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Journal of Neuroscience, Vol 13, 4181-4192, Copyright © 1993 by Society for Neuroscience
Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid
MF Beal, E Brouillet, BG Jenkins, RJ Ferrante, NW Kowall, JM Miller, E Storey, R Srivastava, BR Rosen and BT Hyman
Neurochemistry Laboratory, Massachusetts General Hospital, Boston 02114.
An impairment of energy metabolism may underlie slow excitotoxic neuronal
death in neurodegenerative diseases. We therefore examined the effects of
intrastriatal, subacute systemic, or chronic systemic administration of the
mitochondrial toxin 3-nitropropionic acid (3-NP) in rats. Following
intrastriatal injection 3-NP produced dose-dependent striatal lesions.
Neurochemical and histologic evaluation showed that markers of both spiny
projection neurons (GABA, substance P, calbindin) and aspiny interneurons
(somatostatin, neuropeptide Y, NADPH- diaphorase) were equally affected.
Subacute systemic administration of 3-NP produced age-dependent bilateral
striatal lesions with a similar neurochemical profile. However, in contrast
to the intrastriatal injections, striatal dopaminergic afferent projections
were spared. Both freeze-clamp measurements and chemical shift magnetic
resonance spectroscopy showed that 3-NP impairs energy metabolism in the
striatum in vivo. Microdialysis showed no increase in extracellular
glutamate concentrations after systemic administration of 3-NP. The lesions
produced by intrastriatal injection or systemic administration of 3-NP were
blocked by prior decortication. However, the NMDA antagonist MK- 801 did
not block the effects of intrastriatal 3-NP, consistent with a non-NMDA
excitotoxic mechanism. In contrast to subacute systemic administration of
3-NP, chronic (1 month) administration produced lesions confined to the
striatum in which there was relative sparing of NADPH-diaphorase
interneurons, consistent with an NMDA excitotoxic process. Chronic
administration showed growth-related proliferative changes in dendrites of
spiny neurons similar to changes in Huntington's disease (HD). These
results are consistent with in vitro studies showing that mild metabolic
compromise can selectively activate NMDA receptors while more severe
compromise activates both NMDA and non- NMDA receptors. Chronic
administration of 3-NP over 1 month produces selective striatal lesions
that replicate many of the characteristic histologic and neurochemical
features of HD.
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