Influence of methylene blue on microglia-induced inflammation and motor neuron degeneration in the SOD1G93A model for ALS

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Dibaj, Payam ^a   Zschüntzsch, Jana ^b   Steffens, Heinz ^a,b,c   Scheffel, Jörg ^b   Göricke, Bettina ^b   Weishaupt, Jochen H ^b,d   Le Meur, Karim ^a,b,e   Kirchhoff, Frank ^a,e   Hanisch, Uwe Karsten ^b   Schomburg, Eike D ^b   Neusch, Clemens ^b,d  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^d UNIVERSITY OF ULM   (Germany)

^e SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

METHYLENE BLUE; NITRIC OXIDE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR HORN CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ACTIVITY; CELL FUNCTION; CELL SURVIVAL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE COURSE; DOSE RESPONSE; FEMALE; GLIOSIS; IN VITRO STUDY; IN VIVO STUDY; LASER MICROSCOPY; LOCOMOTION; MALE; MICROGLIA; MOTONEURON; MOTOR DYSFUNCTION; MOUSE; MYELITIS; NERVE CELL DEGENERATION; NEUROPROTECTION; NONHUMAN; ONSET AGE; TIME LAPSE 2 PHOTON LASER SCANNING MICROSCOPY; TRANSGENIC MOUSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL SURVIVAL; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; INFLAMMATION; MALE; METHYLENE BLUE; MICE; MICROGLIA; MOTOR ACTIVITY; MOTOR NEURONS; SUPEROXIDE DISMUTASE; TIME FACTORS;

EID: 84865415329     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043963     Document Type: Article

References (57)

1. Boillee S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, et al. (2006) Onset and Progression in Inherited ALS Determined by Motor Neurons and Microglia. Science 312: 1389-1392.
2. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, et al. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362: 59-62.
3. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, et al. (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264: 1772-1775.
4. Wong PC, Borchelt DR, (1995) Motor neuron disease caused by mutations in superoxide dismutase 1. Curr Opin Neurol 8: 294-301.
5. Boillee S, Vande Velde C, Cleveland DW, (2006) ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52: 39-59.
6. Neusch C, Bahr M, Schneider-Gold C, (2007) Glia cells in amyotrophic lateral sclerosis: new clues to understanding an old disease? Muscle Nerve 35: 712-724.
7. Chattopadhyay M, Valentine JS, (2009) Aggregation of copper-zinc superoxide dismutase in familial and sporadic ALS. Antioxid Redox Signal 11: 1603-1614.
8. Synofzik M, Fernandez-Santiago R, Maetzler W, Schols L, Andersen PM, (2010) The human G93A SOD1 phenotype closely resembles sporadic amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 81: 764-767.
9. Beers DR, Henkel JS, Xiao Q, Zhao W, Wang J, et al. (2006) Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proc Natl Acad Sci U S A 103: 16021-16026.
10. Lobsiger CS, Cleveland DW, (2007) Glial cells as intrinsic components of non-cell-autonomous neurodegenerative disease. Nat Neurosci 10: 1355-1360.
11. Yamanaka K, Chun SJ, Boillee S, Fujimori-Tonou N, Yamashita H, et al. (2008) Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci 11: 251-253.
12. Yamanaka K, Boillee S, Roberts EA, Garcia ML, McAlonis-Downes M, et al. (2008) Mutant SOD1 in cell types other than motor neurons and oligodendrocytes accelerates onset of disease in ALS mice. Proc Natl Acad Sci U S A 105: 7594-7599.
13. Nimmerjahn A, Kirchhoff F, Helmchen F, (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308: 1314-1318.
14. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, et al. (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8: 752-758.
15. Hanisch UK, Kettenmann H, (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10: 1387-1394.
16. Dibaj P, Nadrigny F, Steffens H, Scheller A, Hirrlinger J, et al. (2010) NO mediates microglial response to acute spinal cord injury under ATP control in vivo. Glia 58: 1133-1144.
17. Dibaj P, Steffens H, Nadrigny F, Neusch C, Kirchhoff F, et al. (2010) Long-lasting post-mortem activity of spinal microglia in situ in mice. J Neurosci Res 88: 2431-2440.
18. Duan Y, Sahley CL, Muller KJ, (2009) ATP and NO dually control migration of microglia to nerve lesions. Dev Neurobiol 69: 60-72.
19. Dibaj P, Steffens H, Zschuntzsch J, Nadrigny F, Schomburg ED, et al. (2011) In Vivo imaging reveals distinct inflammatory activity of CNS microglia versus PNS macrophages in a mouse model for ALS. PLoS One 6: e17910.
20. Oz M, Lorke DE, Hasan M, Petroianu GA (2009) Cellular and molecular actions of methylene blue in the nervous system. Med Res Rev.
21. Gura T, (2008) Hope in Alzheimer's fight emerges from unexpected places. Nat Med 14: 894.
22. Oz M, Lorke DE, Petroianu GA, (2009) Methylene blue and Alzheimer's disease. Biochem Pharmacol 78: 927-932.
23. Guegan C, Przedborski S, (2003) Programmed cell death in amyotrophic lateral sclerosis. J Clin Invest 111: 153-161.
24. Hegedus J, Putman CT, Gordon T, (2007) Time course of preferential motor unit loss in the SOD1 G93A mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 28: 154-164.
25. Dibaj P, Steffens H, Zschuntzsch J, Kirchhoff F, Schomburg ED, et al. (2011) In vivo imaging reveals rapid morphological reactions of astrocytes towards focal lesions in an ALS mouse model. Neurosci Lett 497: 148-151.
26. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, et al. (2000) Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20: 4106-4114.
27. Hirrlinger PG, Scheller A, Braun C, Quintela-Schneider M, Fuss B, et al. (2005) Expression of reef coral fluorescent proteins in the central nervous system of transgenic mice. Mol Cell Neurosci 30: 291-303.
28. Hegedus J, Putman CT, Gordon T, (2009) Progressive motor unit loss in the G93A mouse model of amyotrophic lateral sclerosis is unaffected by gender. Muscle Nerve 39: 318-327.
29. Kaiser M, Maletzki I, Hulsmann S, Holtmann B, Schulz-Schaeffer W, et al. (2006) Progressive loss of a glial potassium channel (KCNJ10) in the spinal cord of the SOD1 (G93A) transgenic mouse model of amyotrophic lateral sclerosis. J Neurochem 99: 900-912.
30. De Luca A, Pierno S, Liantonio A, Cetrone M, Camerino C, et al. (2003) Enhanced dystrophic progression in mdx mice by exercise and beneficial effects of taurine and insulin-like growth factor-1. J Pharmacol Exp Ther 304: 453-463.
31. Golumbek PT, Keeling RM, Connolly AM, (2007) Strength and corticosteroid responsiveness of mdx mice is unchanged by RAG2 gene knockout. Neuromuscul Disord 17: 376-384.
32. Liebetanz D, Hagemann K, von Lewinski F, Kahler E, Paulus W, (2004) Extensive exercise is not harmful in amyotrophic lateral sclerosis. Eur J Neurosci 20: 3115-3120.
33. Carreras I, Yuruker S, Aytan N, Hossain L, Choi JK, et al. (2011) Moderate exercise delays the motor performance decline in a transgenic model of ALS. Brain Res 1313: 192-201.
34. Saywell SA, Ford TW, Meehan CF, Todd AJ, Kirkwood PA, (2010) Electrophysiological and morphological characterization of propriospinal interneurons in the thoracic spinal cord. J Neurophysiol 105: 806-826.
35. Unal-Cevik I, Kilinc M, Gursoy-Ozdemir Y, Gurer G, Dalkara T, (2004) Loss of NeuN immunoreactivity after cerebral ischemia does not indicate neuronal cell loss: a cautionary note. Brain Res 1015: 169-174.
36. McPhail LT, McBride CB, McGraw J, Steeves JD, Tetzlaff W, (2004) Axotomy abolishes NeuN expression in facial but not rubrospinal neurons. Exp Neurol 185: 182-190.
37. van Rossum D, Hilbert S, Strassenburg S, Hanisch UK, Bruck W, (2008) Myelin-phagocytosing macrophages in isolated sciatic and optic nerves reveal a unique reactive phenotype. Glia 56: 271-283.
38. Regen T, van Rossum D, Scheffel J, Kastriti ME, Revelo NH, et al. (2011) CD14 and TRIF govern distinct responsiveness and responses in mouse microglial TLR4 challenges by structural variants of LPS. Brain Behav Immun 25: 957-970.
39. Dibaj P, Steffens H, Nadrigny F, Kirchhoff F, Schomburg ED, (2011) Purinergic activation of dorsal root ganglion neurones in vivo. Neurosci Lett 487: 107-109.
40. Duan Y, Haugabook SJ, Sahley CL, Muller KJ, (2003) Methylene blue blocks cGMP production and disrupts directed migration of microglia to nerve lesions in the leech CNS. J Neurobiol 57: 183-192.
41. Walter-Sack I, Rengelshausen J, Oberwittler H, Burhenne J, Mueller O, et al. (2009) High absolute bioavailability of methylene blue given as an aqueous oral formulation. Eur J Clin Pharmacol 65: 179-189.
42. Barbe C, Rochetaing A, Kreher P, (2002) Mechanisms underlying the coronary vasodilation in the isolated perfused hearts of rats submitted to one week of high carbon monoxide exposure in vivo. Inhal Toxicol 14: 273-285.
43. Kulkarni SK, Dhir A, (2007) Possible involvement of L-arginine-nitric oxide (NO)-cyclic guanosine monophosphate (cGMP) signaling pathway in the antidepressant activity of berberine chloride. Eur J Pharmacol 569: 77-83.
44. Boillee S, Lobsiger CS, (2008) [Glial cells not that supportive for motor neurons]. Med Sci (Paris) 24: 124-126.
45. Yamanaka K, Miller TM, McAlonis-Downes M, Chun SJ, Cleveland DW, (2006) Progressive spinal axonal degeneration and slowness in ALS2-deficient mice. Ann Neurol 60: 95-104.
46. Ozdinler PH, Benn S, Yamamoto TH, Guzel M, Brown RH Jr, et al. (2011) Corticospinal motor neurons and related subcerebral projection neurons undergo early and specific neurodegeneration in hSOD1G(3)A transgenic ALS mice. J Neurosci 31: 4166-4177.
47. Audet JN, Soucy G, Julien JP, (2012) Methylene blue administration fails to confer neuroprotection in two amyotrophic lateral sclerosis mouse models. Neuroscience 209: 136-143.
48. Lougheed R, Turnbull J, (2011) Lack of effect of methylene blue in the SOD1 G93A mouse model of amyotrophic lateral sclerosis. PLoS One 6: e23141.
49. Carre-Pierrat M, Lafoux A, Tanniou G, Chambonnier L, Divet A, et al. (2011) Pre-clinical study of 21 approved drugs in the mdx mouse. Neuromuscul Disord 21: 313-327.
50. Martinez JA, Francis GJ, Liu WQ, Pradzinsky N, Fine J, et al. (2008) Intranasal delivery of insulin and a nitric oxide synthase inhibitor in an experimental model of amyotrophic lateral sclerosis. Neuroscience 157: 908-925.
51. Necula M, Kayed R, Milton S, Glabe CG, (2007) Small molecule inhibitors of aggregation indicate that amyloid beta oligomerization and fibrillization pathways are independent and distinct. J Biol Chem 282: 10311-10324.
52. Yamashita M, Nonaka T, Arai T, Kametani F, Buchman VL, et al. (2009) Methylene blue and dimebon inhibit aggregation of TDP-43 in cellular models. FEBS Lett 583: 2419-2424.
53. Arai T, Hasegawa M, Nonoka T, Kametani F, Yamashita M, et al. (2010) Phosphorylated and cleaved TDP-43 in ALS, FTLD and other neurodegenerative disorders and in cellular models of TDP-43 proteinopathy. Neuropathology 30: 170-181.
54. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, et al. (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314: 130-133.
55. Braak H, Ludolph A, Thal DR, Del Tredici K, (2010) Amyotrophic lateral sclerosis: dash-like accumulation of phosphorylated TDP-43 in somatodendritic and axonal compartments of somatomotor neurons of the lower brainstem and spinal cord. Acta Neuropathol 120: 67-74.
56. O'Leary JL, Petty J, Harris AB, Inukai J, (1968) Supravital staining of mammalian brain with intra-arterial methylene blue followed by pressurized oxygen. Stain Technol 43: 197-201.
57. Peter C, Hongwan D, Kupfer A, Lauterburg BH, (2000) Pharmacokinetics and organ distribution of intravenous and oral methylene blue. Eur J Clin Pharmacol 56: 247-250.