Inhibiting effect of minocycline on the regeneration of peripheral nerves

Developmental Neurobiology

Volumn 67, Issue 10, 2007, Pages 1382-1395

  Keilhoff, Gerburg ^a   Langnaese, Kristina ^a   Wolf, Gerald ^a   Fansa, Hisham ^b  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b OWL University   (Germany)

Author keywords

Matrix metalloproteinases; Minocycline; Nerve regeneration; NOS; Wallerian degeneration

Indexed keywords

GELATINASE A; GELATINASE B; INDUCIBLE NITRIC OXIDE SYNTHASE; MINOCYCLINE; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; DEGENERATIVE DISEASE; ELECTRON MICROSCOPY; ENZYME INDUCTION; FEMALE; IMMUNOHISTOCHEMISTRY; INHIBITION KINETICS; MACROPHAGE; MACROPHAGE ACTIVATION; MICROENVIRONMENT; MORPHOLOGY; MORPHOMETRICS; NERVE DEGENERATION; NERVE INJURY; NERVE REGENERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL NERVE; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVASCULARIZATION; SCHWANN CELL; SCIATIC NERVE;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CHEMOTAXIS, LEUKOCYTE; EXTRACELLULAR MATRIX; FEMALE; GROWTH CONES; GROWTH INHIBITORS; MACROPHAGES; MATRIX METALLOPROTEINASES; MICROSCOPY, ELECTRON, TRANSMISSION; MINOCYCLINE; MYELIN SHEATH; NERVE REGENERATION; PERIPHERAL NERVES; PHAGOCYTOSIS; RATS; RATS, WISTAR; SCHWANN CELLS; SCIATIC NEUROPATHY; WALLERIAN DEGENERATION;

EID: 34547784473     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.20384     Document Type: Article

References (48)

1. Amin AR, Patel RN, Thakker GD, Lowenstein CJ, Attur MG, Abramson SB. 1996. Post-transcriptional regulation of inducible nitric oxide synthase mRNA in murine macrophages by doxycycline and chemically modified tetracyclines. FEBS Lett 410:259-264.
2. Best T, Mackinnon SE, Midha R, Hunter D, Evans P. 1999. Revascularization of peripheral nerve autografts and allografts. Plast Reconstr Surg 104:152-160.
3. Blum D, Chtarto A, Tenenbaum L, Brotchi J, Levivier M. 2004. Clinical potential of minocycline for neurodegenerative disorders. Neurobiol Dis 17:359-366.
4. Bouhy D, Malgrange B, Multon S, Poirrier AL, Scholtes F, Schoenen J, Franzen R. 2006. Delayed GM-CSF treatment stimulates axonal regeneration and functional recovery in paraplegic rats via increased BDNF expression by endogenous macrophages. FASEB J 20:1239-1241.
5. Chakraborti S, Mandal M, Das S, Mandal A, Chakraborti T. 2003. Regulation of matrix metalloproteinases: An overview. Mol Cell Biochem 253:269-285.
6. Conti CG, Rostami A, Scarpini E, Baron P, Galimberti D, Bresolin N, Contri M, et al. 2004. Inducible nitric oxide synthase (iNOS) in immune-mediated demyelination and Wallerian degeneration of the rat peripheral nervous system. Exp Neurol 187:350-358.
7. Diguet E, Gross CE, Tison F, Bezard E. 2004. Rise and fall of minocycline in neuroprotection: Need to promote publication of negative results. Exp Neurol 189:1-4.
8. Fansa H, Schneider W, Keilhoff G. 2001. Revascularization of tissue engineered nerve grafts and invasion of macrophages. Tissue Eng 7:519-524.
9. Ferguson TA, Muir D. 2000. MMP-2 and MMP-9 increase the neurite-promoting potential of Schwann cell basal laminae and are upregulated in degenerated nerve. Mol Cell Neurosci 16:157-176.
10. Filbin MT. 2006. How inflammation promotes regeneration. Nat Neurosci 9:715-717.
11. Giuliani F, Hader W, Yong VW. 2005. Minocycline attenuates T cell and microglia activity to impair cytokine production in T cell-microglia interaction. J Leukoc Biol 78:135-143.
12. Griffin JW, George EB, Chaudhry V. 1996. Wallerian degeneration in peripheral nerve disease. Baillieres Clin Neurol 5:65-75.
13. Guix FX, Uribesalgo I, Coma M, Munoz FJ. 2005. The physiology and pathophysiology of nitric oxide in the brain. Prog Neurobiol 76:126-152.
14. Hains BC, Waxman SG. 2006. Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J Neurosci 26:4308-4317.
15. Hodl AK, Bonelli RM. 2005. Huntington's disease and minocycline. Mov Disord 20:510-511.
16. Höke A, Sun HS, Gordon T, Zochodne DW. 2001. Do denervated peripheral nerve trunks become ischemic? The impact of chronic denervation on vasa nervorum. Exp Neurol 172:398-406.
17. Hughes PM, Wells GMA, Perry H, Brown MC, Miller KM. 2002. Comparison of matrix metalloproteinase expression during Wallerian degeneration in the central and peripheral nervous systems. Neuroscience 113:273-287.
18. Ide C. 1996. Peripheral nerve regeneration. Neurosci Res 25:101-121.
19. Keilhoff G, Fansa H, Wolf G. 2003. Nitric oxide synthase, an essential factor in peripheral nerve regeneration. Cell Mol Biol 49:885-897.
20. Kenagy RD, Hart CE, Stetler-Stevenson WG, Clowes AW. 1997. Primate smooth muscle cell migration from aortic explants is mediated by endogenous platelet-derived growth factor and basic fibroblast growth factor acting through matrix metalloproteinases 2 and 9. Circulation 96:3555-3560.
21. Krady JK, Basu A, Allen CM, Xu Y, LaNoue KF, Gardner TW, Levison SW. 2005. Minocycline reduces proinflammatory cytokine expression, microglia activation, and caspase-3 activation in a rodent model of diabetic retinopathy. Diabetes 54:1559-1565.
22. Levy D, Hoke A, Zochodne DW. 1999. Local expression of inducible nitric oxide synthase in an animal model of neuropathic pain. Neurosci Lett 260:207-209.
23. Lovdahl C, Thyberg J, Hultgardh-Nilsson A. 2000. The synthetic metalloproteinase inhibitor batmastat suppresses injury-induced phosphorylation of MAP kinase ERK1/ERK2 and phenotypic modification of arterial smooth muscle cells in vitro. J Vasc Res 37:345-354.
24. Lu X, Richardson PM. 1991. Inflammation near the nerve cell body enhances axonal regeneration. J Neurosci 11:972-978.
25. Myers RR, Sekiguchi Y, Kikuchi S, Scott B, Medicherly S, Protter A, Campana WM. 2003. Inhibition of p38 MAP kinase activity enhances axonal regeneration. Exp Neurol 184:606-614.
26. Osinsky SP, Ganusevich II, Bubanovskaya LN, Valkanovskaya NV, Kovelskaya AV, Sergienko TK, Zimina SV. 2005. Hypoxia level and matrix metalloproteinases-2 and -9 activity in Lewis lung carcinoma: Correlation with metastasis. Exp Oncol 27: 202-205.
27. Platt CI, Krekoski CA, Ward RV, Edwards DR, Gavrilovic J. 2003. Extracellular matrix and matrix metalloproteinases in sciatic nerve. J Neurosci Res 74:417-429.
28. Pontieri FE, Ricci A, Pellicano C, Benincasa D, Buttarelli FR. 2005. Minocycline in amyotrophic lateral sclerosis: A pilot Study. Neurol Sci 26:285-287.
29. Raghavendra V, Tanga F, DeLeo JA. 2003. Inhibition of microglial activation attenuates the development but not existing hypersensitivity in a rat model of neuropathy. J Pharmacol Exp Ther 306:624-630.
30. Schwartz M, Yoles E. 2005. Macrophages and dendritic cells treatment of spinal cord injury: From the bench to the clinic. Acta Neurochir Suppl 93:147-150.
31. Schwartz M, Yoles E. 2006. Immune-based therapy for spinal cord repair: Autologous macrophages and beyond. J Neurotrauma 23:360-370.
32. Shubayev VI, Angert M, Dolkes J, Campana WM, Palenscar K, Myers RR. 2006. TNFα-induced MMP-9 promotes macrophage recruitment into injured peripheral nerve. Mol Cell Neurosci 31:407-415.
33. Smilack JD. 1999. The tetracyclines. Mayo Clin Proc 74: 727-729.
34. Stirling DP, Koochesfahani KM, Steeves JD, Tetzlaff W. 2005. Minocycline as a neuroprotective agent. Neuroscientist 11:308-322.
35. Stoll G, Müller HW. 1999. Nerve injury, axonal degeneration and neuronal regeneration: Basic insights. Brain Pathol 9:313-325.
36. Tikka T, Fiebich BL, Goldsteins G, Keinänen R, Koistinaho J. 2001. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 21:2580-2588.
37. Tsuji M, Wilson MA, Lange MS, Johnston MV. 2004. Minocycline worsens hypoxic-ischemic brain injury in a neonatal mouse model. Exp Neurol 189:58-65.
38. Wells JE, Hurlbert RJ, Fehlings MG, Yong VW. 2003. Neuroprotection by minocycline facilitates significant recovery from spinal cord injury in mice. Brain 126:1628-1637.
39. Xu L, Fagan SC, Waller JL, Edwards D, Borlongan CV, Zheng J, Hill WD, et al. 2004. Low dose intravenous minocycline is neuroprotective after middle artery occlusion-reperfusion in rats. BMC Neurol 4:7.
40. Yao JS, Chen Y, Zhai W, Xu K, Young WL, Yang GY. 2004. Minocycline exerts multiple inhibitory effects on vascular endothelial growth factor-unduced smooth muscle cell migration. Circ Res 95:364-371.
41. Yin Y, Cui Q, Li Y, Irwin N, Fischer D, Harvey AR, Benowitz LI. 2003. Macrophage-derived factors stimulate optic nerve regeneration. J Neurosci 23:2284-2293.
42. Yin Y, Henzl MT, Lorber B, Nakazawa T, Thomas TT, Jiang F, Langer R, Benowitz LI. 2006. Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells. Nat Neurosci 9:843-852.
43. Yong VW, Wells J, Giuliani F, Casha S, Power C, Metz LM. 2004. The promise of minocycline in neurology. Lancet Neurol 3:744-751.
44. Yrjanheikki J, Keinanen R, Pellikka M, Hokfelt T, Koistinaho J. 1998. Tetracyclines inhibit microglia activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci USA 95:15769-15774.
45. Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan PH, Koistinaho J. 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.
46. Zemke D, Majid A. 2004. The potential of minocycline for neuroprotection in human neurologic disease. Clin Neuropharmacol 27:293-298.
47. Zochodne DW, Levy D. 2005. Nitric oxide in damage, disease and repair of the peripheral nervous system. Cell Mol Biol 51:255-267.
48. Zuo YX, Tracy DJ, Geczy C. 2005. Upregulation of matrix metalloproteinases following nerve injury is not mediated by mast cell activation. Neuroimmunomodulation 12:211-219.