The calcium-binding aspartate/glutamate carriers, citrin and aralar1, are new substrates for the DDP1/TIMM8a-TIMM13 complex

Human Molecular Genetics

Volumn 13, Issue 18, 2004, Pages 2101-2111

  Roesch, Karin ^a   Hynds, Peter J ^a   Varga, Renee ^b,d   Tranebjaerg, Libeth ^c   Koehler, Carla M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BOYS TOWN NATIONAL RESEARCH HOSPITAL   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARALAR 1; ASPARTIC ACID; CALCIUM BINDING PROTEIN; CALCIUM ION; CARRIER PROTEIN; DEAFNESS DYSTONIA PROTEIN 1; ERIODICTYOL 7 O GLUCOSIDE; GLUTAMIC ACID; MALIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; TRANSLOCASE OF INNER MITOCHONDRIAL MEMBRANE 13; TRANSLOCASE OF INNER MITOCHONDRIAL MEMBRANE 8A; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CASE REPORT; CENTRAL NERVOUS SYSTEM; COMPLEX FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CROSS LINKING; CYTOSOL; DEAFNESS DYSTONIA SYNDROME; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTRACELLULAR TRANSPORT; LYMPHOBLAST; MITOCHONDRIAL MEMBRANE; MOHR TRANEBJAERG SYNDROME; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; X CHROMOSOME LINKED DISORDER;

ANIMALS; CALCIUM-BINDING PROTEINS; CELL LINE; DEAFNESS; DYSTONIA; HEREDODEGENERATIVE DISORDERS, NERVOUS SYSTEM; HUMANS; IMMUNOPRECIPITATION; INTRACELLULAR MEMBRANES; MEMBRANE TRANSPORT PROTEINS; MICE; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL PROTEINS; ORGANIC ANION TRANSPORTERS; PURKINJE CELLS; SACCHAROMYCES CEREVISIAE; SYNDROME;

MAMMALIA;

EID: 5744230324     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddh217     Document Type: Article

References (57)

1. Tranebjaerg, L., Schwartz, C., Eriksen, H., Andreasson, S., Ponjavic, V., Dahl A., Stevenson, R.E., May, M., Arena, F., Barker, D. et al. (1995) A new X linked recessive deafness syndrome with blindness, dystonia, fractures, and mental deficiency is linked to Xq22. J. Med. Genet., 32, 257-263.
2. Jin, H., May, M., Tranebjaerg, L., Kendall, E., Fontan, G., Jackson, J., Subramony, S.H., Arena, F., Lubs, H., Smith, S. et al. (1996) A novel X-linked gene, DDP, shows mutations in families with deafness (DFN-1), dystonia, mental deficiency and blindness. Nat. Genet., 14, 177-180.
3. Tranebjaerg, L., Jensen, P.K., Van Ghelue, M., Vnencak-Jones, C.L., Sund, S., Elgjo, K., Jakobsen, J., Lindal, S., Warburg, M., Fuglsang-Frederiksen, A. et al. (2001) Neuronal cell death in the visual cortex is a prominent feature of the X-linked recessive mitochondrial deafness-dystonia syndrome caused by mutations in the TIMM8a gene. Ophthalmic Genet., 22, 207-223.
4. Wallace, D.C. (1999) Mitochondrial diseases in man and mouse. Science, 283, 1482-1488.
5. Roesch, K., Curran, S.P., Tranebjaerg, L. and Koehler, C.M, (2002) Human deafness dystonia syndrome is caused by a defect in assembly of the DDP1/TIMM8a-TIMM13 complex. Hum. Mol. Genet., 11, 477-486.
6. Binder, J., Hofmann, S., Kreisel, S., Wohrle, J.C., Bazner, H., Krauss, J.K., Hennerici, M.G. and Bauer, M.F. (2003) Clinical and molecular findings in a patient with a novel mutation in the deafness-dystonia peptide (DDP1) gene. Brain, 126, 1814-1820.
7. Koehler, C.M. (2004) The small Tim proteins and the twin Cx3C motif. Trends Biochem. Sci., 29, 1-4.
8. Curran, S.P., Leuenberger, D., Oppliger, W. and Koehler, C.M. (2002) The Tim9p-Tim10p complex binds to the transmembrane domains of the ADP-ATP carrier. EMBO J., 21, 942-953.
9. Curran, S.P., Leuenberger, D., Schmidt, E. and Koehler, C.M. (2002) The role of the Tim8p-Tim13p complex in a conserved import pathway for mitochondrial polytopic inner membrane proteins. J. Cell Biol., 158, 1017-1027.
10. Lutz, T., Neupert, W. and Herrmann, J.M. (2003) Import of small Tim proteins into the mitochondrial intermembrane space. EMBO J. 22, 4400-4408.
11. Lu, H., Allen, S., Wardleworth, L., Savory, P. and Tokatlidis, K. (2004) Functional TIM10 chaperone assembly is redox-regulated in vivo. J. Biol. Chem., 279, 18952-18958.
12. Lu, H., Golovanov, A.P., Alcock, F., Grossmann, J.G., Allen, S., Lian, L.Y. and Tokatlidis, K. (2004) The structural basis of the TIM10 chaperone sssembly. J. Biol. Chem., 279, 18959-18966.
13. Koehler, C.M., Leuenberger, D., Merchant, S., Renold, A., Junne, T. and Schatz., G. (1999) Human deafness dystonia syndrome is a mitochondrial disease. Proc. Natl Acad. Sci. USA, 96, 2141-2146.
14. Davis, A.J., Sepuri, N.B., Holder, J., Johnson, A.E. and Jensen, R.E. (2000) Two intermembrane space TIM complexes interact with different domains of Tim23p during its import into mitochondria. J. Cell Biol., 150, 1271-1282.
15. Paschen, S.A., Rothbauer, U., Kaldi, K., Bauer, M.F., Neupert, W. and Brunner, M. (2000) The role of the TIM8-13 complex in the import of Tim23 into mitochondria. EMBO J., 19, 6392-6400.
16. Koehler, C.M., Merchant, S., Oppliger, W., Schmid, K., Jarosch, E., Dolfini, L., Junne, T., Schatz, G. and Tokatlidis, K. (1998) Tim9p, an essential partner subunit of Tim10p for the import of mitochondrial carrier proteins. EMBO J., 17, 6477-6486.
17. Adam, A., Endres, M., Sirrenberg, C., Lottspeich, F., Neupert, W. and Brunner, M. (1999) Tim9, a new component of the TIM22.54 translocase in mitochondria. EMBO J., 18, 313-319.
18. Murphy, M.P., Leuenberger, D., Curran, S.P., Oppliger, W. and Koehler, C.M. (2001) The essential function of the small Tim proteins in the TIM22 import pathway does not depend on formation of the soluble 70-kilodalton complex. Mol. Cell. Biol., 21, 6132-6138.
19. Rothbauer, U., Hofmann, S., Muhlenbein, N., Paschen, S.A., Gerbitz, K.D., Neupert, W., Brunner, M. and Bauer, M.F. (2001) Role of the deafness dystonia peptide 1 (DDP1) in import of human Tim23 into the inner membrane of mitochondria. J. Biol. Chem., 276, 37327-37334.
20. Muhlenbein, N., Hofmann, S., Rothbauer, U. and Bauer, M.F. (2004) Organization and function of the small Tim complexes acting along the import pathway of metabolite carriers into mammalian mitochondria. J. Biol. Chem., 279, 13540-13546.
21. Leuenberger, D., Bally, N.A., Schatz, G. and Koehler, C.M. (1999) Different import pathways through the mitochondrial intermembrane space for inner membrane proteins. EMBO J., 17, 4816-4822.
22. Endres, M., Neupert, W. and Brunner, M. (1999) Transport of the ADP/ATP carrier of mitochondria from the TOM complex to the TIM22.54 complex. EMBO J., 18, 3214-3221.
23. Hoppins, S.C. and Nargang, F.E. (2004) The Tim8-Tim13 complex of Neurospora crassa functions in the assembly of proteins into both mitochondrial membranes. J. Biol. Chem., 279, 12396-12405.
24. Wiedemann, N., Truscott, K.N., Pfannschmidt, S., Guiard, B., Meisinger, C. and Pfanner, N. (2004) Biogenesis of the protein import channel Tom40 of the mitochondrial outer membrane: Intermembrane space components are involved in an early stage of the assembly pathway. J. Biol. Chem., 279, 18188-18194.
25. Palmieri, L., Pardo, B., Lasorsa, F.M., del Arco, A., Kobayashi, K., Iijima, M., Runswick, M.J., Walker, J.E., Saheki, T., Satrustegui, J. et al. (2001) Citrin and aralar1 are Ca(2+)-stimulated aspartate/glutamate transporters in mitochondria. EMBO J., 20, 5060-5069.
26. Cavero, S., Vozza, A., del Arco, A., Palmieri, L., Villa, A., Blanco, E., Runswick, M.J., Walker, J.E., Cerdan, S., Palmieri, F. et al. (2003) Identification and metabolic role of the mitochondrial aspartate-glutamate transporter in Saccharomyces cerevisiae. Mol. Microbiol., 50, 1257-1269.
27. Del Arco, A., Agudo, M. and Satrustegui, J. (2000) Characterization of a second member of the subfamily of calcium-binding mitochondrial carriers expressed in human non-excitable tissues. Biochem. J., 345, 725-732.
28. Tranebjaerg, L., Hamel, B.C., Gabreels, F.J., Reiner, W.O. and Van Ghelue, M. (2000) A de novo missense mutation in a critical domain of the X-linked DDP gene causes the typical deafness-dystonia-optic atrophy syndrome. Eur. J. Hum. Genet., 8, 464-467.
29. Swerdlow, R.H. and Wooten, G.F. (2001) A novel deafness/dystonia peptide gene mutation that causes dystonia in female carriers of Mohr-Tranebjaerg syndrome. Ann. Neurol., 50, 537-540.
30. Merchant, S.N., McKenna, M.J., Nadol, J.B., Kristiansen, A.G., Tropitzsch, A., Lindal, S. and Tranebjaerg, L. (2001) Temporal bone histopathologic and genetic studies in Mohr-Tranebjaerg Syndrome (DFN-1). Otol. Neurotol., 22, 506-511.
31. Ishihara, N. and Mihara, K. (1998) Identification of the protein import components of the rat mitochondrial inner membrane, rTIM17, rTIM23, and rTIM44. J. Biochem., 123, 722-732.
32. Bauer, M.F., Gempel, K., Reichert, A.S., Rappold, G.A., Lichtner, P., Gerbitz, K.D., Neupert, W., Brunner, M. and Hofmann, S. (1999) Genetic and structural characterization of the human mitochondrial inner membrane translocase. J. Mol. Biol., 289, 69-82.
33. Rodrigo, J., Alonso, D., Fernandez, A.P., Serrano, J., Richart, A., Lopez, J.C., Santacana, M., Martinez-Murillo, R., Bentura, M.L., Ghiglione, M. et al. (2001) Neuronal and inducible nitric oxide synthase expression and protein nitration in rat cerebellum after oxygen and glucose deprivation. Brain Res., 909, 20-45.
34. Sanz, R., del Arco, A., Ayuso, C., Ramos, C. and Satrustegui, J. (2000) Assignment of the calcium-binding mitochondrial carrier Aralar1 gene (SLC25A12) to human chromosome band 2q31 by in situ hybridization. Cytogenet. Cell Genet., 89, 143-144.
35. del Arco, A., Morcillo, J., Martinez-Morales, J.R., Galian, C., Martos, V., Bovolenta, P. and Satrustegui, J. (2002) Expression of the aspartate/glutamate mitochondrial carriers aralar1 and citrin during development and in adult rat tissues. Eur. J. Biochem., 269, 3313-3320.
36. Ramos, M., del Arco, A., Pardo, B., Martinez-Serrano, A., Martinnez-Morales, J.R., Kobayashi, K., Yasuda, T., Bogonez, E., Bovolenta, P., Saheki, T. et al. (2003) Developmental changes in the Ca(2+)-regulated mitochondrial aspartate-glutamate carrier aralar1 in brain and prominent expression in the spinal cord. Dev. Brain Res., 143, 33-46.
37. Kobayashi, K., Sinasac, D.S., Iijima, M., Boright, A.P., Begum, L., Lee, J.R., Yasuda, T., Ikeda, S., Hirano, R., Terazono, H. et al. (1999) The gene mutated in adult-onset type II citrullinaemia encodes a putative mitochondrial carrier protein. Nat. Genet., 22, 159-163.
38. Hofmann, S., Rothbauer, U., Muhlenbein, N., Neupert, W., Gerbitz, K.D., Brunner, M. and Bauer, M.F. (2002) The C66W mutation in the deafness dystonia peptide 1 (DDP1) affects the formation of functional DDP1.TIM13 complexes in the mitochondrial intermembrane space. J. Biol. Chem., 277, 23287-23893.
39. Davis, A.J., Ryan, K.R. and Jensen, R.E. (1998) Tim23p contains separate and distinct signals for targeting to mitochondria and insertion into the inner membrane. Mol. Biol. Cell, 9, 2577-2693.
40. Del Arco, A. and Satrustegui, J. (2004) Identification of a novel human subfamily of mitochondrial carriers with calcium-binding domains. J. Biol. Chem., 279, 24701-24713.
41. Koehler, C.M., Jarosch, E., Tokatlidis, K., Schmid, K., Schweyen, R.J. and Schatz, G. (1998) Import of mitochondrial carriers mediated by essential proteins of the intermembrane space. Science, 279, 369-373.
42. Rehling, P., Model, K., Brandner, K., Kovermann, P., Sickmann, A., Meyer, H.E., Kuhlbrandt, W., Wagner, R., Truscott, K.N. and Pfanner, N. (2003) Protein insertion into the mitochondrial inner membrane by a twin-pore translocase. Science, 299, 1747-1751.
43. Bourgeron, T., Chretien, D., Rotig, A., Munnich, A. and Rustin, P. (1992) Isolation and characterization of mitochondria from human B lymphoblastoid cell lines. Biochem. Biophys. Res. Commun., 186, 16-23.
44. Wong-Riley, M.T. (1989) Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci., 12, 94-101.
45. Palmieri, F. (1994) Mitochondrial carrier proteins. FEBS Lett., 346, 48-54.
46. Brix, J., Rudiger, S., Bukau, B., Schneider-Mergener, J. and Pfanner, N. (1999) Distribution of binding sequences for the mitochondrial import receptors Tom20, Tom22, and Tom70 in a presequence-carrying preprotein and a non-cleavable preprotein. J. Biol. Chem., 274, 16522-16530.
47. Inoue, T. (2003) Dynamics of calcium and its roles in the dendrite of the cerebellar Purkinje cell. Keio J. Med., 52, 244-249.
48. Lasorsa, F.M., Pinton, P., Palmieri, L., Fiermonte, G., Rizzuto, R. and Palmieri, F. (2003) Recombinant expression of the Ca(2+)-sensitive aspartate/glutamate carrier increases mitochondrial ATP production in agonist-stimulated Chinese hamster ovary cells. J. Biol. Chem., 278, 38686-38692.
49. Sinasac, D.S., Moriyami, M., Jalil, M.A., Begum, L., Li, M.X, Iijima, M., Horiuchi, M., Robinson, B.H., Kobayashi, K., Saheki, T. et al. (2004) Slc25a13-knockout mice harbor metabolic deficits but fail to display hallmarks of adult-onset type II citrullinemia. Mol. Biol. Cell, 24, 527-536.
50. Geitz, R.D. and Schiestl, R.H. (1991) Applications of high efficiency lithium acetate transformation of intact yeast cells using single-stranded nucleic acids as carrier. Yeast, 7, 253-263.
51. Guthrie, C. and Fink, G.R. (1991) Guide to Yeast Genetics and Molecular Biology. Academic Press, San Diego, CA.
52. Rospert, S. and Schatz, G. (1998) Protein translocation into mitochondria. In Celis, J.E. (ed.), Cell Biology: A Laboratory Handbook, 2nd edn. Academic Press, San Diego, Vol. 2, pp. 277-285.
53. Hofhaus, G., Shakeley, R.M. and Attardi, G. (1996) Use of polarography to detect respiration defects in cell cultures. Method. Enzymol., 264, 476-483.
54. Ishihara, N. and Mihara, K. (1998) Identification of the protein import components of the rat mitochondrial inner membrane, rTIM17, rTIM23, and rTIM44. J. Biochem., 123, 722-732.
55. Renold, A., Koehler, C.M. and Murphy, M.P. (2000) Mitochondrial import of the long and short isoforms of human uncoupling protein 3. FEBS Lett., 465, 135-140.
56. Wood, J.D., MacMillan, J.C., Harper, P.S., Lowenstein, P.R. and Jones, A.L. (1996) Partial characterisation of murine huntingtin and apparent variations in the subcellular localisation of huntingtin in human, mouse and rat brain. Hum. Mol. Genet., 5, 481-487.
57. Zhang, J.H., Sampogna, S., Morales, F.R. and Chase, M.H. (2001) Orexin (hypocretin)-like immunoreactivity in the cat hypothalamus: a light and electron microscopic study. Sleep, 24, 67-76.