Single-nucleotide evolution quantifies the importance of each site along the structure of mitochondrial carriers

Cellular and Molecular Life Sciences

Volumn 71, Issue 2, 2014, Pages 349-364

  Pierri, Ciro Leonardo ^a   Palmieri, Ferdinando ^a   De Grassi, Anna ^a,b  

^a UNIVERSITY OF BARI   (Italy)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Evolution; Mitochondrial carrier; PhyloP; Protein structure; Transporter

Indexed keywords

2 OXOGLUTARIC ACID; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CARRIER PROTEIN; GLYCINE; MITOCHONDRIAL CARRIER; PROLINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; BINDING SITE; ENZYME SPECIFICITY; EVOLUTIONARY RATE; GENETIC CODE; HUMAN; INTRACELLULAR TRANSPORT; MITOCHONDRIAL MEMBRANE; MOLECULAR EVOLUTION; NAMED INVENTORIES, QUESTIONNAIRES AND RATING SCALES; NUCLEOTIDE SEQUENCE; PHYLOP SCORE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; SINGLE NUCLEOTIDE POLYMORPHISM;

AMINO ACID MOTIFS; ANIMALS; BIOLOGICAL EVOLUTION; DATABASES, GENETIC; GENOME; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SUBSTRATE SPECIFICITY;

VERTEBRATA;

EID: 84903362773     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1389-y     Document Type: Article

References (57)

1. Pollard KS, Hubisz MJ, Rosenbloom KR, Siepel A (2010) Detection of non-neutral substitution rates on mammalian phylogenies. Genome Res 20:110-121
2. Veltman JA, Brunner HG (2012) De novo mutations in human genetic disease. Nat Rev Genet 13:565-575
3. Lyon GJ, Wang K (2012) Identifying disease mutations in genomic medicine settings: current challenges and how to accelerate progress. Genome Med 4:58
4. Timmermann B, Kerick M, Roehr C, Fischer A, Isau M et al (2010) Somatic mutation profiles of MSI and MSS colorectal cancer identified by whole exome next generation sequencing and bioinformatics analysis. PLoS One 5:e15661
5. Håndstad T, Rye MB, Drabløs F, Sætrom P (2011) A ChIP-Seq benchmark shows that sequence conservation mainly improves detection of strong transcription factor binding sites. PLoS One 6:e18430
6. Sterne-Weiler T, Howard J, Mort M, Cooper DN, Sanford JR (2011) Loss of exon identity is a common mechanism of human inherited disease. Genome Res 21:1563-1571
7. Palmieri F (2004) The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Arch 447:689-709 (Pubitemid 38241455)
8. Palmieri F (2013) The mitochondrial transporter family SLC25: identification, properties and physiopathology. Mol Aspects Med 34:465-484
9. Saraste M, Walker J (1982) Internal sequence repeats and the path of polypeptide in mitochondrial ADP/ATP translocase. FEBS Lett 144:250-254
10. Palmieri F (1994) Mitochondrial carrier proteins. FEBS Lett 346:48-54 (Pubitemid 24183826)
11. Pebay-Peyroula E, Dahout-Gonzalez C, Kahn R, Trézéguet V, Lauquin G et al (2003) Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426:39-44 (Pubitemid 37432535)
12. Berardi MJ, Shih WM, Harrison SC, Chou JJ (2011) Mitochondrial uncoupling protein 2 structure determined by NMR molecular fragment searching. Nature 476:109-113
13. Klingenberg M (1979) The ADP, ATP shuttle of the mitochondrion. Trends Biochem Sci 4:249-252
14. Klingenberg M (2008) The ADP and ATP transport in mitochondria and its carrier. Biochim Biophys Acta 1778:1978-2021
15. Palmieri F, Pierri CL (2010) Mitochondrial metabolite transport. Essays Biochem 47:37-52
16. Kunji ERS, Robinson AJ (2010) Coupling of proton and substrate translocation in the transport cycle of mitochondrial carriers. Curr Opin Struct Biol 20:440-447
17. Palmieri F, Pierri CL, De Grassi A, Nunes-Nesi A, Fernie AR (2011) Evolution, structure and function of mitochondrial carriers: a review with new insights. Plant J 66:161-181
18. Rhead B, Karolchik D, Kuhn RM, Hinrichs AS, Zweig AS et al (2010) The UCSC genome browser database: update 2010. Nucleic Acids Res 38:D613-D619
19. Waterhouse A, Procter J, Martin D, Clamp M, Barton G (2009) Jalview version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189-1191
20. Cappello AR, Curcio R, Miniero DV, Stipani I, Robinson AJ et al (2006) Functional and structural role of amino acid residues in the even-numbered transmembrane alpha-helices of the bovine mitochondrial oxoglutarate carrier. J Mol Biol 363:51-62 (Pubitemid 44414854)
21. Cappello AR, Miniero DV, Curcio R, Ludovico A, Daddabbo L et al (2007) Functional and structural role of amino acid residues in the odd-numbered transmembrane alpha-helices of the bovine mitochondrial oxoglutarate carrier. J Mol Biol 369:400-412 (Pubitemid 46678053)
22. Miniero DV, Cappello AR, Curcio R, Ludovico A, Daddabbo L et al (2011) Functional and structural role of amino acid residues in the matrix alpha-helices, termini and cytosolic loops of the bovine mitochondrial oxoglutarate carrier. Biochim Biophys Acta 1807:302-310
23. Sánchez R, Sali A (2000) Comparative protein structure modeling. Introduction and practical examples with modeller. Methods Mol Biol 143:97-129
24. Pierri CL, Parisi G, Porcelli V (2010) Computational approaches for protein function prediction: a combined strategy from multiple sequence alignment to molecular docking-based virtual screening. Biochim Biophys Acta 1804:1695-1712
25. Walters D, Kaplan R (2004) Homology-modeled structure of the yeast mitochondrial citrate transport protein. Biophys J 87:907-911 (Pubitemid 39095072)
26. Wohlrab H (2004) Novel inter- and intrasubunit contacts between transport-relevant residues of the homodimeric mitochondrial phosphate transport protein. Biochem Biophys Res Commun 320:685-688 (Pubitemid 38887198)
27. Morozzo Della Rocca B, Miniero D, Tasco G, Dolce V, Falconi M et al (2005) Substrate-induced conformational changes of the mitochondrial oxoglutarate carrier: a spectroscopic and molecular modelling study. Mol Membr Biol 22:443-452 (Pubitemid 41747106)
28. Tonazzi A, Giangregorio N, Indiveri C, Palmieri F (2005) Identification by site-directed mutagenesis and chemical modification of three vicinal cysteine residues in rat mitochondrial carnitine/acylcarnitine transporter. J Biol Chem 280:19607-19612 (Pubitemid 41379483)
29. Robinson AJ, Kunji ERS (2006) Mitochondrial carriers in the cytoplasmic state have a common substrate binding site. Proc Natl Acad Sci USA 103:2617-2622
30. Palmieri F, Pierri CL (2010) Structure and function of mitochondrial carriers - role of the transmembrane helix P and G residues in the gating and transport mechanism. FEBS Lett 584:1931-1939
31. Robinson AJ, Overy C, Kunji ERS (2008) The mechanism of transport by mitochondrial carriers based on analysis of symmetry. Proc Natl Acad Sci USA 105:17766-17771
32. Stipani V, Cappello A, Daddabbo L, Natuzzi D, Miniero D et al (2001) The mitochondrial oxoglutarate carrier: cysteine-scanning mutagenesis of transmembrane domain IV and sensitivity of Cys mutants to sulfhydryl reagents. Biochemistry 40:15805-15810 (Pubitemid 34015210)
33. Ma C, Remani S, Sun J, Kotaria R, Mayor J et al (2007) Identification of the substrate binding sites within the yeast mitochondrial citrate transport protein. J Biol Chem 282:17210-17220 (Pubitemid 47093228)
34. Müller V, Heidkämper D, Nelson D, Klingenberg M (1997) Mutagenesis of some positive and negative residues occurring in repeat triad residues in the ADP/ATP carrier from yeast. Biochemistry 36:16008-16018 (Pubitemid 28027406)
35. Wohlrab H, Annese V, Haefele A (2002) Single replacement constructs of all hydroxyl, basic, and acidic amino acids identify new function and structure-sensitive regions of the mitochondrial phosphate transport protein. Biochemistry 41:3254-3261 (Pubitemid 34184655)
36. Lawrence SA, Hackett JC, Moran RG (2011) Tetrahydrofolate recognition by the mitochondrial folate transporter. J Biol Chem 286:31480-31489
37. Giangregorio N, Tonazzi A, Console L, Indiveri C, Palmieri F (2010) Site-directed mutagenesis of charged amino acids of the human mitochondrial carnitine/acylcarnitine carrier: insight into the molecular mechanism of transport. Biochim Biophys Acta 1797:839-845
38. Monné M, Miniero DV, Daddabbo L, Robinson AJ, Kunji ER et al (2012) Substrate specificity of the two mitochondrial ornithine carriers can be swapped by single mutation in substrate binding site. J Biol Chem 287:7925-7934
39. Tonazzi A, Console L, Giangregorio N, Indiveri C, Palmieri F (2012) Identification by site-directed mutagenesis of a hydrophobic binding site of the mitochondrial carnitine/acylcarnitine carrier involved in the interaction with acyl groups. Biochim Biophys Acta 1817:697-704
40. Tonazzi A, Giangregorio N, Indiveri C, Palmieri F (2009) Site-directed mutagenesis of the His residues of the rat mitochondrial carnitine/acylcarnitine carrier: implications for the role of His-29 in the transport pathway. Biochim Biophys Acta 1787:1009-1015
41. Covian R, Balaban RS (2012) Cardiac mitochondrial matrix and respiratory complex protein phosphorylation. Am J Physiol Heart Circ Physiol 303:H940-H966
42. Nelson DR, Felix CM, Swanson JM (1998) Highly conserved charge-pair networks in the mitochondrial carrier family. J Mol Biol 277:285-308 (Pubitemid 28174969)
43. Wang Y, Tajkhorshid E (2008) Electrostatic funneling of substrate in mitochondrial inner membrane carriers. Proc Natl Acad Sci U S A 105:9598-9603 (Pubitemid 352031346)
44. Halfmann R, Alberti S, Krishnan R, Lyle N, O'Donnell CW et al (2011) Opposing effects of glutamine and asparagine govern prion formation by intrinsically disordered proteins. Mol Cell 43:72-84
45. Balabin RM (2009) Conformational equilibrium in glycine: focal-point analysis and ab initio limit. Chem Phys Lett 479:195-200
46. Hamelberg D, McCammon JA (2005) Fast peptidyl cis-trans isomerization within the flexible Gly-rich flaps of HIV-1 protease. J Am Chem Soc 127:13778-13779 (Pubitemid 41437013)
47. Dehez F, Pebay-Peyroula E, Chipot C (2008) Binding of ADP in the mitochondrial ADP/ATP carrier is driven by an electrostatic funnel. J Am Chem Soc 130:12725-12733
48. Marobbio CMT, Giannuzzi G, Paradies E, Pierri CL, Palmieri F (2008) Alpha-isopropylmalate, a leucine biosynthesis intermediate in yeast, is transported by the mitochondrial oxalacetate carrier. J Biol Chem 283:28445-28453
49. Edvardson S, Porcelli V, Jalas C, Soiferman D, Kellner Y et al (2013) Agenesis of corpus callosum and optic nerve hypoplasia due to mutations in SLC25A1 encoding the mitochondrial citrate transporter. J Med Genet 50:240-245
50. Falconi M, Chillemi G, Marino DD, Palmieri L, Desideri A (2006) Structural dynamics of the mitochondrial ADP/ATP carrier revealed by Molecular dynamics simulation studies. Proteins 691:681-691 (Pubitemid 44583217)
51. Hessa T, Kim H, Bihlmaier K, Lundin C, Boekel J et al (2005) Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433:377-381 (Pubitemid 40203311)
52. Sanchez Katheryn M, Kang G, Wu B, Kim Judy E (2011) Tryptophan-lipid interactions in membrane protein folding probed by ultraviolet resonance Raman and fluorescence spectroscopy. Biophys J 100:2121-2130
53. Adamian L, Liang J (2006) Prediction of transmembrane helix orientation in polytopic membrane proteins. BMC Struct Biol 6:13 (Pubitemid 44232099)
54. Mailloux RJ, Harper M-E (2011) Uncoupling proteins and the control of mitochondrial reactive oxygen species production. Free Radical Biol Med 51:1106-1115
55. Malorni W, Farrace MG, Matarrese P, Tinari A, Ciarlo L, Mousavi-Shafaei P, D'Eletto M, Di Giacomo G, Melino G, Palmieri L, Rodolfo C, Piacentini M (2009) The adenine nucleotide translocator 1 acts as a type 2 transglutaminase substrate: implications for mitochondrial-dependent apoptosis. Cell Death Differ 16:1480-1492
56. Park D, Chiu J, Perrone GG, Dilda PJ, Hogg PJ (2012) The tumour metabolism inhibitors GSAO and PENAO react with cysteines 57 and 257 of mitochondrial adenine nucleotide translocase. Cancer Cell Int 12:11
57. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188-1190 (Pubitemid 38811555)