocycline is neuroprotective after middle cerebral artery occlusion-reperfusion in rats. BMC Neurol. 2004;4:7. (Pubitemid 38729097)
33. Machado LS, Sazonova IY, Kozak A, et al. Minocycline and tissue-type plasminogen activator for stroke: assessment of interaction potential. Stroke. 2009;40:3028-3033.
34. Murata Y, Rosell A, Scannevin RH, et al. Extension of the thrombolytic time window with minocycline in experimental stroke. Stroke. 2008;39:3372-3377.
35. Machado LS, Kozak A, Ergul A, et al. Delayed minocycline inhibits ischemia-activated matrix metalloproteinases 2 and 9 after experimental stroke. BMC Neurosci. 2006;7:56. (Pubitemid 44237000)
36. Gieseler A, Schultze AT, Kupsch K, et al. Inhibitory modulation of the mitochondrial permeability transition by minocycline. Biochem Pharmacol. 2009;77:888-896.
37. Haroon MF, Fatima A, Scholer S, et al. Minocycline, a possible neuroprotective agent in Leber's hereditary optic neuropathy (LHON): studies of cybrid cells bearing 11,778 mutation. Neurobiol Dis. 2007;28:237-250. (Pubitemid 350116596)
38. Theruvath TP, Zhong Z, Pediaditakis P, et al. Minocycline and N-methyl-4-isoleucine cyclosporin (NIM811) mitigate storage/reperfusion injury after rat liver transplantation through suppression of the mitochondrial permeability transition. Hepatology. 2008;47:236-246.
39. Alano CC, Kauppinen TM, Valls AV, Swanson RA. Minocycline inhibits poly(ADP-ribose) polymerase-1 at nanomolar concentrations. Proc Natl Acad Sci U S A. 2006;103:9685-9690.
40. Petrilli V, Herceg Z, Hassa PO, et al. Noncleavable poly(ADP-ribose) polymerase-1 regulates the inflammation response in mice. J Clin Invest. 2004;114:1072-1081. (Pubitemid 39578696)
41. Moroni F, Chiarugi A. Post-ischemic brain damage: targeting PARP-1 within the ischemic neurovascular units as a realistic avenue to stroke treatment. FEBS J. 2009;276:36-45.
42. Moroni F. Poly(ADP-ribose)polymerase 1 (PARP-1) and postischemic brain damage. Curr Opin Pharmacol. 2008;8:96-103. (Pubitemid 351168695)
43. Andrabi SA, Kim NS, Yu SW, et al. Poly(ADP-ribose) (PAR) polymer is a death signal. Proc Natl Acad Sci U S A. 2006;103:18308-18313.
44. David KK, Andrabi SA, Dawson TM, Dawson VL. Parthanatos, a messenger of death. Front Biosci. 2009;14:1116-1128.
45. Wang Y, Dawson VL, Dawson TM. Poly(ADP-ribose) signals to mitochondrial AIF: a key event in parthanatos. Exp Neurol. 2009;218:193-202.
46. Kauppinen TM, Suh SW, Berman AE, et al. Inhibition of poly(ADP-ribose) polymerase suppresses inflammation and promotes recovery after ischemic injury. J Cereb Blood Flow Metab. 2009;29:820-829.
47. McCullough LD, Zeng Z, Blizzard KK, et al. Ischemic nitric oxide and poly (ADP-ribose) polymerase-1 in cerebral ischemia: male toxicity, female protection. J Cereb Blood Flow Metab. 2005;25:502-512. (Pubitemid 40503000)
48. Li J, McCullough LD. Sex differences in minocycline-induced neuroprotection after experimental stroke. J Cereb Blood Flow Metab. 2009;29:670-674.
49. Sumii T, Lo EH. Involvement of matrix metalloproteinase in thrombolysis-associated hemorrhagic transformation after embolic focal ischemia in rats. Stroke. 2002;33:831-836. (Pubitemid 34204013)
50. Montaner J, Rovira A, Molina CA, et al. Plasmatic level of neuroinflammatory markers predict the extent of diffusion-weighted image lesions in hyperacute stroke. J Cereb Blood Flow Metab. 2003;23:1403-1407. (Pubitemid 38018258)
51. Rosell A, Cuadrado E, Ortega-Aznar A, et al. MMP-9-positive neutrophil infiltration is associated to blood-brain barrier breakdown and basal lamina type IV collagen degradation during hemorrhagic transformation after human ischemic stroke. Stroke. 2008;39:1121-1126. (Pubitemid 351440679)
52. Montaner J, Alvarez-Sabin J, Molina CA, et al. Matrix metalloproteinase expression is related to hemorrhagic transformation after cardioembolic stroke. Stroke. 2001;32:2762-2767. (Pubitemid 33134461)
53. Heo JH, Kim SH, Lee KY, et al. Increase in plasma matrix metalloproteinase-9 in acute stroke patients with thrombolysis failure. Stroke. 2003;34:e48-e50.
54. Wang X, Lee SR, Arai K, et al. Lipoprotein receptor-mediated induction of matrix metalloproteinase by tissue plasminogen activator. Nat Med. 2003;9:1313-1317. (Pubitemid 37279856)
55. Horstmann S, Kalb P, Koziol J, et al. Profiles of matrix metalloproteinases, their inhibitors, and laminin in stroke patients: influence of different therapies. Stroke. 2003;34:2165-2170. (Pubitemid 37099830)
56. Kelly PJ, Morrow JD, Ning M, et al. Oxidative stress and matrix metalloproteinase-9 in acute ischemic stroke: the biomarker evaluation for antioxidant therapies in stroke (BEAT-Stroke) study. Stroke. 2008;39:100-104.
57. Montaner J, Molina CA, Monasterio J, et al. Matrix metalloproteinase-9 pretreatment level predicts intracranial hemorrhagic complications after thrombolysis in human stroke. Circulation. 2003;107:598-603. (Pubitemid 36176811)
58. Castellanos M, Sobrino T, Millan M, et al. Serum cellular fibronectin and matrix metalloproteinase- 9 as screening biomarkers for the prediction of parenchymal hematoma after thrombolytic therapy in acute ischemic stroke: a multicenter confirmatory study. Stroke. 2007;38:1855-1859. (Pubitemid 46847259)
59. Rifkin BR, Vernillo AT, Golub LM. Blocking periodontal disease progression by inhibiting tissue-destructive enzymes: a potential therapeutic role for tetracyclines and their chemically-modified analogs. J Periodontol. 1993;64:819-827.
60. Ashley RA. Clinical trials of a matrix metalloproteinase inhibitor in human periodontal disease. SDD clinical research team. Ann N Y Acad Sci. 1999;878:335-346.
61. Greenwald RA. Treatment of destructive arthritic disorders with MMP inhibitors. Potential role of tetracyclines. Ann N Y Acad Sci. 1994;732:181-198.
62. Brundula V, Rewcastle NB, Metz LM, et al. Targeting leukocyte MMPs and transmigration: minocycline as a potential therapy for multiple sclerosis. Brain. 2002;125:1297-1308. (Pubitemid 34587139)
63. Power C, Henry S, Del Bigio MR, et al. Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann Neurol. 2003;53:731-742. (Pubitemid 36622510)
64. Koistinaho M, Malm TM, Kettunen MI, et al. Minocycline protects against permanent cerebral ischemia in wild type but not in matrix metalloprotease-9- deficient mice. J Cereb Blood Flow Metab. 2005;25:460-467. (Pubitemid 40502995)
65. Brown DL, Desai KK, Vakili BA, et al. Clinical and biochemical results of the metalloproteinase inhibition with subantimicrobial doses of doxycycline to prevent acute coronary syndromes (MIDAS) pilot trial. Arterioscler Thromb Vasc Biol. 2004;24:733-738.
66. Lampl Y, Boaz M, Gilad R, et al. Minocycline treatment in acute stroke: an open-label, evaluator-blinded study. Neurology. 2007;69:1404-1410. (Pubitemid 47511461)