Discoveries, metabolic roles and diseases of mitochondrial carriers: A review

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1863, Issue 10, 2016, Pages 2362-2378

  Palmieri, Ferdinando ^a   Monné, Magnus ^a,b  

^a UNIVERSITY OF BARI   (Italy)

^b UNIVERSITY OF BASILICATA   (Italy)

Author keywords

Mitochondria; Mitochondrial carrier; Mitochondrial carrier associated diseases; Mitochondrial transporter; SLC25; Transport

Indexed keywords

3' PHOSPHOADENOSINE 5' PHOSPHATE CARRIER PROTEIN; ADENOSINE 5' PHOSPHOSULFATE CARRIER PROTEIN; ADENOSINE TRIPHOSPHATE MAGNESIUM PHOSPHATE CARRIER PROTEIN; AMINO ACID TRANSPORTER; ASPARTATE GLUTAMATE CARRIER PROTEIN; CARNITINE CARRIER PROTEIN; CARRIER PROTEIN; CITRATE OXOGLUTARATE CARRIER PROTEIN; COENZYME A CARRIER PROTEIN; DICARBOXYLATE TRANSPORTER; FLAVINE ADENINE NUCLEOTIDE CARRIER PROTEIN; FOUR CARBON METABOLITE PHOSPHATE CARRIER PROTEIN; GLUTAMATE CARRIER PROTEIN; GUANOSINE TRIPHOSPHATE GUANOSINE DIPHOSPHATE CARRIER PROTEIN; LIPOSOME; MITOCHONDRIAL CARRIER FAMILY PROTEIN; MITOCHONDRIAL PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE CARRIER PROTEIN; OXALOACETATE SULFATECARRIER PROTEIN; PEROXISOMAL ADENINE NUCLEOTIDE CARRIER PROTEIN; PYRIMIDINE NUCLEOTIDE CARRIER PROTEIN; RECOMBINANT PROTEIN; S ADENOSYLMETHIONINE CARRIER PROTEIN; SUCCINATE FURAMARATE CARRIER PROTEIN; THIAMINE PYROPHOSPHATE CARRIER PROTEIN; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS THALIANA; ARTICLE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENOME; HUMAN; KNOCKOUT GENE; METABOLIC DISORDER; MITOCHONDRIAL RESPIRATION; NONHUMAN; ORTHOLOGY; PHENOTYPE; PHYLOGENETIC TREE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MOTIF; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TRANSPORT ASSAY; ANIMAL; DEFICIENCY; GENE EXPRESSION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; PHYSIOLOGY; PROTEIN DOMAIN; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; GENE EXPRESSION; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL MEMBRANES; PHYLOGENY; PROTEIN DOMAINS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84961780322     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2016.03.007     Document Type: Article

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113. Casimir, M., Lasorsa, F.M., Rubi, B., Caille, D., Palmieri, F., Meda, P., et al. Mitochondrial glutamate carrier GC1 as a newly identified player in the control of glucose-stimulated insulin secretion. J. Biol. Chem. 284 (2009), 25004–25014.
114. Molinari, F., Raas-Rothschild, A., Rio, M., Fiermonte, G., Encha-Razavi, F., Palmieri, L., et al. Impaired mitochondrial glutamate transport in autosomal recessive neonatal myoclonic epilepsy. Am. J. Hum. Genet. 76 (2005), 334–339.
115. Molinari, F., Kaminska, A., Fiermonte, G., Boddaert, N., Raas-Rothschild, A., Plouin, P., et al. Mutations in the mitochondrial glutamate carrier SLC25A22 in neonatal epileptic encephalopathy with suppression bursts. Clin. Genet. 76 (2009), 188–194.
116. Poduri, A., Heinzen, E.L., Chitsazzadeh, V., Lasorsa, F.M., Elhosary, P.C., LaCoursiere, C.M., et al. SLC25A22 is a novel gene for migrating partial seizures in infancy. Ann. Neurol. 74 (2013), 873–882.
117. Traba, J., Satrústegui, J., del Arco, A., Characterization of SCaMC-3-like/slc25a41, a novel calcium-independent mitochondrial ATP-Mg/Pi carrier. Biochem. J. 418 (2009), 125–133.
118. +)-dependent ATP-Mg/Pi transport. Structure 22 (2014), 209–217.
119. Harborne, S.P.D., Ruprecht, J.J., Kunji, E.R.S., Calcium-induced conformational changes in the regulatory domain of the human mitochondrial ATP-Mg/Pi carrier. Biochim. Biophys. Acta 1847 (2015), 1245–1253.
120. +) buffering. Cell Death Differ. 19 (2012), 650–660.
121. 2 + uptake, interacts with MCU, and induces oxidative stress-mediated cell death. Mol. Biol. Cell 25 (2014), 936–947.
122. Dolce, V., Scarcia, P., Iacopetta, D., Palmieri, F., A fourth ADP/ATP carrier isoform in man: identification, bacterial expression, functional characterization and tissue distribution. FEBS Lett. 579 (2005), 633–637.
123. Brower, J.V., Lim, C.H., Jorgensen, M., Oh, S.P., Terada, N., Adenine nucleotide translocase 4 deficiency leads to early meiotic arrest of murine male germ cells. Reproduction 138 (2009), 463–470.
124. Haitina, T., Lindblom, J., Renström, T., Fredriksson, R., Fourteen novel human members of mitochondrial solute carrier family 25 (SLC25) widely expressed in the central nervous system. Genomics 88 (2006), 779–790.
125. Fiermonte, G., Paradies, E., Todisco, S., Marobbio, C.M.T., Palmieri, F., A novel member of solute carrier family 25 (SLC25A42) is a transporter of coenzyme A and adenosine 3′,5′-diphosphate in human mitochondria. J. Biol. Chem. 284 (2009), 18152–18159.
126. Shamseldin, H.E., Smith, L.L., Kentab, A., Alkhalidi, H., Summers, B., Alsedairy, H., et al. Mutation of the mitochondrial carrier SLC25A42 causes a novel form of mitochondrial myopathy in humans. Hum. Genet. 135 (2016), 21–30.
127. Honsho, M., Fujiki, Y., Topogenesis of peroxisomal membrane protein requires a short, positively charged intervening-loop sequence and flanking hydrophobic segments: study using human membrane protein PMP34. J. Biol. Chem. 276 (2001), 9375–9382.
128. Titus, S.A., Moran, R.G., Retrovirally mediated complementation of the glyB phenotype. Cloning of a human gene encoding the carrier for entry of folates into mitochondria. J. Biol. Chem., 275, 2000 (36811–36807).
129. Bedhomme, M., Hoffmann, M., McCarthy, E.A., Gambonnet, B., Moran, R.G., Rébeillé, F., et al. Folate metabolism in plants: an Arabidopsis homolog of the mammalian mitochondrial folate transporter mediates folate import into chloroplasts. J. Biol. Chem. 280 (2005), 34823–34831.
130. + carrier proteins. J. Biol. Chem. 284 (2009), 31249–31259.
131. Linka, N., Theodoulou, F.L., Haslam, R.P., Linka, M., Napier, J.A., Neuhaus, H.E., et al. Peroxisomal ATP import is essential for seedling development in Arabidopsis thaliana. Plant Cell 20 (2008), 3241–3257.
132. +. Biochem. J. 443 (2012), 241–247.
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134. Nicholls, D.G., The physiological regulation of uncoupling proteins. Biochim. Biophys. Acta, 1757, 459–466.
135. Vozza, A., Parisi, G., De Leonardis, F., Lasorsa, F.M., Castegna, A., Amorese, D., et al. UCP2 transports C4 metabolites out of mitochondria, regulating glucose and glutamine oxidation. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 960–965.
136. F. Bouillaud, contribution to this BBA-MCR Special Issue.
137. Sekoguchi, E., Sato, N., Yasui, A., Fukada, S., Nimura, Y., Aburatani, H., et al. A novel mitochondrial carnitine-acylcarnitine translocase induced by partial hepatectomy and fasting. J. Biol. Chem. 278 (2003), 38796–38802.
138. Camacho, J.A., Rioseco-Camacho, N., The human and mouse SLC25A29 mitochondrial transporters rescue the deficient ornithine metabolism in fibroblasts of patients with the hyperornithinemia-hyperammonemia-homocitrullinuria (HHH) syndrome. Pediatr. Res. 66 (2009), 35–41.
139. Porcelli, V., Fiermonte, G., Longo, A., Palmieri, F., The human gene SLC25A29, of solute carrier family 25, encodes a mitochondrial transporter of basic amino acids. J. Biol. Chem. 289 (2014), 13374–13384.
140. Picault, N., Palmieri, L., Pisano, I., Hodges, M., Palmieri, F., Identification of a novel transporter for dicarboxylates and tricarboxylates in plant mitochondria. Bacterial expression, reconstitution, functional characterization, and tissue distribution. J. Biol. Chem. 277 (2002), 24204–24211.
141. Hoyos, M.E., Palmieri, L., Wertin, T., Arrigoni, R., Polacco, J.C., Palmieri, F., Identification of a mitochondrial transporter for basic amino acids in Arabidopsis thaliana by functional reconstitution into liposomes and complementation in yeast. Plant J. 33 (2003), 1027–1035.
142. Palmieri, L., Todd, C.D., Arrigoni, R., Hoyos, M.E., Santoro, A., Polacco, J.C., et al. Arabidopsis mitochondria have two basic amino acid transporters with partially overlapping specificities and differential expression in seedling development. Biochim. Biophys. Acta 1757 (2006), 1277–1283.
143. Palmieri, L., Arrigoni, R., Blanco, E., Carrari, F., Zanor, M.I., Studart-Guimaraes, C., et al. Molecular identification of an Arabidopsis S-adenosylmethionine transporter. Analysis of organ distribution, bacterial expression, reconstitution into liposomes, and functional characterization. Plant Physiol. 142 (2006), 855–865.
144. Bouvier, F., Linka, N., Isner, J.-C., Mutterer, J., Weber, A.P.M., Camara, B., Arabidopsis SAMT1 defines a plastid transporter regulating plastid biogenesis and plant development. Plant Cell 18 (2006), 3088–3105.
145. Palmieri, L., Picault, N., Arrigoni, R., Besin, E., Palmieri, F., Hodges, M., Molecular identification of three Arabidopsis thaliana mitochondrial dicarboxylate carrier isoforms: organ distribution, bacterial expression, reconstitution into liposomes and functional characterization. Biochem. J. 410 (2008), 621–629.
146. Palmieri, L., Santoro, A., Carrari, F., Blanco, E., Nunes-Nesi, A., Arrigoni, R., et al. Identification and characterization of ADNT1, a novel mitochondrial adenine nucleotide transporter from Arabidopsis. Plant Physiol. 148 (2008), 1797–1808.
147. + carrier of Arabidopsis thaliana transports coenzyme A and its derivatives. J. Bioenerg. Biomembr. 44 (2012), 333–340.
148. Gigolashvili, T., Geier, M., Ashykhmina, N., Frerigmann, H., Wulfert, S., Krueger, S., et al. The Arabidopsis thylakoid ADP/ATP carrier TAAC has an additional role in supplying plastidic phosphoadenosine 5′-phosphosulfate to the cytosol. Plant Cell 24 (2012), 4187–4204.
149. Monné, M., Miniero, D.V., Obata, T., Daddabbo, L., Palmieri, L., Vozza, A., et al. Functional characterization and organ distribution of three mitochondrial ATP-Mg/Pi carriers in Arabidopsis thaliana. Biochim. Biophys. Acta 1847 (2015), 1220–1230.
150. Haferkamp, I., Hackstein, J.H.P., Voncken, F.G.J., Schmit, G., Tjaden, J., Functional integration of mitochondrial and hydrogenosomal ADP/ATP carriers in the Escherichia coli membrane reveals different biochemical characteristics for plants, mammals and anaerobic chytrids. Eur. J. Biochem. 269 (2002), 3172–3181.
151. Leroch, M., Neuhaus, H.E., Kirchberger, S., Zimmermann, S., Melzer, M., Gerhold, J., et al. Identification of a novel adenine nucleotide transporter in the endoplasmic reticulum of Arabidopsis. Plant Cell 20 (2008), 438–451.
152. Arai, Y., Hayashi, M., Nishimura, M., Proteomic identification and characterization of a novel peroxisomal adenine nucleotide transporter supplying ATP for fatty acid beta-oxidation in soybean and Arabidopsis. Plant Cell 20 (2008), 3227–3240.
153. Kirchberger, S., Tjaden, J., Neuhaus, H.E., Characterization of the Arabidopsis Brittle1 transport protein and impact of reduced activity on plant metabolism. Plant J. 56 (2008), 51–63.
154. Bahaji, A., Ovecka, M., Bárány, I., Risueño, M.C., Muñoz, F.J., Baroja-Fernández, E., et al. Dual targeting to mitochondria and plastids of AtBT1 and ZmBT1, two members of the mitochondrial carrier family. Plant Cell Physiol. 52 (2011), 597–609.
155. Rieder, B., Neuhaus, H.E., Identification of an Arabidopsis plasma membrane-located ATP transporter important for anther development. Plant Cell 23 (2011), 1932–1944.
156. Catoni, E., Desimone, M., Hilpert, M., Wipf, D., Kunze, R., Schneider, A., et al. Expression pattern of a nuclear encoded mitochondrial arginine-ornithine translocator gene from Arabidopsis. BMC Plant Biol., 3, 2003, 1.
157. Frelin, O., Agrimi, G., Laera, V.L., Castegna, A., Richardson, L.G.L., Mullen, R.T., et al. Identification of mitochondrial thiamin diphosphate carriers from Arabidopsis and maize. Funct. Integr. Genomics 12 (2012), 317–326.
158. Zallot, R., Agrimi, G., Lerma-Ortiz, C., Teresinski, H.J., Frelin, O., Ellens, K.W., et al. Identification of mitochondrial coenzyme A transporters from maize and Arabidopsis. Plant Physiol. 162 (2013), 581–588.
159. Palmieri, F., Diseases caused by defects of mitochondrial carriers: a review. Biochim. Biophys. Acta 1777 (2008), 564–578.
160. Guernsey, D.L., Jiang, H., Campagna, D.R., Evans, S.C., Ferguson, M., Kellogg, M.D., et al. Mutations in mitochondrial carrier family gene SLC25A38 cause nonsyndromic autosomal recessive congenital sideroblastic anemia. Nat. Genet. 41 (2009), 651–653.
161. Abrams, A.J., Hufnagel, R.B., Rebelo, A., Zanna, C., Patel, N., Gonzalez, M.A., et al. Mutations in SLC25A46, encoding a UGO1-like protein, cause an optic atrophy spectrum disorder. Nat. Genet. 47 (2015), 926–932.
162. Iacobazzi, V., Infantino, V., Palmieri, F., Transcriptional regulation of the mitochondrial citrate and carnitine/acylcarnitine transporters: two genes involved in fatty acid biosynthesis and β-oxidation. Biology 2 (2013), 284–303.
163. Gouy, M., Guindon, S., Gascuel, O., SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27 (2010), 221–224.
164. Edvardson, S., Porcelli, V., Jalas, C., Soiferman, D., Kellner, Y., Shaag, A., et al. Agenesis of corpus callosum and optic nerve hypoplasia due to mutations in SLC25A1 encoding the mitochondrial citrate transporter. J. Med. Genet. 50 (2013), 240–245.
165. Nota, B., Struys, E.A., Pop, A., Jansen, E.E., Fernandez Ojeda, M.R., Kanhai, W.A., et al. Deficiency in SLC25A1, encoding the mitochondrial citrate carrier, causes combined D-2- and L-2-hydroxyglutaric aciduria. Am. J. Hum. Genet. 92 (2013), 627–631.
166. Mayr, J.A., Merkel, O., Kohlwein, S.D., Gebhardt, B.R., Böhles, H., Fötschl, U., et al. Mitochondrial phosphate-carrier deficiency: a novel disorder of oxidative phosphorylation. Am. J. Hum. Genet. 80 (2007), 478–484.
167. Mayr, J.A., Zimmermann, F.A., Horváth, R., Schneider, H.-C., Schoser, B., Holinski-Feder, E., et al. Deficiency of the mitochondrial phosphate carrier presenting as myopathy and cardiomyopathy in a family with three affected children. Neuromuscul. Disord. 21 (2011), 803–808.
168. Palmieri, L., Alberio, S., Pisano, I., Lodi, T., Meznaric-Petrusa, M., Zidar, J., et al. Complete loss-of-function of the heart/muscle-specific adenine nucleotide translocator is associated with mitochondrial myopathy and cardiomyopathy. Hum. Mol. Genet. 14 (2005), 3079–3088.
169. Echaniz-Laguna, A., Chassagne, M., Ceresuela, J., Rouvet, I., Padet, S., Acquaviva, C., et al. Complete loss of expression of the ANT1 gene causing cardiomyopathy and myopathy. J. Med. Genet. 49 (2012), 146–150.
170. Kaukonen, J., Juselius, J.K., Tiranti, V., Kyttälä, A., Zeviani, M., Comi, G.P., et al. Role of adenine nucleotide translocator 1 in mtDNA maintenance. Science 289 (2000), 782–785.
171. Tessa, A., Fiermonte, G., Dionisi-Vici, C., Paradies, E., Baumgartner, M.R., Chien, Y.-H., et al. Identification of novel mutations in the SLC25A15 gene in hyperornithinemia-hyperammonemia-homocitrullinuria (HHH) syndrome: a clinical, molecular, and functional study. Hum. Mutat. 30 (2009), 741–748.
172. Ersoy Tunalı, N., Marobbio, C.M.T., Tiryakioğlu, N.O., Punzi, G., Saygılı, S.K., Onal, H., et al. A novel mutation in the SLC25A15 gene in a Turkish patient with HHH syndrome: functional analysis of the mutant protein. Mol. Genet. Metab. 112 (2014), 25–29.
173. Indiveri, C., Iacobazzi, V., Tonazzi, A., Giangregorio, N., Infantino, V., Convertini, P., et al. The mitochondrial carnitine/acylcarnitine carrier: function, structure and physiopathology. Mol. Asp. Med. 32 (2011), 223–233.
174. Stanley, C.A., Palmieri, F., Bennett, M.J., Disorders of the mitochondrial carnitine shuttle. Valle, D., Vogelstein, B., Kinzler, K., Antonarakis, S., Ballagio, A., Gibson, K., et al. (eds.) Online Mol. Metab. Basis Inherit. dis, 2013, McGraw Hill, 10.1036/ommbid.101a.