Diseases caused by defects of mitochondrial carriers: A review

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1777, Issue 7-8, 2008, Pages 564-578

  Palmieri, Ferdinando ^a  

^a UNIVERSITY OF BARI   (Italy)

Author keywords

Carrier deficiencies; Mitochondria; Mitochondrial carrier related diseases; Mitochondrial carriers; Mitochondrial diseases; Transporters

Indexed keywords

ARGININE; ARYLBUTYRIC ACID DERIVATIVE; BENZOIC ACID; CARNITINE; CITRULLINE; MITOCHONDRIAL DNA; ORNITHINE; PHENOBARBITAL;

AAC1 DEFICIENCY; AMISH MICROCEPHALY; ASPARTATE GLUTAMATE CARRIER ISOFORM 2 DEFICIENCY; AUTOSOMAL DOMINANT PROGRESSIVE EXTERNAL OPHTHALMOPLEGIA; BIOCHEMISTRY; CARNITINE ACYLCARNITINE CARRIER DEFICIENCY; CITRULLINEMIA; CONTRACTURE; DIET SUPPLEMENTATION; DIET THERAPY; GENE MUTATION; HETEROZYGOTE; HHH SYNDROME; HUMAN; HYPERAMMONEMIA; INBORN ERROR OF METABOLISM; LIVER TRANSPLANTATION; MITOCHONDRION; MOLECULAR BIOLOGY; NEONATAL MYOCLONIC EPILEPSY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION; PATHOGENESIS; PATHOPHYSIOLOGY; PHENOTYPE; PHYSIOLOGY; PHYSIOTHERAPY; PIC DEFICIENCY; PRIORITY JOURNAL; PROTEIN RESTRICTION; REVIEW; SEIZURE; SENGER SYNDROME; VITAMIN SUPPLEMENTATION;

ANIMALS; CARRIER PROTEINS; GENES, DOMINANT; HUMANS; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL DISEASES; MITOCHONDRIAL PROTEINS; MUTATION; OPHTHALMOPLEGIA;

EID: 46349088952     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2008.03.008     Document Type: Review

References (94)

1. Holt I.J., Harding A.E., and Morgan-Hughes J.A. Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies. Nature 331 (1988) 717-719
2. Wallace D.C., Singh G., Lott M.T., Hodge J.A., Schurr T.G., Lezza A.M., Elsas II L.J., and Nikoskelainen E.K. Mitochondrial DNA mutation associated with Leber's hereditary optic neuropathy. Science 242 (1988) 1427-1430
3. Rustin P., Bourgeron T., Parfait B., Chretien D., Munnich A., and Rötig A. Inborn errors of the Krebs cycle: a group of unusual mitochondrial diseases in human. Biochim. Biophys. Acta 1361 (1997) 185-197
4. Rinaldo P., Matern D., and Bennett M.J. Fatty acid oxidation disorders. Annu. Rev. Physiol. 64 (2002) 477-502
5. Schlame M., Towbin J.A., Heerdt P.M., Jehle R., DiMauro S., and Blanck T.J. Deficiency of tetralinoleoyl-cardiolipin in Barth syndrome. Ann. Neurol. 51 (2002) 634-637
6. Valianpour F., Wanders R.J., Overmars H., Vreken P., Van Gennip A.H., Baas F., Plecko B., Santer R., Becker K., and Barth P.G. Cardiolipin deficiency in X-linked cardioskeletal myopathy and neutropenia (Barth syndrome, MIM 302060): a study in cultured skin fibroblasts. J. Pediatr. 141 (2002) 729-733
7. Napier I., Ponka P., and Richardson D.R. Iron trafficking in the mitochondrion: novel pathways revealed by disease. Blood 105 (2005) 1867-1874
8. Estévez A.G., Crow J.P., Sampson J.B., Reiter C., Zhuang Y., Richardson G.J., Tarpey M.M., Barbeito L., and Beckman J.S. Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science 286 (1999) 2498-2500
9. MacKenzie J.A., and Payne R.M. Mitochondrial protein import and human health and disease. Biochim. Biophys. Acta 1772 (2007) 509-523
10. Detmer S.A., and Chan D.C. Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol. 8 (2007) 870-879
11. Rustin P. Mitochondria, from cell death to proliferation. Nat. Genet. 30 (2002) 352-353
12. Brandon M., Baldi P., and Wallace D.C. Mitochondrial mutations in cancer. Oncogene 25 (2006) 4647-4662
13. DiMauro S., and Schon E.A. Mitochondrial respiratory-chain diseases. New Engl. J. Med. 348 (2003) 2656-2668
14. Zeviani M., and Spinazzola A. Mitochondrial disorders. Curr. Neurol. Neurosci. Rep. 3 (2003) 423-432
15. Schmiedel J., Jackson S., Schäfer J., and Reichmann H. Mitochondrial cytopathies. J. Neurol. 250 (2003) 267-277
16. Rötig A., and Munnich A. Genetic features of mitochondrial respiratory chain disorders. J. Am. Soc. Nephrol. 14 (2003) 2995-3007
17. DiMauro S., and Davidzon G. Mitochondrial DNA and disease. Ann. Med. 37 (2005) 222-232
18. Shapira A.H. Mitochondrial disease. Lancet 368 (2006) 70-82
19. Smeitink J.A., Zeviani M., Turnbull D.M., and Jacobs H.T. Mitochondrial medicine: a metabolic perspective on the pathology of oxidative phosphorylation disorders. Cell Metab. 3 (2006) 9-13
20. Ohta S. A multi-functional organelle mitochondrion is involved in cell death, proliferation and disease. Curr. Med. Chem. 10 (2003) 2485-2494
21. Duchen M.R. Roles of mitochondria in health and disease. Diabetes 53 (2004) 96-102
22. Wallace D.C. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu. Rev. Genet. 39 (2005) 359-407
23. Mariani E., Polidori M.C., Cherubini A., and Mecocci P. Oxidative stress in brain aging, neurodegenerative and vascular diseases: an overview. J. Chromatogr. B 827 (2005) 65-75
24. Lin M.T., and Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443 (2006) 787-795
25. Chan D.C. Mitochondria: dynamic organelles in disease, aging, and development. Cell 125 (2006) 1241-1252
26. Zeviani M., and Carelli V. Mitochondrial disorders. Curr. Opin. Neurol. 20 (2007) 564-571
27. Trushina E., and McMurray C.T. Oxidative stress and mitochondrial dysfunction in neurodegenerative diseases. Neuroscience 145 (2007) 1233-1248
28. Palmieri F. The mitochondrial transporter family (SLC25): physiological and pathological implications. In: Hediger M.A. (Ed). The ABC of solute carriers. Pflugers Arch. - Eur. J. Physiol. 447 (2004) 689-709
29. Palmieri F., and Klingenberg M. Mitochondrial metabolite transporter family. In: Lennarz W.J., and Lane M.D. (Eds). Encyclopedia of Biological Chemistry, vol. 2 (2004), Elsevier, Oxford 725-732
30. Pebay-Peyroula E., Dahout-Gonzalez C., Kahn R., Trézéguet V., Lauquin G.J., and Brandolin G. Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426 (2003) 39-44
31. Kunji E.R., and Harding M. Projection structure of the atractyloside-inhibited mitochondrial ADP/ATP carrier of Saccharomyces cerevisiae. J. Biol. Chem. 278 (2003) 36985-36988
32. Robinson A.J., and Kunji E.R. Mitochondrial carriers in the cytoplasmic state have a common substrate binding site. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 2617-2622
33. Cappello A.R., Miniero D.V., Curcio R., Ludovico A., Daddabbo L., Stipani I., Robinson A.J., Kunji E.R.S., and Palmieri F. Functional and structural role of amino acid residues in the odd-numbered transmembrane α-helices of the bovine mitochondrial oxoglutarate carrier. J. Mol. Biol. 369 (2007) 400-412
34. Fiermonte G., De Leonardis F., Todisco S., Palmieri L., Lasorsa F.M., and Palmieri F. Identification of the mitochondrial ATP-Mg/Pi transporter. Bacterial expression, reconstitution, functional characterization and tissue distribution. J. Biol. Chem. 279 (2004) 30722-30730
35. Agrimi G., Di Noia M.A., Marobbio C.M.T., Fiermonte G., Lasorsa F.M., and Palmieri F. Identification of the human mitochondrial S-adenosylmethionine transporter: bacterial expression, reconstitution, functional characterization and tissue distribution. Biochem. J. 379 (2004) 183-190
36. Dolce V., Scarcia P., Iacopetta D., and Palmieri F. A fourth ADP/ATP carrier isoform in man: identification, bacterial expression, functional characterization and tissue distribution. FEBS Lett. 579 (2005) 633-637
37. Floyd S., Favre C., Lasorsa F.M., Leahy M., Trigiante G., Stroebel P., Marx A., Loughran G., O'Callaghan K., Marobbio C.M.T., Slotboom D.J., Kunji E.R.S., Palmieri F., and O'Connor R. The insulin-like growth factor-I-mTOR signaling pathway induces the mitochondrial pyrimidine nucleotide carrier to promote cell growth. Mol. Biol. Cell 18 (2007) 3545-3555
38. Palmieri L., Alberio S., Pisano I., Lodi T., Meznaric Petrusa M., Zidar J., Santoro A., Scarcia P., Fontanesi F., Lamantea E., Ferrero I., and Zeviani M. 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
39. Curran A.R., and Engelman D.M. Sequence motifs, polar interactions and conformational changes in helical membrane proteins. Curr. Opin. Struct. Biol. 13 (2003) 412-417
40. Graham B.H., Waymire K.G., Cottrell B., Trounce I.A., MacGregor G.R., and Wallace D.C. A mouse model for mitochondrial myopathy and cardiomyopathy resulting from a deficiency in the heart/muscle isoform of the adenine nucleotide translocator. Nat. Genet. 16 (1997) 226-234
41. Jordens E.Z., Palmieri L., Huizing M., van den Heuvel L.P., Sengers R.C.A., Doërner A., Ruitenbeek W., Trijbels J.M.F., Valsson J., Sigfusson G., Palmieri F., and Smeitink J.A.M. Adenine nucleotide translocator 1 deficiency associated with Sengers syndrome. Ann. Neurol. 52 (2002) 95-99
42. Mayr J.A., Merkel O., Kohlwein S.D., Gebhardt B.R., Böhles H., Fötschl U., Koch J., Jaksch M., Lochmüller H., Horváth R., Freisinger P., and Sperl W. Mitochondrial phosphate-carrier deficiency: a novel disorder of oxidative phosphorylation. Am. J. Hum. Genet. 80 (2007) 478-484
43. Dolce V., Iacobazzi V., Palmieri F., and Walker J.E. The sequences of human and bovine genes of the phosphate carrier from mitochondria contain evidence of alternatively spliced forms. J. Biol. Chem. 269 (1994) 10451-10460
44. Fiermonte G., Dolce V., and Palmieri F. Expression in Escherichia coli, functional characterization, and tissue distribution of isoforms A and B of the phosphate carrier from bovine mitochondria. J. Biol. Chem. 273 (1998) 22782-22787
45. Dolce V., Fiermonte G., and Palmieri F. Tissue-specific expression of the two isoforms of the mitochondrial phosphate carrier in bovine tissues. FEBS Lett. 399 (1996) 95-98
46. Kaukonen J., Juselius J.K., Tiranti V., Kyttälä A., Zeviani M., Comi G.P., Keränen S., Peltonen L., and Suomalainen A. Role of adenine nucleotide translocator 1 in mtDNA maintenance. Science 289 (2000) 782-785
47. Van Goethem G., Dermaut B., Löfgren A., Martin J.J., and Van Broeckhoven C. Mutation of POLG is associated with progressive external ophthalmoplegia characterized by mtDNA deletions. Nat. Genet. 28 (2001) 211-212
48. Spelbrink J.N., Li F.Y., Tiranti V., Nikali K., Yuan Q.P., Tariq M., Wanrooij S., Garrido N., Comi G., Morandi L., Santoro L., Toscano A., Fabrizi G.M., Somer H., Croxen R., Beeson D., Poulton J., Suomalainen A., Jacobs H.T., Zeviani M., and Larsson C. Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria. Nat. Genet. 28 (2001) 223-231
49. Fontanesi F., Palmieri L., Scarcia P., Lodi T., Donnini C., Limongelli A., Tiranti V., Zeviani M., Ferrero I., and Viola A.M. Mutations in AAC2, equivalent to human adPEO-associated ANT1 mutations, lead to defective oxidative phosphorylation in Saccharomyces cerevisiae and affect mitochondrial DNA stability. Hum. Mol. Genet. 13 (2004) 923-934
50. Huizing M., Iacobazzi V., Ijlst L., Savelkoul P., Ruitenbeek W., van den Heuvel L.P., Indiveri C., Smeitink J., Trijbels F.J.M., Wanders R.J.A., and Palmieri F. Cloning of the human carnitine-acylcarnitine carrier cDNA, and identification of the molecular defect in a patient. Am. J. Hum. Genet. 61 (1997) 1239-1245
51. Iacobazzi V., Naglieri M.A., Stanley C.A., Wanders R.J.A., and Palmieri F. The structure and organization of the human carnitine/acylcarnitine translocase (CACT) gene. Biochem. Biophys. Res. Commun. 252 (1998) 770-774
52. Indiveri C., Iacobazzi V., Giangregorio N., and Palmieri F. The mitochondrial carnitine carrier protein: cDNA cloning, primary structure, and comparison with other mitochondrial transport proteins. Biochem. J. 321 (1997) 713-719
53. de Lucas J.R., Indiveri C., Tonazzi A., Perez P., Giangregorio N., Iacobazzi V., and Palmieri F. Functional characterisation of residues within the carnitine/acylcarnitine translocase RX2PANAAXF distinct motif. Mol. Membr. Biol. 25 (2008) 152-163
54. Stanley C.A., Hale D.E., Berry G.T., Deleeuw S., Boxer J., and Bonnefont J.P. Brief report: a deficiency of carnitine-acylcarnitine translocase in the inner mitochondrial membrane. New Engl. J. Med. 327 (1992) 19-23
55. Pande S.V., Brivet M., Slama A., Demaugre F., Aufrant C., and Saudubray J.M. Carnitine-acylcarnitine translocase deficiency with severe hypoglycemia and auriculo ventricular block. Translocase assay in permeabilized fibroblasts. J. Clin. Invest. 91 (1993) 1247-1252
56. Iacobazzi V., Invernizzi F., Baratta S., Pons R., Chung W., Garavaglia B., Dionisi-Vici C., Ribes A., Parini R., Huertas M.D., Roldan S., Lauria G., Palmieri F., and Taroni F. Molecular and functional analysis of SLC25A20 mutations causing carnitine-acylcarnitine translocase deficiency. Hum. Mutat. 24 (2004) 312-320
57. IJlst L., van Roermund C.W., Iacobazzi V., Oostheim W., Ruiter J.P., Williams J.C., Palmieri F., and Wanders R.J. Functional analysis of mutant human carnitine acylcarnitine translocases in yeast. Biochem. Biophys. Res. Commun. 280 (2001) 700-706
58. Pérez P., Martínez O., Romero B., Olivas I., Pedregosa A.M., Palmieri F., Laborda F., and De Lucas J.R. Functional analysis of mutations in the human carnitine/acylcarnitine translocase in Aspergillus nidulans. Fungal Genet. Biol. 39 (2003) 211-220
59. Camacho J.A., Obie C., Biery B., Goodman B.K., Hu C.A., Almashanu S., Steel G., Casey R., Lambert M., Mitchell G.A., and Valle D. Hyperornithinaemia-hyperammonaemia-homocitrullinuria syndrome is caused by mutations in a gene encoding a mitochondrial ornithine transporter. Nat. Genet. 22 (1999) 151-158
60. Indiveri C., Tonazzi A., and Palmieri F. Identification and purification of the ornithine/citrulline carrier from rat liver mitochondria. Eur. J. Biochem. 207 (1992) 449-454
61. Palmieri L., De Marco V., Iacobazzi V., Palmieri F., Runswick M.J., and Walker J.E. Identification of the yeast ARG-11 gene as a mitochondrial ornithine carrier involved in arginine biosynthesis. FEBS Lett. 410 (1997) 447-451
62. Fiermonte G., Dolce V., David L., Santorelli F.M., Dionisi-Vici C., Palmieri F., and Walker J.E. The mitochondrial ornithine transporter. Bacterial expression, reconstitution, functional characterization, and tissue distribution of two human isoforms. J. Biol. Chem. 278 (2003) 32778-32783
63. Kuo F.C., Hwu W.L., Valle D., and Darnell Jr. J.E. Colocalization in pericentral hepatocytes in adult mice and similarity in developmental expression pattern of ornithine aminotransferase and glutamine synthetase mRNA. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 9468-9472
64. Indiveri C., Tonazzi A., Stipani I., and Palmieri F. The purified and reconstituted ornithine/citrulline carrier from rat liver mitochondria: electrical nature and coupling of the exchange reaction with H+ translocation. Biochem. J. 327 (1997) 349-355
65. Salvi S., Santorelli F.M., Bertini E., Boldrini R., Meli C., Donati A., Burlina A.B., Rizzo C., Di Capua M., Fariello G., and Dionisi-Vici C. Clinical and molecular findings in hyperornithinemia-hyperammonemia-homocitrullinuria syndrome. Neurology 57 (2001) 911-914
66. Camacho J., Mardach R., Rioseco-Camacho N., Ruiz-Pesini E., Derbeneva O., Andrade D., Zaldivar F., Qu Y., and Cederbaum S.D. Clinical and functional characterization of a human ORNT1 mutation (T32R) in the hyperornithinemia-hyperammonemia-homocitrullinuria (HHH) syndrome. Pediatr. Res. 60 (2006) 423-429
67. Shih V.E., Efron M.L., and Moser H.W. Hyperornithinemia, hyperammonemia, and homocitrullinuria. A new disorder of amino acid metabolism associated with myoclonic seizures and mental retardation. Am. J. Dis. Child. 117 (1969) 83-92
68. A. Tessa, G. Fiermonte, C. Dionisi-Vici, E. Paradies, M.R. Baumgartner, Y.H. Chien, S. Fecarotta, C. Loguercio, H. Ogier de Baulny, M.C. Nassogne, F. Deodato, G. Parenti, S.L. Rutledge, M.A. Villaseca, G. Scarano, C.L. Pierri, F. Palmieri, F.M. Santorelli, Identification of novel mutations in the SLC25A15 gene in hyperornithinemia, hyperammonemia, and homocitrullinuria (HHH) syndrome: a clinical, molecular and functional study. Under submission.
69. Lu Y.B., Kobayashi K., Ushikai M., Tabata A., Iijima M., Li M.X., Lei L., Kawabe K., Taura S., Yang Y., Liu T.T., Chiang S.H., Hsiao K.J., Lau Y.L., Tsui L.C., Lee D.H., and Saheki T. Frequency and distribution in East Asia of 12 mutations identified in the SLC25A13 gene of Japanese patients with citrin deficiency. J. Hum. Genet. 50 (2005) 338-346
70. Kobayashi K., Sinasac D.S., Iijima M., Boright A.P., Begum L., Lee J.R., Yasuda T., Ikeda S., Hirano R., Terazono H., Crackower M.A., Kondo I., Tsui L.C., Scherer S.W., and Saheki T. The gene mutated in adult-onset type II citrullinaemia encodes a putative mitochondrial carrier protein. Nat. Genet. 22 (1999) 159-163
71. 2+-stimulated aspartate/glutamate transporters in mitochondria. EMBO J. 20 (2001) 5060-5069
72. del Arco A., Agudo M., and Satrústegui J. Characterization of a second member of the subfamily of calcium-binding mitochondrial carriers expressed in human non-excitable tissues. Biochem. J. 345 (2000) 725-732
73. Iijima M., Jalil A., Begum L., Yasuda T., Yamaguchi N., Xian Li M., Kawada N., Endou H., Kobayashi K., and Saheki T. Pathogenesis of adult-onset type II citrullinemia caused by deficiency of citrin, a mitochondrial solute carrier protein: tissue and subcellular localization of citrin. Adv. Enzyme Regul. 41 (2001) 325-342
74. Lasorsa F.M., Pinton P., Palmieri L., Fiermonte G., Rizzuto R., and Palmieri F. Recombinant expression of the Ca2+-sensitive aspartate/glutamate carrier increases mitochondrial ATP production in agonist-stimulated Chinese hamster ovary cells. J. Biol. Chem. 278 (2003) 38686-38692
75. Kobayashi K., Shaheen N., Kumashiro R., Tanikawa K., O'Brien W.E., Beaudet A.L., and Saheki T. A search for the primary abnormality in adult-onset type II citrullinemia. Am. J. Hum. Genet. 53 (1993) 1024-1030
76. Kobayashi K., Kakinoki H., Fukushige T., Shaheen N., Terazono H., and Saheki T. Nature and frequency of mutations in the argininosuccinate synthetase gene that cause classical citrullinemia. Hum. Genet. 96 (1995) 454-463
77. Ohura T., Kobayashi K., Tazawa Y., Nishi I., Abukawa D., Sakamoto O., Iinuma K., and Saheki T. Neonatal presentation of adult-onset type II citrullinemia. Hum. Genet. 108 (2001) 87-90
78. Dimmock D., Kobayashi K., Iijima M., Tabata A., Wong L.J., Saheki T., Lee B., and Scaglia F. Citrin deficiency: a novel cause of failure to thrive that responds to a high-protein, low-carbohydrate diet. Pediatrics 119 (2007) 773-777
79. Moriyama M., Li M.X., Kobayashi K., Sinasac D.S., Kannan Y., Iijima M., Horiuchi M., Tsui L.C., Tanaka M., Nakamura Y., and Saheki T. Pyruvate ameliorates the defect in ureogenesis from ammonia in citrin-deficient mice. J. Hepatol. 44 (2006) 930-938
80. Yasuda T., Yamaguchi N., Kobayashi K., Nishi I., Horinouchi H., Jalil M.A., Li M.X., Ushikai M., Iijima M., Kondo I., and Saheki T. Identification of two novel mutations in the SLC25A13 gene and detection of seven mutations in 102 patients with adult-onset type II citrullinemia. Hum. Genet. 107 (2000) 537-545
81. Fiermonte G., Soon D., Chaudhuri A., Paradies E., Lee P.J., Krywawych S., Palmieri F., and Lachmann R.H. An adult with type II citrullinemia presenting in Europe. New Engl. J. Med. 338 (2008) 1408-1409
82. Cappello A.R., Curcio R., Miniero D.V., Stipani I., Robinson A.J., Kunji E.R.S., and Palmieri F. Functional and structural role of amino acid residues in the even-numbered transmembrane α-helices of the bovine mitochondrial oxoglutarate carrier. J. Mol. Biol. 363 (2006) 51-62
83. Verdonk M.L., Cole J.C., Hartshorn M.J., Murray C.W., and Taylor R.D. Improved protein-ligand docking using GOLD. Proteins 52 (2003) 609-623
84. Sinasac D.S., Moriyama M., Jalil M.A., Begum L., Li M.X., Iijima M., Horiuchi M., Robinson B.H., Kobayashi K., Saheki T., and Tsui L.C. Slc25a13-knockout mice harbor metabolic deficits but fail to display hallmarks of adult-onset type II citrullinemia. Mol. Cell. Biol. 24 (2004) 527-536
85. Saheki T., Iijima M., Li M.X., Kobayashi K., Horiuchi M., Ushikai M., Okumura F., Meng X.J., Inoue I., Tajima A., Moriyama M., Eto K., Kadowaki T., Sinasac D.S., Tsui L.C., Tsuji M., Okano A., and Kobayashi T. Citrin/mitochondrial glycerol-3-phosphate dehydrogenase double-knockout mice recapitulate features of human citrin deficiency. J. Biol. Chem. 282 (2007) 25041-25052
86. Kelley R.I., Robinson D., Puffenberger E.G., Strauss K.A., and Morton D.H. Amish lethal microcephaly: a new metabolic disorder with severe congenital microcephaly and 2-ketoglutaric aciduria. Am. J. Med. Genet. 112 (2002) 318-326
87. Rosenberg M.J., Agarwala R., Bouffard G., Davis J., Fiermonte G., Hilliard M.S., Koch T., Kalikin L.M., Makalowska I., Morton D.H., Petty E.M., Weber J.L., Palmieri F., Kelley R.I., Schäffer A.A., and Biesecker L.G. Mutant deoxynucleotide carrier is associated with congenital microcephaly. Nat. Genet. 32 (2002) 175-179
88. Dolce V., Fiermonte F., Runswick M.J., Palmieri F., and Walker J.E. The human mitochondrial deoxynucleotide carrier and its role in toxicity of nucleoside antivirals. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 2284-2288
89. Lindhurst M.J., Fiermonte G., Song S., Struys E., De Leonardis F., Schwartzberg P.L., Chen A., Castegna A., Verhoeven N., Mathews C.K., Palmieri F., and Biesecker L.G. Knockout of Slc25a19 causes mitochondrial thiamine pyrophosphate depletion, embryonic lethality, CNS malformations, and anemia. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 15927-15932
90. Iacobazzi V., Ventura M., Fiermonte G., Prezioso G., Rocchi M., and Palmieri F. Genomic organization and mapping of the gene (SLC25A19) encoding the human mitochondrial deoxynucleotide carrier (DNC). Cytogenet. Cell Genet. 93 (2001) 40-42
91. Molinari F., Raas-Rothschild A., Rio M., Fiermonte G., Encha-Razavi F., Palmieri L., Palmieri F., Ben-Neriah Z., Khadom N., Vekemans M., Attié-Bitach T., Munnich A., Rustin P., and Colleaux L. Impaired mitochondrial glutamate transport in autosomal recessive neonatal myoclonic epilepsy. Am. J. Hum. Genet. 76 (2005) 334-339
92. Fiermonte G., Palmieri L., Todisco S., Agrimi G., Palmieri F., and Walker J.E. Identification of the mitochondrial glutamate transporter. Bacterial expression, reconstitution, functional characterization, and tissue distribution of two human isoforms. J. Biol. Chem. 277 (2002) 19289-19294
93. Berkich D.A., Ola M.S., Cole J., Sweatt A.J., Hutson S.M., and LaNoue K.F. Mitochondrial transport proteins of the brain. J. Neurosci. Res. 85 (2007) 3367-3377
94. Ramos M., del Arco A., Pardo B., Martínez-Serrano A., Martínez-Morales J.R., Kobayashi K., Yasuda T., Bogónez E., Bovolenta P., Saheki T., and Satrústegui J. Developmental changes in the Ca2+-regulated mitochondrial aspartate-glutamate carrier aralar1 in brain and prominent expression in the spinal cord. Brain Res. Dev. Brain Res. 143 (2003) 33-46