Journal of Bioenergetics and Biomembranes, Vol. 30, No. 3, 1998
Human Mitochondrial Transmembrane Metabolite
Carriers: Tissue Distribution and Its Implication for
Mitochondrial Disorders
Marjan Huizing,1 Wim Ruitenbeek,1 Lambert P. van den Heuvel,1 Vincenza Dolce,2
Vito Iacobazzi,2 Jan A. M. Smeitink,1 Ferdinando Palmieri,2 and J. M. Frans Trijbels1
Received December 10, 1997; accepted April 29, 1998
Mitochondrial transmembrane carrier deficiencies are a recently discovered group of disorders,
belonging to the so-called mitochondriocytopathies. We examined the human tissue distribution
of carriers which are involved in the process of oxidative phosphorylation (adenine nucleotide
translocator, phosphate carrier, and voltage-dependent anion channel) and some mitochondrial
substrate carriers (2-oxoglutarate carrier, carnitine-acylcarnitine carrier, and citrate carrier).
The tissue distribution on mRNA level of mitochondrial transport proteins appears to be
roughly in correlation with the dependence of these tissues on mitochondrial energy production
capacity. In general the main mRNA expression of carriers involved in mitochondrial energy
metabolism occurs in skeletal muscle and heart. Expression in liver and pancreas differs
between carriers. Expression in brain, placenta, lung, and kidney is lower than in the other
tissues. Western and Northern blotting experiments show a comparable HVDAC1 protein and
mRNA distribution for the tested tissues. Patient's studies showed that cultured skin fibroblasts
may not be a reliable alternative for skeletal muscle in screening for human mitochondrial
carrier defects.
KEY WORDS: Mitochondrial transmembrane carrier; tissue distribution; mitochondriopathy; adenine
nucleotide translocator; phosphate carrier; voltage-dependent anion channel; citrate carrier; oxoglutarate
carrier; carnitine-acylcarnitine carrier.
INTRODUCTION
When studying mitochondrial disorders it is
worthwhile to consider the mitochondrial transmem-
brane carriers because a defective functioning of such
carriers may lead to a disturbed mitochondrial energy
generation (Ruitenbeek et al., 1995; Huizing et al.,
1996a). Of particular interest are the carriers which
are directly involved in the process of oxidative phos-
phorylation, such as the adenine nucleotide transloca-
tor (ANT3) and the phosphate carrier (PiC). However,
also defects in mitochondrial carriers for transport of
specific substrates (such as pyruvate, 2-oxoglutarate,
malate, carnitine, and glutamate), directly or indirectly
involved in mitochondrial energy metabolism, have to
be considered. Many of these carriers have been iso-
lated and some of them have been cloned and
sequenced (Palmieri, 1994; Palmieri and Van Ommen,
1998). Defects in transmembrane cation transporters
may also induce imperfect energy metabolism proba-
bly as a result of osmotic disturbances within the mito-
1 Department of Pediatrics, University Hospital, Nijmegen, The
Netherlands.
2 Department of Pharmaco-Biology, University of Bari, Bari, Italy.
3 Abbreviations used: ANT, adenine nucleotide translocator; bp,
base pairs; CAC, carnitine-acylcarnitine carrier; CIC, citrate car-
rier; HVDAC, human voltage-dependent anion channel; Mi-CK,
mitochondrial creatine kinase; OGC, 2-oxoglutarate carrier; PiC,
phosphate carrier.
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0145-479X/98/0600-0277$l5.00/0 © 1998 Plenum Publishing Corporation