This study isolated cytochrome oxidase subunit genes from a murine brain cDNA library. It characterized the expression of mitochondrial subunit III and nuclear subunit VIa at the light and electron microscopic level. Subunit III mRNA was localized to mitochondria in cell bodies and processes, while subunit VIa mRNA was associated with the rough endoplasmic reticulum in cell bodies. Monocular enucleation in mice induced downregulation of both subunit mRNAs in the lateral geniculate nucleus, with mitochondrial subunit III decreasing more than nuclear subunit VIa. This suggests tighter regulation of mitochondrial gene expression by neuronal activity.

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Abstract
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Abbreviations
1. Experimental procedures
2. Results
3. Discussion
4. Conclusions
Acknowledgements
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doi:10.1016/S0306-4522(96)00410-1
Neuroscience
Volume 76, Issue 4, 15 January 1997, Pages 1035–1055
Brain cytochrome oxidase subunit complementary DNAs:
isolation, subcloning, sequencing, light and electron
microscopic in situ hybridization of transcripts, and regulation
by neuronal activity
M.T.T Wong-Riley , M.A Mullen, Z Huang, C Guyer
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Abstract
The goal of the present study was to isolate, for the first time, cytochrome oxidase
subunit genes from murine brain complementary DNA library and to characterize the
expression of these genes from mitochondrial and nuclear sources at both light and
electron microscopic levels. Brain subunit III (mitochondrial) shared 100% identity with
that of murine L cells. Subunit VIa (nuclear) was known to have tissue-specific isoforms
in other species: the ubiquitous liver isoform and the heart/muscle isoform. Our brain
subunit VIa shared 93% homology with that of the rat liver and 100% identity with the
recently reported murine liver isoform, which is only 62% identical to that of the rat heart
isoform. In situ hybridization with riboprobes revealed messenger RNA labelling that was
similar, though not identical, to that of cytochrome oxidase histochemistry. Monocular
enucleation in adult mice induced a significant down-regulation of both subunit
messages in the contralateral lateral geniculate nucleus. However, the decrease in
subunit III messenger RNAs surpassed that of subunit VIa at all time periods examined,
suggesting that mitochondrial gene expression is more tightly regulated by neuronal
activity than that of nuclear ones. At the electron microscopic level, subunit III messenger
RNA was localized to the mitochondrial compartment in both cell bodies and processes,
while that of nuclear-encoded subunit VIa was present exclusively in the
extramitochondrial compartment of somata and not of dendrites or axons. Surprisingly,
the message was primarily associated with the rough endoplasmic reticulum, suggesting
a novel pathway for its synthesis and trafficking.
Our results indicate that the unique properties of neurons impose special requirements
for subunits of a single mitochondrial enzyme with dual genomic origins. At sites of high
energy demands (such as postsynaptic dendrites and some axon terminals),
mitochondrial-encoded cytochrome oxidase subunits can be locally transcribed and
translated, and they provide the framework for the subsequent importation and
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2. incorporation of nuclear-encoded subunits, which are strictly synthesized in the cell
bodies. Dynamic local energy needs are met when subunits from the two genomic
sources are assembled to form functional holoenzymes.
Keywords
energy metabolism; monocular enucleation; gene regulation; mitochondria; mouse
visual system; mRNAs
Abbreviations
b.p., base pairs; BSA, bovine serum albumin; C.O., cytochrome oxidase; EDTA,
ethylenediaminetetra-acetate; LGN, lateral geniculate nucleus; mCO, mitochondrial
cytochrome oxidase subunit; MCS, multiple cloning site; nCO, nuclear cytochrome
oxidase subunit; PBS, phosphate-buffered saline; PCR, polymerase chain reaction;
RER, rough endoplasmic reticulum; RT, room temperature; SSC, sodium
chloride/sodium citrate
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Copyright © 1996 IBRO. Published by Elsevier Ltd. All rights reserved.
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