Calcium-induced conformational changes of the regulatory domain of human mitochondrial aspartate/glutamate carriers

Nature Communications

Volumn 5, Issue , 2014, Pages

  Thangaratnarajah, Chancievan ^a   Ruprecht, Jonathan J ^a   Kunji, Edmund R S ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; CALCIUM; GLUTAMIC ACID; MALIC ACID; CARRIER PROTEIN; SLC25A12 PROTEIN, HUMAN; SLC25A13 PROTEIN, HUMAN;

CALCIUM; CHEMICAL BONDING; DISEASE INCIDENCE; MITOCHONDRION; SUBSTRATE;

AMINO TERMINAL SEQUENCE; ARTICLE; CALCIUM BINDING; CARBOXY TERMINAL SEQUENCE; COMPARATIVE STUDY; CONFORMATION; CONFORMATIONAL TRANSITION; CRYSTALLIZATION; DIMERIZATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GLUCONEOGENESIS; HUMAN; HUMAN CELL; HYDROGEN BOND; LIGHT SCATTERING; MITOCHONDRION; MYELINATION; PROTEIN MOTIF; UREA CYCLE; METABOLISM; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

ASPARTIC ACID; CALCIUM; CRYSTALLOGRAPHY, X-RAY; GLUTAMIC ACID; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY;

EID: 84923239495     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6491     Document Type: Article

References (70)

1. LaNoue, K. F. & Tischler, M. E. Electrogenic characteristics of the mitochondrial glutamate-aspartate antiporter. J. Biol. Chem. 249, 7522-7528 (1974).
2. LaNoue, K. F., Bryla, J. & Bassett, D. J. Energy-driven aspartate efflux from heart and liver mitochondria. J. Biol. Chem. 249, 7514-7521 (1974).
3. LaNoue, K. F., Meijer, A. J. & Brouwer, A. Evidence for electrogenic aspartate transport in rat liver mitochondria. Arch. Biochem. Biophys. 161, 544-550 (1974).
4. Dierks, T. & Krämer, R. Asymmetric orientation of the reconstituted aspartate/glutamate carrier from mitochondria. Biochim. Biophys. Acta 937, 112-126 (1988).
5. Dierks, T., Riemer, E. & Krämer, R. Reaction mechanism of the reconstituted aspartate/glutamate carrier from bovine heart mitochondria. Biochim. Biophys. Acta 943, 231-244 (1988).
6. Palmieri, L. et al. Citrin and aralar1 are Ca(2+)-stimulated aspartate/glutamate transporters in mitochondria. EMBO J. 20, 5060-5069 (2001).
7. Azzi, A., Chappell, J. B. & Robinson, B. H. Penetration of the mitochondrial membrane by glutamate and aspartate. Biochem. Biophys. Res. Commun. 29, 148-152 (1967).
8. Del Arco, A. & Satrústegui, J. Molecular cloning of Aralar, a new member of the mitochondrial carrier superfamily that binds calcium and is present in human muscle and brain. J. Biol. Chem. 273, 23327-23334 (1998).
9. Kobayashi, K. et al. The gene mutated in adult-onset type II citrullinaemia encodes a putative mitochondrial carrier protein. Nat. Genet. 22, 159-163 (1999).
10. Del Arco, A., Agudo, M. & Satrústegui, J. Characterization of a second member of the subfamily of calcium-binding mitochondrial carriers expressed in human non-excitable tissues. Biochem. J. 345(Pt 3): 725-732 (2000).
11. LaNoue, K. F. & Schoolwerth, A. C. Metabolite transport in mitochondria. Annu. Rev. Biochem. 48, 871-922 (1979).
12. Borst, P. Hydrogen Transport And Transport Metabolites. in Funktionelle und Morphologische Organisation der Zelle (ed. Karson, P.) 137-162 (Springer Verlag, 1963).
13. Williamson, J. R. in Gluconeogenesis: Its Regulation in Mammalian Species (eds Hanson, R. & Mehlman, M.) 165-220 (John Wiley, 1976).
14. Meijer, A. J. et al. Interrelationships between gluconeogenesis and ureogenesis in isolated hepatocytes. J. Biol. Chem. 253, 2308-2320 (1978).
15. Jalil, M. A. et al. Reduced N-acetylaspartate levels in mice lacking aralar, a brain- and muscle-type mitochondrial aspartate-glutamate carrier. J. Biol. Chem. 280, 31333-31339 (2005).
16. Wibom, R. et al. AGC1 deficiency associated with global cerebral hypomyelination. New Engl. J. Med. 361, 489-495 (2009).
17. 2+ Activation kinetics of the two aspartate-glutamate mitochondrial carriers, aralar and citrin: role in the heart malate-aspartate NADH shuttle. J. Biol. Chem. 282, 7098-7106 (2007).
18. 2+-sensitive aspartate/glutamate carrier increases mitochondrial ATP production in agonist-stimulated chinese hamster ovary cells. J. Biol. Chem. 278, 38686-38692 (2003).
19. 2+ signals to neuronal mitochondria. J. Biol. Chem. 281, 1039-1047 (2006).
20. 2+-binding sites in Ca2+ signal transduction in mitochondria from INS-1 clonal beta-cells. J. Biol. Chem. 284, 515-524 (2009).
21. Pebay-Peyroula, E. et al. Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426, 39-44 (2003).
22. Ruprecht, J. J. et al. Structures of yeast mitochondrial ADP/ATP carriers support a domain-based alternating-access transport mechanism. Proc. Natl Acad. Sci. USA 111, E426-E434 (2014).
23. Kunji, E. R. & Harding, M. Projection structure of the atractyloside-inhibited mitochondrial ADP/ATP carrier of Saccharomyces cerevisiae. J. Biol. Chem. 278, 36985-36988 (2003).
24. Bamber, L., Harding, M., Butler, P. J. & Kunji, E. R. Yeast mitochondrial ADP/ATP carriers are monomeric in detergents. Proc. Natl Acad. Sci. USA 103, 16224-16229 (2006).
25. Bamber, L., Harding, M., Monne, M., Slotboom, D. J. & Kunji, E. R. The yeast mitochondrial ADP/ATP carrier functions as a monomer in mitochondrial membranes. Proc. Natl Acad. Sci. USA 104, 10830-10834 (2007).
26. Nury, H. et al. Mitochondrial bovine ADP/ATP carrier in detergent is predominantly monomeric but also forms multimeric species. Biochemistry 47, 12319-12331 (2008).
27. Kunji, E. R. & Crichton, P. G. Mitochondrial carriers function as monomers. Biochim. Biophys. Acta 1797, 817-831 (2010).
28. Chae, P. S. et al. Maltose-neopentyl glycol (MNG) amphiphiles for solubilization, stabilization and crystallization of membrane proteins. Nat. Methods 7, 1003-1008 (2010).
29. Slotboom, D. J., Duurkens, R. H., Olieman, K. & Erkens, G. B. Static light scattering to characterize membrane proteins in detergent solution. Methods 46, 73-82 (2008).
30. Robinson, A. J., Overy, C. & Kunji, E. R. The mechanism of transport by mitochondrial carriers based on analysis of symmetry. Proc. Natl Acad. Sci. USA 105, 17766-17771 (2008).
31. Miroux, B., Frossard, V., Raimbault, S., Ricquier, D. & Bouillaud, F. The topology of the brown adipose tissue mitochondrial uncoupling protein determined with antibodies against its antigenic sites revealed by a library of fusion proteins. EMBO J. 12, 3739-3745 (1993).
32. Capobianco, L., Brandolin, G. & Palmieri, F. Transmembrane topography of the mitochondrial phosphate carrier explored by peptide-specific antibodies and enzymatic digestion. Biochemistry 30, 4963-4969 (1991).
33. Yap, K. L., Ames, J. B., Swindells, M. B. & Ikura, M. Diversity of conformational states and changes within the EF-hand protein superfamily. Proteins Struct. Funct. Genet. 37, 499-507 (1999).
34. 2+-binding helix-loop-helix EF-hand motifs. Biochem. J. 405, 199-221 (2007).
35. Kirberger, M. et al. Integration of Diverse Research Methods to Analyze and Engineer Ca-Binding Proteins: From Prediction to Production. Curr. Bioinform. 5, 68-80 (2010).
36. Kretsinger, R. H., Rudnick, S. E. & Weissman, L. J. Crystal structure of calmodulin. J. Inorg. Biochem. 28, 289-302 (1986).
37. Meador, W. E., Means, A. R. & Quiocho, F. A. Target enzyme recognition by calmodulin: 2.4 A structure of a calmodulin-peptide complex. Science 257, 1251-1255 (1992).
38. Réty, S. et al. The crystal structure of a complex of p11 with the annexin II N-terminal peptide. Nat. Struct. Biol. 6, 89-95 (1999).
39. Réty, S. et al. Structural basis of the Ca(2+)-dependent association between S100C (S100A11) and its target, the N-terminal part of annexin I. Structure 8, 175-184 (2000).
40. Song, Y. Z. et al. SLC25A13 gene analysis in citrin deficiency: sixteen novel mutations in East Asian patients, and the mutation distribution in a large pediatric cohort in China. PLoS ONE 8, e74544 (2013).
41. Dimmock, D. et al. Citrin deficiency, a perplexing global disorder. Mol. Genet. Metab. 96, 44-49 (2009).
42. Woo, H. I., Park, H. D. & Lee, Y. W. Molecular genetics of citrullinemia types I and II. Clin. Chim. Acta 431C, 1-8 (2014).
43. Saheki, T., Inoue, K., Tushima, A., Mutoh, K. & Kobayashi, K. Citrin deficiency and current treatment concepts. Mol. Genet. Metab. 100(Suppl 1): S59-S64 (2010).
44. Saheki, T. et al. Pathogenesis and pathophysiology of citrin (a mitochondrial aspartate glutamate carrier) deficiency. Metab. Brain Dis. 17, 335-346 (2002).
45. Liu, G. et al. A novel mutation of the SLC25A13 gene in a Chinese patient with citrin deficiency detected by target next-generation sequencing. Gene 533, 547-553 (2014).
46. Zhang, Z. H. et al. Clinical, molecular and functional investigation on an infant with neonatal intrahepatic cholestasis caused by citrin deficiency (NICCD). PLoS ONE 9, e89267 (2014).
47. Fu, H. Y. et al. The mutation spectrum of the SLC25A13 gene in Chinese infants with intrahepatic cholestasis and aminoacidemia. J. Gastroenterol. 46, 510-518 (2011).
48. Kunji, E. R., Slotboom, D. J. & Poolman, B. Lactococcus lactis as host for overproduction of functional membrane proteins. Biochim. Biophys. Acta 1610, 97-108 (2003).
49. Nurizzo, D. et al. The ID23-1 structural biology beamline at the ESRF. J. Synchrotron. Radiat. 13, 227-238 (2006).
50. Flot, D. et al. The ID23-2 structural biology microfocus beamline at the ESRF. J. Synchrotron. Radiat. 17, 107-118 (2010).
51. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
52. Kabsch, W. Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr. D Biol. Crystallogr. 66, 133-144 (2010).
53. Evans, P. R. An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr. D Biol. Crystallogr. 67, 282-292 (2011).
54. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242 (2011).
55. Schneider, T. R. & Sheldrick, G. M. Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58, 1772-1779 (2002).
56. Vonrhein, C., Blanc, E., Roversi, P. & Bricogne, G. Automated structure solution with autoSHARP. Methods Mol. Biol. 364, 215-230 (2007).
57. Cowtan, K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62, 1002-1011 (2006).
58. Cowtan, K. Fitting molecular fragments into electron density. Acta Crystallogr. D Biol. Crystallogr. 64, 83-89 (2008).
59. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
60. Murshudov, G. N. et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367 (2011).
61. Afonine, P. V. et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D Biol. Crystallogr. 68, 352-367 (2012).
62. Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta. Crystallogr. D. Biol. Crystallogr. 66, 12-21 (2010).
63. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
64. Gasteiger, E. et al. in The Proteomics Protocols Handbook (ed. Walker, J. M.) 571-607 (Humana Press, 2005).
65. Bunkoczi, G. & Read, R. J. Improvement of molecular-replacement models with Sculptor. Acta Crystallogr. D Biol. Crystallogr. 67, 303-312 (2011).
66. Terwilliger, T. C. et al. Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard. Acta Crystallogr. D Biol. Crystallogr. 64, 61-69 (2008).
67. Terwilliger, T. C. Maximum-likelihood density modification. Acta Crystallogr. D Biol. Crystallogr 56, 965-972 (2000).
68. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
69. Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 (2007).
70. Hayward, S. & Berendsen, H. J. Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme. Proteins 30, 144-154 (1998).