A novel approach for imaging brain-behavior relationships in mice reveals unexpected metabolic patterns during seizures in the absence of tissue plasminogen activator

NeuroImage

Volumn 38, Issue 1, 2007, Pages 34-42

  Mirrione, Martine M ^a,b   Schiffer, Wynne K ^b   Fowler, Joanna S ^b   Alexoff, Dave L ^b   Dewey, Stephen L ^a,b,c   Tsirka, Stella E ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINERGIC RECEPTOR; FLUORODEOXYGLUCOSE F 18; GLUCOSE; PILOCARPINE; SERINE PROTEINASE; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; BRAIN METABOLISM; BRAIN REGION; C57BL 6 MOUSE; CONTROLLED STUDY; DATA ANALYSIS; GLUCOSE BLOOD LEVEL; INFLAMMATION; MOUSE; NERVE DEGENERATION; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; SEIZURE; SEIZURE SUSCEPTIBILITY; SEIZURE THRESHOLD; STATISTICAL ANALYSIS; TEMPORAL LOBE EPILEPSY; WILD TYPE;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; FLUORODEOXYGLUCOSE F18; METABOLIC CLEARANCE RATE; MICE; MICE, KNOCKOUT; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS; SEIZURES; TISSUE PLASMINOGEN ACTIVATOR;

EID: 34548713439     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2007.06.032     Document Type: Article

References (45)

1. Abbey C.K., Borowsky A.D., McGoldrick E.T., Gregg J.P., Maglione J.E., Cardiff R.D., and Cherry S.R. In vivo positron-emission tomography imaging of progression and transformation in a mouse model of mammary neoplasia. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 11438-11443
2. Alexoff D.L., Vaska P., Marsteller D., Gerasimov T., Li J., Logan J., Fowler J.S., Taintor N.B., Thanos P.K., and Volkow N.D. Reproducibility of 11C-raclopride binding in the rat brain measured with the microPET R4: effects of scatter correction and tracer specific activity. J. Nucl. Med. 44 (2003) 815-822
3. Baranes D., Lederfein D., Huang Y.Y., Chen M., Bailey C.H., and Kandel E.R. Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron 21 (1998) 813-825
4. Carne R.P., O'Brien T.J., Kilpatrick C.J., MacGregor L.R., Hicks R.J., Murphy M.A., Bowden S.C., Kaye A.H., and Cook M.J. MRI-negative PET-positive temporal lobe epilepsy: a distinct surgically remediable syndrome. Brain 127 (2004) 2276-2285
5. Carroll P.M., Tsirka S.E., Richards W.G., Frohman M.A., and Strickland S. The mouse tissue plasminogen activator gene 5′ flanking region directs appropriate expression in development and a seizure-enhanced response in the CNS. Development 120 (1994) 3173-3183
6. Centonze D., Napolitano M., Saulle E., Gubellini P., Picconi B., Martorana A., Pisani A., Gulino A., Bernardi G., and Calabresi P. Tissue plasminogen activator is required for corticostriatal long-term potentiation. Eur. J. Neurosci. 16 (2002) 713-721
7. de Lanerolle N.C., Kim J.H., Williamson A., Spencer S.S., Zaveri H.P., Eid T., and Spencer D.D. A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: evidence for distinctive patient subcategories. Epilepsia 44 (2003) 677-687
8. Diehl B., LaPresto E., Najm I., Raja S., Rona S., Babb T., Ying Z., Bingaman W., Luders H.O., and Ruggieri P. Neocortical temporal FDG-PET hypometabolism correlates with temporal lobe atrophy in hippocampal sclerosis associated with microscopic cortical dysplasia. Epilepsia 44 (2003) 559-564
9. Frey U., Müller M., and Kuhl D. A different form of long-lasting potentiation revealed in tissue plasminogen activator mutant mice. J. Neurosci. 16 (1996) 2057-2063
10. Garrido Sanabria E.R., Castaneda M.T., Banuelos C., Perez-Cordova M.G., Hernandez S., and Colom L.V. Septal GABAergic neurons are selectively vulnerable to pilocarpine-induced status epilepticus and chronic spontaneous seizures. Neuroscience 142 (2006) 871-883
11. Gispert J.D., Pascau J., Reig S., Martinez-Lazaro R., Molina V., Garcia-Barreno P., and Desco M. Influence of the normalization template on the outcome of statistical parametric mapping of PET scans. NeuroImage 19 (2003) 601-612
12. Hamilton S.E., Loose M.D., Qi M., Levey A.I., Hille B., McKnight G.S., Idzerda R.L., and Nathanson N.M. Disruption of the m1 receptor gene ablates muscarinic receptor-dependent M current regulation and seizure activity in mice. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 13311-13316
13. Kornblum H.I., Araujo D.M., Annala A.J., Tatsukawa K.J., Phelps M.E., and Cherry S.R. In vivo imaging of neuronal activation and plasticity in the rat brain by high resolution positron emission tomography (microPET). Nat. Biotechnol. 18 (2000) 655-660
14. 18F]FDG-PET reveals temporal hypometabolism in patients with temporal lobe epilepsy even when quantitative MRI and histopathological analysis show only mild hippocampal damage. Arch. Neurol. 58 (2001) 933-939
15. Ma Y., Hof P.R., Grant S.C., Blackband S.J., Bennett R., Slatest L., McGuigan M.D., and Benveniste H. A three-dimensional digital atlas database of the adult C57BL/6J mouse brain by magnetic resonance microscopy. Neuroscience 135 (2005) 1203-1215
16. Madani R., Hulo S., Toni N., Madani H., Steimer T., Muller D., and Vassalli J.D. Enhanced hippocampal long-term potentiation and learning by increased neuronal expression of tissue-type plasminogen activator in transgenic mice. EMBO J. 18 (1999) 3007-3012
17. Maslanski J.A., Powelt R., Deirmengiant C., and Patelt J. Assessment of the muscarinic receptor subtypes involved in pilocarpine-induced seizures in mice. Neurosci. Lett. 168 (1994) 225-228
18. Mirrione M.M., Schiffer W.K., Siddiq M., Dewey S.L., and Tsirka S.E. PET imaging of glucose metabolism in a mouse model of temporal lobe epilepsy. Synapse 59 (2006) 119-121
19. Nicole O., Docagne F., Ali C., Margaill I., Carmeliet P., MacKenzie E.T., Vivien D., and Buisson A. The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling. Nat. Med. 7 (2001) 59-64
20. Nuyts J., and Fessler J.A. A penalized-likelihood image reconstruction method for emission tomography, compared to postsmoothed maximum-likelihood with matched spatial resolution. IEEE Trans. Med. Imag. 22 (2003) 1042-1052
21. Pawlak R., Melchor J.P., Matys T., Skrzypiec A.E., and Strickland S. Ethanol-withdrawal seizures are controlled by tissue plasminogen activator via modulation of NR2B-containing NMDA receptors. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 443-448
22. Paxinos G., and Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates. 2nd ed. (2001), Academic Press, San Diego
23. Pereira de Vasconcelos A., Ferrandon A., and Nehlig A. Local cerebral blood flow during lithium-pilocarpine seizures in the developing and adult rat: role of coupling between blood flow and metabolism in the genesis of neuronal damage. J. Cereb. Blood Flow Metab. 22 (2002) 196-205
24. Qian Z., Gilbert M.E., Colicos M.A., Kandel E.R., and Kuhl D. Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature 361 (1993) 453-457
25. Racine R., Gartner J., and Burnham W. Epileptiform activity and neural plasticity in limbic structures. Brain Res. 47 (1972) 262-268
26. Salles F.J., and Strickland S. Localization and regulation of the tissue plasminogen activator-plasmin system in the hippocampus. J. Neurosci. 22 (2002) 2125-2134
27. Schauwecker P.E., and Steward O. Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 4103-4108
28. Schiffer W.K., Alexoff D.L., Shea C., Logan J., and Dewey S.L. Development of a simultaneous PET/microdialysis method to identify the optimal dose of 11C-raclopride for small animal imaging. J. Neurosci. Methods 144 (2005) 25-34
29. Schiffer W.K., Lee D.E., Alexoff D.L., Ferrieri R., Brodie J.D., and Dewey S.L. Metabolic correlates of toluene abuse: decline and recovery of function in adolescent animals. Psychopharmacology (Berlin) 186 (2006) 159-167
30. Schiffer W.K., Mirrione M.M., Biegon A., Alexoff D.L., Patel V., and Dewey S.L. Serial microPET measures of the metabolic reaction to a microdialysis probe implant. J. Neurosci. Methods 155 (2006) 272-284
31. Schmidt K.C., Lucignani G., and Sokoloff L. Fluorine-18-fluorodeoxyglucose PET to determine regional cerebral glucose utilization: a re-examination. J. Nucl. Med. 37 (1996) 394-399
32. Schweinhardt P., Fransson P., Olson L., Spenger C., and Andersson J.L. A template for spatial normalisation of MR images of the rat brain. J. Neurosci. Methods 129 (2003) 105-113
33. Scorza F.A., Arida R.M., Priel M.R., Calderazzo L., and Cavalheiro E.A. Glucose utilisation during status epilepticus in an epilepsy model induced by pilocarpine: a qualitative study. Arq. Neuro-Psiquiatr. 60 (2002) 198-203
34. Seeds N.W., Williams B.L., and Bickford P.C. Tissue plasminogen activator induction in Purkinje neurons after cerebellar motor learning. Science 270 (1995) 1992-1994
35. Shibley H., and Smith B.N. Pilocarpine-induced status epilepticus results in mossy fiber sprouting and spontaneous seizures in C57BL/6 and CD-1 mice. Epilepsy Res. 49 (2002) 109-120
36. 18F]FDG PET: a clinical validation of statistical parametric mapping. NeuroImage 9 (1999) 63-80
37. Smolders I., Van Belle K., Ebinger G., and Michotte Y. Hippocampal and cerebellar extracellular amino acids during pilocarpine-induced seizures in freely moving rats. Eur. J. Pharmacol. 319 (1997) 21-29
38. Sossi V., and Ruth T.J. Micropet imaging: in vivo biochemistry in small animals. J. Neural Transm. 112 (2005) 319-330
39. Tanaka S., Sako K., Tanaka T., Nishihara I., and Yonemasu Y. Uncoupling of local blood flow and metabolism in the hippocampal CA3 in kainic acid-induced limbic seizure status. Neuroscience 36 (1990) 339-348
40. Tsirka S.E., Gualandris A., Amaral D.G., and Strickland S. Excitotoxin-induced neuronal degeneration and seizure are mediated by tissue plasminogen activator. Nature 377 (1995) 340-344
41. Turski W.A., Cavalheiro E.A., Bortolotto Z.A., Mello L.M., Schwarz M., and Turski L. Seizures produced by pilocarpine in mice: a behavioral, electroencephalographic and morphological analysis. Brain Res. 321 (1984) 237-253
42. Wu Y.P., Siao C.J., Lu W., Sung T.C., Frohman M.A., Milev P., Bugge T.H., Degen J.L., Levine J.M., Margolis R.U., and Tsirka S.E. The tissue plasminogen activator (tPA)/plasmin extracellular proteolytic system regulates seizure-induced hippocampal mossy fiber outgrowth through a proteoglycan substrate. J. Cell Biol. 148 (2000) 1295-1304
43. Yepes M., Sandkvist M., Coleman T.A., Moore E., Wu J.Y., Mitola D., Bugge T.H., and Lawrence D.A. Regulation of seizure spreading by neuroserpin and tissue-type plasminogen activator is plasminogen-independent. J. Clin. Invest. 109 (2002) 1571-1578
44. Zhang Y., Kanaho Y., Frohman M.A., and Tsirka S.E. Phospholipase D1-promoted release of tissue plasminogen activator facilitates neurite outgrowth. J. Neurosci. 25 (2005) 1797-1805
45. Zhuo M., Holtzman D.M., Li Y., Osaka H., DeMaro J., Jacquin M., and Bu G. Role of tissue plasminogen activator receptor LRP in hippocampal long-term potentiation. J. Neurosci. 20 (2000) 542-549