In vivo imaging of glia activation using 1H-magnetic resonance spectroscopy to detect putative biomarkers of tissue epileptogenicity

Epilepsia

Volumn 53, Issue 11, 2012, Pages 1907-1916

  Filibian, Marta ^a,c   Frasca, Angelisa ^a   Maggioni, Daniela ^b   Micotti, Edoardo ^a   Vezzani, Annamaria ^a   Ravizza, Teresa ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF PAVIA   (Italy)

Author keywords

Astrocytes; Glutathione; Inflammation; Microglia; Neurodegeneration; Seizures; Status epilepticus

Indexed keywords

BIOLOGICAL MARKER; GLUTATHIONE; INOSITOL; LACTIC ACID; N ACETYLASPARTIC ACID; PROTEIN S100B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CHRONIC DISEASE; CONTROLLED STUDY; EPILEPTOGENESIS; GLIA; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LONGITUDINAL STUDY; MACROPHAGE ACTIVATION; METABOLITE; MICROGLIA; NERVE CELL LESION; NERVE DEGENERATION; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; PROGNOSIS; PROTON NUCLEAR MAGNETIC RESONANCE; RAT;

ANIMALS; BIOLOGICAL MARKERS; EPILEPSY; HIPPOCAMPUS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; NEUROGLIA; PROTONS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84869082704     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2012.03685.x     Document Type: Article

References (62)

1. Abe K, Nakanishi K, Saito H,. (2000) The possible role of endogenous glutathione as an anticonvulsant in mice. Brain Res 854: 235-238. (Pubitemid 30067682)
2. Bendotti C, Guglielmetti F, Tortarolo M, Samanin R, Hirst WD,. (2000) Differential expression of S100beta and glial fibrillary acidic protein in the hippocampus after kainic acid-induced lesions and mossy fiber sprouting in adult rat. Exp Neurol 161: 317-329. (Pubitemid 30136553)
3. Blumenfeld H, Klein JP, Schridde U, Vestal M, Rice T, Khera DS, Bashyal C, Giblin K, Paul-Laughinghouse C, Wang F, Phadke A, Mission J, Agarwal RK, Englot DJ, Motelow J, Nersesyan H, Waxman SG, Levin AR,. (2008) Early treatment suppresses the development of spike-wave epilepsy in a rat model. Epilepsia 49: 400-409. (Pubitemid 351294541)
4. Boer K, Spliet WG, van Rijen PC, Redeker S, Troost D, Aronica E,. (2006) Evidence of activated microglia in focal cortical dysplasia. J Neuroimmunol 173: 188-195.
5. Brand A, Richter-Landsberg C, Leibfritz D,. (1993) Multinuclear NMR studies on the energy metabolism of glial and neuronal cells. Dev Neurosci 15: 289-298. (Pubitemid 24258162)
6. Briellmann RS, Mark Wellard R, Masterton RA, Abbott DF, Berkovic SF, Jackson GD,. (2007) Hippocampal sclerosis: MR prediction of seizure intractability. Epilepsia 48: 315-323. (Pubitemid 46213884)
7. Bruce AJ, Baudry M,. (1995) Oxygen free radicals in rat limbic structures after kanate-induced seizures. Free Radical Biol Med 18: 993-1002.
8. Butler T, Ichise M, Teich AF, Gerard E, Osborne J, French J, Devinsky O, Kuzniecky R, Gilliam F, Pervez F, Provenzano F, Goldsmith S, Vallabhajosula S, Stern E, Silbersweig D,. (2011) Imaging inflammation in a patient with epilepsy due to focal cortical dysplasia. J Neuroimaging [Epub ahead of print]. Doi: 10.1111/j.1552-6569.2010.00572.x.
9. Colciaghi F, Finardi A, Frasca A, Balosso S, Nobili P, Carriero G, Locatelli D, Vezzani A, Battaglia G,. (2011) Status epilepticus-induced pathologic plasticity in a rat model of focal cortical dysplasia. Brain 134: 2828-2843.
10. Devi PU, Manocha A, Vohora D,. (2008) Seizures, antiepileptics, antioxidants and oxidative stress: an insight for researchers. Expert Opin Pharmacother 9: 3169-3177.
11. Doelken MT, Stefan H, Pauli E, Stadlbauer A, Struffert T, Engelhorn T, Richter G, Ganslandt O, Doerfler A, Hammen T,. (2008) (1)H-MRS profile in MRI positive- versus MRI negative patients with temporal lobe epilepsy. Seizure 17: 490-497.
12. Dringen R, Pfeiffer B, Hamprecht B,. (1999) Synthesis of the antioxidant glutathione in neurons: supply by astrocytes of CysGly as precursor for neuronal glutathione. J Neurosci 19: 562-569. (Pubitemid 29036007)
13. During MJ, Spencer DD,. (1993) Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 341: 1607-1610. (Pubitemid 23175242)
14. Ebisu T, Rooney WD, Graham SH, Weiner MW, Maudsley AA,. (1994) N-acetylaspartate as an in vivo marker of neuronal viability in kainate-induced status epilepticus: 1H magnetic resonance spectroscopic imaging. J Cereb Blood Flow Metab 14: 373-382.
15. Engel J,. (2011) Biomarkers in epilepsy: introduction. Biomark Med 5: 537-544.
16. Fernandes MJ, Dube C, Boyet S, Marescaux C, Nehlig A,. (1999) Correlation between hypermetabolism and neuronal damage during status epilepticus induced by lithium and pilocarpine in immature and adult rats. J Cereb Blood Flow Metab 19: 195-209. (Pubitemid 29284268)
17. Fisher SK, Novak JE, Agranoff BW,. (2002) Inositol and higher inositol phosphates in neural tissues: homeostasis, metabolism and functional significance. J Neurochem 82: 736-754.
18. Govindaraju V, Young K, Maudsley AA,. (2000) Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed 13: 129-153. (Pubitemid 30414704)
19. Gruetter R,. (1993) Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn Reson Med 29: 804-811. (Pubitemid 23182863)
20. Hammen T, Hildebrandt M, Stadlbauer A, Doelken M, Engelhorn T, Kerling F, Kasper B, Romstoeck J, Ganslandt O, Nimsky C, Blumcke I, Doerfler A, Stefan H,. (2008) Non-invasive detection of hippocampal sclerosis: correlation between metabolite alterations detected by (1)H-MRS and neuropathology. NMR Biomed 21: 545-552.
21. Hanisch UK, Kettenmann H,. (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10: 1387-1394. (Pubitemid 350014685)
22. Hetherington H,. (2011) Magnetic resonance spectroscopy. In, Chugany HT, (Ed.) Neuroimaging in epilepsy. Oxford University Press, New York, pp. 63-76.
23. Janaky R, Ogita K, Pasqualotto BA, Bains JS, Oja SS, Yoneda Y, Shaw CA,. (1999) Glutathione and signal transduction in the mammalian CNS. J Neurochem 73: 889-902. (Pubitemid 29395445)
24. Klitgaard H, Matagne A, Vanneste-Goemaere J, Margineanu DG,. (2002) Pilocarpine-induced epileptogenesis in the rat: impact of initial duration of status epilepticus on electrophysiological and neuropathological alterations. Epilpesy Res 51: 93-107. (Pubitemid 35283881)
25. Koh JY, Choi DW,. (1987) Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J Neurosci Methods 20: 83-90. (Pubitemid 17062742)
26. Koprowski H, Zheng YM, Heber-Katz E, Fraser N, Rorke L, Fu ZF, Hanlon C, Dietzschold B,. (1993) In vivo expression of inducible nitric oxide synthase in experimentally induced neurologic diseases. Proc Natl Acad Sci U S A 90: 3024-3027. (Pubitemid 23113550)
27. Levy DI, Sucher NJ, Lipton SA,. (1991) Glutathione prevents N-methyl-d-aspartate receptor-mediated neurotoxicity. NeuroReport 2: 345-347.
28. Lopez-Villegas D, Lenkinski RE, Wehrli SL, Ho WZ, Douglas SD,. (1995) Lactate production by human monocytes/macrophages determined by proton MR spectroscopy. Magn Reson Med 34: 32-38.
29. Mader I, Rauer S, Gall P, Klose U,. (2008) (1)H MR spectroscopy of inflammation, infection and ischemia of the brain. Eur J Radiol 67: 250-257.
30. Magistretti PJ,. (2009) Role of glutamate in neuron-glia metabolic coupling. Am J Clin Nutr 90: 875S-880S.
31. Mao H, Toufexis D, Wang X, Lacreuse A, Wu S,. (2007) Changes of metabolite profile in kainic acid induced hippocampal injury in rats measured by HRMAS NMR. Exp Brain Res 183: 477-485. (Pubitemid 350029364)
32. McDaniel SS, Wong M,. (2011) Therapeutic role of mammalian target of rapamycin (mTOR) inhibition in preventing epileptogenesis. Neurosci Lett 497: 231-239.
33. Mizuno S, Takahashi Y, Kato Z, Goto H, Kondo N, Hoshi H,. (2000) Magnetic resonance spectroscopy of tubers in patients with tuberous sclerosis. Acta Neurol Scand 102: 175-178. (Pubitemid 30645135)
34. Mueller SG, Laxer KD, Suhy J, Lopez RC, Flenniken DL, Weiner MW,. (2003) Spectroscopic metabolic abnormalities in mTLE with and without MRI evidence for mesial temporal sclerosis using hippocampal short-TE MRSI. Epilepsia 44: 977-980. (Pubitemid 36842191)
35. Naressi A, Couturier C, Devos JM, Janssen M, Mangeat C, de Beer R, Graveron-Demilly D,. (2001) Java-based graphical user interface for the MRUI quantitation package. MAGMA 12: 141-152. (Pubitemid 32510133)
36. Nehlig A,. (2011) Hippocampal MRI and other structural biomarkers: experimental approach to epileptogenesis. Biomark Med 5: 585-597.
37. Paxinos G, Watson C,. (2005) The rat brain in stereotaxic coordinates. Academic Press, New York.
38. Pfeuffer J, Tkac I, Provencher SW, Gruetter R,. (1999) Toward an in vivo neurochemical profile: quantification of 18 metabolites in short-echo-time (1)H NMR spectra of the rat brain. J Magn Reson 141: 104-120. (Pubitemid 129608901)
39. Pitkanen A, Lukasiuk K,. (2011) Molecular biomarkers of epileptogenesis. Biomark Med 5: 629-633.
40. Raps SP, Lai JC, Hertz L, Cooper AJ,. (1989) Glutathione is present in high concentrations in cultured astrocytes but not in cultured neurons. Brain Res 493: 398-401. (Pubitemid 19183160)
41. Ravizza T, Boer K, Redeker S, Spliet WG, van Rijen PC, Troost D, Vezzani A, Aronica E,. (2006) The IL-1beta system in epilepsy-associated malformations of cortical development. Neurobiol Dis 24: 128-143. (Pubitemid 44416213)
42. Ravizza T, Gagliardi B, Noé F, Boer K, Aronica E, Vezzani A,. (2008) Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol Dis 29: 142-160. (Pubitemid 350180489)
43. Riederer F, Bittsansky M, Schmidt C, Mlynarik V, Baumgartner C, Moser E, Serles W,. (2006) 1H magnetic resonance spectroscopy at 3 T in cryptogenic and mesial temporal lobe epilepsy. NMR Biomed 19: 544-553.
44. Sakatani S, Seto-Ohshima A, Shinohara Y, Yamamoto Y, Yamamoto H, Itohara S, Hirase H,. (2008) Neural-activity-dependent release of S100B from astrocytes enhances kainate-induced gamma oscillations in vivo. J Neurosci 28: 10928-10936.
45. Scantlebury MH, Heida JG, Hasson HJ, Veliskova J, Velisek L, Galanopoulou AS, Moshe SL,. (2007) Age-dependent consequences of status epilepticus: animal models. Epilepsia 48 (Suppl. 2): 75-82. (Pubitemid 46850005)
46. Seeger U, Klose U, Mader I, Grodd W, Nagele T,. (2003) Parameterized evaluation of macromolecules and lipids in proton MR spectroscopy of brain diseases. Magn Reson Med 49: 19-28. (Pubitemid 36042330)
47. Seifert G, Carmignoto G, Steinhauser C,. (2010) Astrocyte dysfunction in epilepsy. Brain Res Rev 63: 212-221.
48. Shih MT, Singh AK, Wang AM, Patel S,. (2004) Brain lesions with elevated lactic acid peaks on magnetic resonance spectroscopy. Curr Probl Diagn Radiol 33: 85-95. (Pubitemid 38262965)
49. Simister RJ, Woermann FG, McLean MA, Bartlett PA, Barker GJ, Duncan JS,. (2002) A short-echo-time proton magnetic resonance spectroscopic imaging study of temporal lobe epilepsy. Epilepsia 43: 1021-1031. (Pubitemid 35006477)
50. Simmons ML, Frondoza CG, Coyle JT,. (1991) Immunocytochemical localization of N-acetyl-aspartate with monoclonal antibodies. Neuroscience 45: 37-45.
51. Slivka A, Mytilineou C, Cohen G,. (1987) Histochemical evaluation of glutathione in brain. Brain Res 409: 275-284. (Pubitemid 17077548)
52. Terpstra M, Henry PG, Gruetter R,. (2003) Measurement of reduced glutathione (GSH) in human brain using LCModel analysis of difference-edited spectra. Magn Reson Med 50: 19-23. (Pubitemid 36841855)
53. Tkac I, Starcuk Z, Choi IY, Gruetter R,. (1999) In vivo 1H NMR spectroscopy of rat brain at 1 ms echo time. Magn Reson Med 41: 649-656. (Pubitemid 29205710)
54. Tkac I, Henry PG, Andersen P, Keene CD, Low WC, Gruetter R,. (2004) Highly resolved in vivo 1H NMR spectroscopy of the mouse brain at 9.4 T. Magn Reson Med 52: 478-484. (Pubitemid 39108958)
55. Turkdogan-Sozuer D, Ozek MM, Sav A, Dincer A, Pamir MN,. (2000) Serial MRI and MRS studies with unusual findings in Rasmussen's encephalitis. Eur Radiol 10: 962-966. (Pubitemid 30353730)
56. van Eijsden P, Notenboom RG, Wu O, de Graan PN, van Nieuwenhuizen O, Nicolay K, Braun KP,. (2004) In vivo 1H magnetic resonance spectroscopy, T2-weighted and diffusion-weighted MRI during lithium-pilocarpine-induced status epilepticus in the rat. Brain Res 1030: 11-18. (Pubitemid 39563823)
57. Vezzani A, French J, Bartfai T, Baram TZ,. (2011) The role of inflammation in epilepsy. Nat Rev Neurol 7: 31-40.
58. Volterra A, Meldolesi J,. (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6: 626-640. (Pubitemid 41059337)
59. Wellard RM, Briellmann RS, Prichard JW, Syngeniotis A, Jackson GD,. (2003) Myoinositol abnormalities in temporal lobe epilepsy. Epilepsia 44: 815-821. (Pubitemid 36754007)
60. Wilson M, Reynolds G, Kauppinen RA, Arvanitis TN, Peet AC,. (2011) A constrained least-squares approach to the automated quantitation of in vivo (1)H magnetic resonance spectroscopy data. Magn Reson Med 65: 1-12.
61. Worrell GA, Parish L, Cranstoun SD, Jonas R, Baltuch G, Litt B,. (2004) High-frequency oscillations and seizure generation in neocortical epilepsy. Brain 127: 1496-1506. (Pubitemid 38899403)
62. Zahr NM, Crawford EL, Hsu O, Vinco S, Mayer D, Rohlfing T, Sullivan EV, Pfefferbaum A,. (2009) In vivo glutamate decline associated with kainic acid-induced status epilepticus. Brain Res 1300: 65-78.