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(Received for publication, June 11, 1996, and in revised form, August 2, 1996)
From the Departments of Biology and Kinesiology, York University,
North York, Ontario M3J 1P3, Canada
To date, no studies have described the import of
proteins in mitochondria obtained from skeletal muscle. In this tissue,
mitochondria consist of the functionally and biochemically distinct
intermyofibrillar (IMF) and subsarcolemmal (SS) subfractions, which are
localized in specialized cellular compartments. This mitochondrial
heterogeneity in muscle could be due, in part, to differential rates of
protein import. To evaluate this possibility, the import of precursor
malate dehydrogenase and ornithine carbamyltransferase proteins was
investigated in isolated IMF and SS mitochondria in vitro.
Import of these was 3-4-fold greater in IMF compared with SS
mitochondria as a function of time. This could account for the higher
malate dehydrogenase enzyme activity in IMF mitochondria. Divergent
import rates in IMF and SS mitochondria likely result from a
differential reliance on various components of the import pathway. SS
mitochondria possess a greater content of the molecular chaperones
hsp60 and Grp75, yet import is lower than in IMF mitochondria. On the
other hand, adriamycin inhibition studies illustrated a greater
reliance on acidic phospholipids (i.e. cardiolipin) for the
import process in SS mitochondria. Matrix ATP levels were 3-fold higher
in IMF mitochondria, but experiments in which ATP depletion was
performed with atractyloside and oligomycin illustrated a dissociation
between import rates and levels of ATP. In contrast, a close
relationship was found between the rate of ATP production
(i.e. mitochondrial respiration) and protein import. When
respiratory rates in IMF and SS mitochondria were equalized, import
rates in both subfractions were similar. These data indicate that 1)
import rates are more closely related to the rate of ATP production
than the steady state ATP level, 2) import into IMF and SS
mitochondrial subfractions is regulated differently, and 3)
mitochondrial heterogeneity within a cell type can be due to
differences in the rates of protein import, suggesting that this step
is a potentially regulatable event in determining the final
mitochondrial phenotype.
Volume 271, Number 44,
Issue of November 1, 1996
pp. 27285-27291
©1996 by The American Society for Biochemistry and Molecular Biology, Inc.
DIFFERENTIAL IMPORT REGULATION IN DISTINCT SUBCELLULAR
REGIONS
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