Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: An [11C](R)-PK11195 positron emission tomography study

Neurobiology of Disease

Volumn 15, Issue 3, 2004, Pages 601-609

  Turner, M R ^a,b   Cagnin, A ^c   Turkheimer, F E ^b,d   Miller, C C J ^a   Shaw, C E ^a   Brooks, D J ^b,e   Leigh, P N ^a   Banati, R B ^b,d  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b HAMMERSMITH HOSPITAL   (United Kingdom)

^c UNIVERSITY OF PADOVA   (Italy)

^d IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Amyotrophic lateral sclerosis; Microglia; Motor neuron disease; PK11195; Positron emission tomography

Indexed keywords

CARBON 11; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE;

ADULT; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BINDING SITE; BRAIN; CELL ACTIVATION; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; HUMAN; MALE; MICROGLIA; MOTONEURON; MOTOR CORTEX; PATHOLOGY; PONS; POSITRON EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; THALAMUS;

EID: 1842471942     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2003.12.012     Document Type: Article

References (89)

1. Abrahams S., Goldstein L.H., Kew J.J.et al. Frontal lobe dysfunction in amyotrophic lateral sclerosis. A PET study. Brain. 119(Pt 6):1996;2105-2120.
2. Abrahams S., Leigh P.N., Harvey A., Vythelingum G.N., Grise D., Goldstein L.H. Verbal fluency and executive dysfunction in amyotrophic lateral sclerosis (ALS). Neuropsychologia. 38:2000;734-747.
3. Akiyama H., Nishimura T., Kondo H., Ikeda K., Hayashi Y., McGeer P.L. Expression of the receptor for macrophage colony stimulating factor by brain microglia and its upregulation in brains of patients with Alzheimer's disease and amyotrophic lateral sclerosis. Brain Res. 639:1994;171-174.
4. Al-Chalabi A., Leigh P.N. Recent advances in amyotrophic lateral sclerosis. Curr. Opin. Neurol. 13:2000;397-405.
5. Alexianu M.E., Kozovska M., Appel S.H. Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology. 57:2001;1282-1289.
6. Asanuma M., Nishibayashi-Asanuma S., Miyazaki I., Kohno M., Ogawa N. Neuroprotective effects of non-steroidal anti-inflammatory drugs by direct scavenging of nitric oxide radicals. J. Neurochem. 76:2001;1895-1904.
7. Banati R.B. Visualising microglial activation in vivo. Glia. 40:2002;206-217.
8. Banati R.B. Brain plasticity and microglia: is transsynaptic glial activation in the thalamus after limb denervation linked to cortical plasticity and central sensitisation? J. Physiol. (Paris). 96:2002;289-299.
9. Banati R.B., Gehrmann J., Kellner M., Holsboer F. Antibodies against microglia/brain macrophages in the cerebrospinal fluid of a patient with acute amyotrophic lateral sclerosis and presenile dementia. Clin. Neuropathol. 14:1995;197-200.
10. 11C](R)-PK11195 positron emission tomography imaging of activated microglia in vivo in Rasmussen's encephalitis. Neurology. 53:1999;2199-2203.
11. 3H]PK11195 binding to activated microglia. J. Neurocytol. 26:1997;77-82.
12. Banati R.B., Newcombe J., Gunn R.N.et al. The peripheral benzodiazepine binding site in the brain in multiple sclerosis: Quantitative in vivo imaging of microglia as a measure of disease activity. Brain. 123:2000;2321-2337.
13. Beaulieu J.M., Nguyen M.D., Julien J.P. Late onset death of motor neurons in mice overexpressing wild-type peripherin. J. Cell Biol. 147:1999;531-544.
14. 3H]PK 11195, an isoquinoline carboxamide derivative: kinetic studies and autoradiographic localization. J. Neurochem. 41:1983;1744-1750.
15. Borasio G.D., Robberecht W., Leigh P.N.et al. A placebo-controlled trial of insulin-like growth factor-I in amyotrophic lateral sclerosis. European ALS/IGF-I Study Group. Neurology. 51:1998;583-586.
16. Brooks, B.R., Miller, R.G., Swash, M., Munsat, T.L. El Escorial Revisited: Revised Criteria for the Diagnosis of Amyotrophic Lateral Sclerosis at http://www.wfnals.org/guidelines/1998elescorial/elescorial1998.htm.
17. Cagnin A., Brooks D.J., Kennedy A.M.et al. In-vivo measurement of activated microglia in dementia. Lancet. 358:2001;461-467.
18. 11C] (R)-PK11195-PET following herpes encephalitis reveals projected neuronal damage beyond the primary focal lesion. Brain. 124:2001;2014-2027.
19. Cedarbaum J.M., Stambler N., Malta E.et al. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J. Neurol. Sci. 169:1999;13-21.
20. Chan S., Shungu D.C., Douglas-Akinwande A., Lange D.J., Rowland L.P. Motor neuron diseases: comparison of single-voxel proton MR spectroscopy of the motor cortex with MR imaging of the brain. Radiology. 212:1999;763-769.
21. Chou S.M., Norris F.H. Amyotrophic lateral sclerosis: lower motor neuron disease spreading to upper motor neurons. Muscle Nerve. 16:1993;864-869.
22. Ciesielski-Treska J., Ulrich G., Chasserot-Golaz S.et al. Mechanisms underlying neuronal death induced by chromogranin A-activated microglia. J. Biol. Chem. 276:2001;13113-13120.
23. Cleveland D.W., Rothstein J.D. From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat. Rev. Neurosci. 2:2001;806-819.
24. 3H]PK 11195: anatomical and subcellular distribution. Brain Res. Bull. 18:1987;49-61.
25. Drachman D.B., Frank K., Dykes-Hoberg M.et al. Cyclooxygenase 2 inhibition protects motor neurons and prolongs survival in a transgenic mouse model of ALS. Ann. Neurol. 52:2002;771-778.
26. Eisen A., Kim S., Pant B. Amyotrophic lateral sclerosis (ALS): a phylogenetic disease of the corticomotoneuron? Muscle Nerve. 15:1992;219-224.
27. Ellis C.M., Simmons A., Jones D.K.et al. Diffusion tensor MRI assesses corticospinal tract damage in ALS. Neurology. 53:1999;1051-1058.
28. Ellis C.M., Suckling J., Amaro E. Jr.et al. Volumetric analysis reveals corticospinal tract degeneration and extramotor involvement in ALS. Neurology. 57:2001;1571-1578.
29. Engelhardt J.I., Tajti J., Appel S.H. Lymphocytic infiltrates in the spinal cord in amyotrophic lateral sclerosis. Arch. Neurol. 50:1993;30-36.
30. Flugel A., Bradl M., Kreutzberg G.W., Graeber M.B. Transformation of donor-derived bone marrow precursors into host microglia during autoimmune CNS inflammation and during the retrograde response to axotomy. J. Neurosci. Res. 66:2001;74-82.
31. 11C](R)-PK11195 PET imaging of microglial activation in multiple system atrophy. Neurology. 61:2003;686-689.
32. 11C]PK11195 and positron emission tomography in patients after ischemic stroke. NeuroReport. 11:2000;2957-2960.
33. Gunn R.N., Lammertsma A.A., Cunningham V.J. Parametric imaging of ligand-receptor interactions using a reference tissue model and cluster analysis. Carson R.E., Daube-Witherspoon M.E., Herscovitch P. Quanititative Functional Brain Imaging with Positron Emission Tomography. 1998;401-406 Academic Press, San Diego.
34. Gunn R.N., Lammertsma A.A., Hume S.P., Cunningham V.J. Parametric imaging of ligand-receptor binding in PET using a simplified reference region model. NeuroImage. 6:1997;279-287.
35. Hall E.D., Oostveen J.A., Gurney M.E. Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia. 23:1998;249-256.
36. Ince P.G., Evans J., Knopp M.et al. Corticospinal tract degeneration in the progressive muscular atrophy variant of ALS. Neurology. 60:2003;1252-1258.
37. Kawamata T., Akiyama H., Yamada T., McGeer P.L. Immunologic reactions in amyotrophic lateral sclerosis brain and spinal cord tissue. Am. J. Pathol. 140:1992;691-707.
38. Kew J., Leigh N. Dementia with motor neurone disease. Baillieres Clin. Neurol. 1:1992;611-626.
39. Kew J.J., Leigh P.N., Playford E.D.et al. Cortical function in amyotrophic lateral sclerosis. A positron emission tomography study. Brain. 116(Pt 3):1993;655-680.
40. Klegeris A., McGeer P.L. Cyclooxygenase and 5-lipoxygenase inhibitors protect against mononuclear phagocyte neurotoxicity. Neurobiol. Aging. 23:2002;787-794.
41. Kostic V., Jackson-Lewis V., de Bilbao F., Dubois-Dauphin M., Przedborski S. Bcl-2: prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis. Science. 277:1997;559-562.
42. Kriz J., Nguyen M., Julien J. Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis. Neurobiol. Dis. 10:2002;268.
43. Kriz J., Gowing G., Julien J.P. Efficient three-drug cocktail for disease induced by mutant superoxide dismutase. Ann. Neurol. 53:2003;429-436.
44. Kushner P.D., Stephenson D.T., Wright S. Reactive astrogliosis is widespread in the subcortical white matter of amyotrophic lateral sclerosis brain. J. Neuropathol. Exp. Neurol. 50:1991;263-277.
45. Kyriakis J.M., Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81:2001;807-869.
46. Lammertsma A.A., Hume S.P. Simplified reference tissue model for PET receptor studies. NeuroImage. 4:1996;153-158.
47. Latsoudis H., Karim N., Everall I.et al. Extra-motor cortical lesions in MND: an unbiased stereological estimation of the density of neurons, astrocytes and microglia by the optical dissector. Proceedings of the 10th International Symposium on ALS/MND, Vancouver:1999;. Abstract.
48. 11C]flumazenil. Brain. 123:2000;2289-2296.
49. Lomen-Hoerth C., Anderson T., Miller B. The overlap of amyotrophic lateral sclerosis and frontotemporal dementia. Neurology. 59:2002;1077-1079.
50. Ludolph A.C., Langen K.J., Regard M.et al. Frontal lobe function in amyotrophic lateral sclerosis: a neuropsychologic and positron emission tomography study. Acta Neurol. Scand. 85:1992;81-89.
51. Mariotti R., Bentivoglio M. Activation and response to axotomy of microglia in the facial motor nuclei of G93A superoxide dismutase transgenic mice. Neurosci. Lett. 285:2000;87-90.
52. Massman P.J., Sims J., Cooke N., Haverkamp L.J., Appel V., Appel S.H. Prevalence and correlates of neuropsychological deficits in amyotrophic lateral sclerosis. J. Neurol. Neurosurg. Psychiatry. 61:1996;450-455.
53. McGeer P.L., McGeer E.G. Glial cell reactions in neurodegenerative diseases: pathophysiology and therapeutic interventions. Alzheimer Dis. Assoc. Disord. 12(Suppl. 2):1998;S1-S6.
54. McGeer P.L., McGeer E.G. Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve. 26:2002;459-470.
55. McGeer P.L., Kawamata T., Walker D.G., Akiyama H., Tooyama I., McGeer E.G. Microglia in degenerative neurological disease. Glia. 7:1993;84-92.
56. Nagy D., Kato T., Kushner P.D. Reactive astrocytes are widespread in the cortical gray matter of amyotrophic lateral sclerosis. J. Neurosci. Res. 38:1994;336-347.
57. Neary D., Snowden J. Fronto-temporal dementia: nosology, neuropsychology, and neuropathology. Brain Cogn. 31:1996;176-187.
58. Obal I., Jakab J.S., Siklos L., Engelhardt J.I. Recruitment of activated microglia cells in the spinal cord of mice by ALS IgG. NeuroReport. 12:2001;2449-2452.
59. 11C]PK11195. Neurology. 55:2000;1052-1054.
60. Piao Y.S., Wakabayashi K., Kakita A.et al. Neuropathology with clinical correlations of sporadic amyotrophic lateral sclerosis: 102 autopsy cases examined between 1962 and 2000. Brain Pathol. 13:2003;10-22.
61. Pohl C., Block W., Traber F.et al. Proton magnetic resonance spectroscopy and transcranial magnetic stimulation for the detection of upper motor neuron degeneration in ALS patients. J. Neurol. Sci. 190:2001;21-27.
62. Pompl P.N., Ho L., Bianchi M., McManus T., Qin W., Pasinetti G.M. A therapeutic role for cyclooxygenase-2 inhibitors in a transgenic mouse model of amyotrophic lateral sclerosis. FASEB J. 17:2003;725-727.
63. Przedborski S., Dhawan V., Donaldson D.M.et al. Nigrostriatal dopaminergic function in familial amyotrophic lateral sclerosis patients with and without copper/zinc superoxide dismutase mutations. Neurology. 47:1996;1546-1551.
64. Raivich G., Jones L.L., Kloss C.U., Werner A., Neumann H., Kreutzberg G.W. Immune surveillance in the injured nervous system: T-lymphocytes invade the axotomized mouse facial motor nucleus and aggregate around sites of neuronal degeneration. J. Neurosci. 18:1998;5804-5816.
65. Raoul C., Estevez A.G., Nishimune H.et al. Motoneuron death triggered by a specific pathway downstream of Fas. potentiation by ALS-linked SOD1 mutations. Neuron. 35:2002;1067-1083.
66. Rathke-Hartlieb S., Schmidt V.C., Jockusch H., Schmitt-John T., Bartsch J.W. Spatiotemporal progression of neurodegeneration and glia activation in the wobbler neuropathy of the mouse. NeuroReport. 10:1999;3411-3416.
67. Robertson J., Beaulieu J.M., Doroudchi M.M., Durham H.D., Julien J.P., Mushynski W.E. Apoptotic death of neurons exhibiting peripherin aggregates is mediated by the proinflammatory cytokine tumor necrosis factor-alpha. J. Cell Biol. 155:2001;217-226.
68. Rowland L.P., Shneider N.A. Amyotrophic lateral sclerosis. N. Engl. J. Med. 344:2001;1688-1700.
69. Schulte-Mattler W.J., Muller T., Zierz S. Transcranial magnetic stimulation compared with upper motor neuron signs in patients with amyotrophic lateral sclerosis. J. Neurol. Sci. 170:1999;51-56.
70. Schwab C., Steele J.C., McGeer P.L. Neurofibrillary tangles of Guam Parkinson-dementia are associated with reactive microglia and complement proteins. Brain Res. 707:1996;196-205.
71. Shinsuke K., Shaw P., Wood-Allum C., Leigh P.N., Shaw C.E. Amyotrophic lateral sclerosis. Dickson D. Neurodegeneration: The Molecular Pathology of Dementia and Movement Disorders. 2003;350-368 International Society of Neuropathology, Neuropath Press, Basel.
72. 3H]PK11195 of spinal tract degeneration in amyotrophic lateral sclerosis. Acta Neuropathol. (Berl). 101:2001;75-78.
73. Swash M. Amyotrophic lateral sclerosis: a phylogenetic disease of the corticomotoneuron? Comments on the hypothesis. Muscle Nerve. 15:1992;226-228.
74. Takahashi H., Snow B.J., Bhatt M.H., Peppard R., Eisen A., Calne D.B. Evidence for a dopaminergic deficit in sporadic amyotrophic lateral sclerosis on positron emission scanning. Lancet. 342:1993;1016-1018.
75. Tikka T.M., Vartiainen N.E., Goldsteins G.et al. Minocycline prevents neurotoxicity induced by cerebrospinal fluid from patients with motor neurone disease. Brain. 125:2002;722-731.
76. Tortarolo M., Veglianese P., Calvaresi N.et al. Persistent activation of p38 mitogen-activated protein kinase in a mouse model of familial amyotrophic lateral sclerosis correlates with disease progression. Mol. Cell. Neurosci. 23:2003;180-192.
77. Troost D., Van den Oord J.J., Vianney de Jong J.M. Immunohistochemical characterization of the inflammatory infiltrate in amyotrophic lateral sclerosis. Neuropathol. Appl. Neurobiol. 16:1990;401-410.
78. Troost D., Claessen N., Van den Oord J.J., Swaab D.F., de Jong J.M. Neuronophagia in the motor cortex in amyotrophic lateral sclerosis. Neuropathol. Appl. Neurobiol. 19:1993;390-397.
79. Turkheimer F.E., Smith C.B., Schmidt K. Estimation of the number of "true" null hypotheses in multivariate analysis of neuroimaging data. NeuroImage. 13:2001;920-930.
80. Turner M.R., Leigh P.N. Positron emission tomography (PET) - its potential to provide surrogate markers in ALS. Amyotroph. Lateral Scler. Other Mot. Neuron Disord. 1(Suppl. 2):2000;S17-S22.
81. Turner M.R., Bakker M., Sham P., Shaw C.E., Leigh P.N., Al-Chalabi A. Prognostic modeling of therapeutic interventions in amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Other Mot. Neuron Disord. 3:2002;15-21.
82. Turner M.R., Parton M.J., Shaw C.E., Leigh P.N., Al Chalabi A. Prolonged survival in motor neuron disease: a descriptive study of the King's database 1990-2002. J. Neurol. Neurosurg. Psychiatry. 74:2003;995-997.
83. Urbanek K., Jansa P. Amyotrophic lateral sclerosis. Abnormal cellular inflammatory response. Arch. Neurol. 30:1974;186-187.
84. Van Den Bosch L., Tilkin P., Lemmens G., Robberecht W. Minocycline delays disease onset and mortality in a transgenic model of ALS. NeuroReport. 13:2002;1067-1070.
85. Weydt P., Weiss M.D., Moller T., Carter G.T. Neuro-inflammation as a therapeutic target in amyotrophic lateral sclerosis. Curr. Opin. Investig. Drugs. 3:2002;1720-1724.
86. Wisniewska K., Tytulska D. Morphologic manifestations of the "inflammation" in sclerosis lateralis amyotrophica and their biologic significance. Neuropatol. Pol. 4:1966;151-170.
87. Yasojima K., Tourtellotte W.W., McGeer E.G., McGeer P.L. Marked increase in cyclooxygenase-2 in ALS spinal cord: implications for therapy. Neurology. 57:2001;952-956.
88. Yermakova A., O'Banion M.K. Cyclooxygenases in the central nervous system: implications for treatment of neurological disorders. Curr. Pharm. Des. 6:2000;1755-1776.
89. Zhu S., Stavrovskaya I.G., Drozda M.et al. Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature. 417:2002;74-78.