Introducing a novel human mtDNA mutation into the Paracoccus denitrificans COX I gene explains functional deficits in a patient

Neurogenetics

Volumn 7, Issue 1, 2006, Pages 51-57

  Lucioli, Simona ^a   Hoffmeier, Klaus ^b   Carrozzo, Rosalba ^a   Tessa, Alessandra ^a   Ludwig, Bernd ^a   Santorelli, Filippo M ^a  

^a BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

Bacterial model; Cytochrome c oxidase; MELAS; mtDNA mutation; Paracoccus denitrificans

Indexed keywords

BACTERIAL ENZYME; CYCLOOXYGENASE 1; MITOCHONDRIAL DNA;

ADULT; ANAMNESIS; ARTICLE; BACTERIAL GENE; CARDIOMYOPATHY; CASE REPORT; CLINICAL FEATURE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENCEPHALOMYOPATHY; ENZYME ACTIVITY; FEMALE; FUNCTIONAL DISEASE; GENE MUTATION; HUMAN; LABORATORY TEST; MAMMAL; MITOCHONDRIAL CARDIOENCEPHALOMYOPATHY; NONHUMAN; PARACOCCUS DENITRIFICANS; PATHOGENICITY; PHENOTYPE; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; STRUCTURAL HOMOLOGY;

ADULT; ANIMALS; DNA MUTATIONAL ANALYSIS; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX IV; FEMALE; HUMANS; MUTATION; PARACOCCUS DENITRIFICANS; PHENOTYPE; PROTEIN CONFORMATION; PROTEIN SUBUNITS;

BACTERIA (MICROORGANISMS); MAMMALIA; PARACOCCUS DENITRIFICANS;

EID: 33644654904     PISSN: 13646745     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10048-005-0015-z     Document Type: Article

References (36)

1. Schultz BE, Chan SI (2001) Structures and proton-pumping strategies of mitochondrial respiratory enzymes. Annu Rev Biophys Biomol Struct 30:23-65
2. Richter OM, Ludwig B (2003) Cytochrome c oxidase - structure, function, and physiology of a redox-driven molecular machine. Rev Physiol Biochem Pharmacol 147:47-74
3. Brzezinski P, Larsson G (2003) Redox-driven proton-pumping by heme-copper oxidases. Biochim Biophys Acta 1605:1-13
4. Tiranti V, Hoertnagel K, Carrozzo R, Galimberti C, Munaro M, Granatiero M, Zelante L, Gasparini P, Marzella R, Rocchi M, Bayona-Bafaluy MP, Enriquez JA, Uziel G, Bertini E, Dionisi-Vici C, Franco B, Meitinger T, Zeviani M (1998) Mutations of SURF-1 in Leigh disease associated with cytochrome c oxidase deficiency. Am J Hum Genet 63:1609-1621
5. Valnot I, von Kleist-Retzow JC, Barrientos A, Gorbatyuk M, Taanman JW, Mehaye B, Rustin P, Tzagoloff A, Munnich A, Rotig A (2000) A mutation in the human heme A farnesyl-transferase gene (COX10) causes cytochrome c oxidase deficiency. Hum Mol Genet 9:1245-1249
6. Valnot I, Osmond S, Gigarel NS, Mehaye B, Amiel J, Cormier-Daire V, Munnich A, Bonnefont JP, Rustin P, Rotig A (2000) Mutations of the SCO1 gene in mitochondrial cytochrome c oxidase deficiency with neonatal-onset hepatic failure and encephalopathy. Am J Hum Genet 67:1104-1109
7. Papadopoulou LC, Sue CM, Davidson MM, Tanji K, Nishino I, Sadlock JE, Krishna S, Walker W, Selby J, Glerum DM, Coster RV, Lyon G, Scalais E, Lebel R, Kaplan P, Shanske S, De Vivo DC, Bonilla E, Hirano M, DiMauro S, Schon EA (1999) Fatal infantile cardioencephalomyopathy with COX deficiency and mutations in SCO2, a COX assembly gene. Nat Genet 23:333-337
8. Antonickà H, Mattman H, Carlson CG, Glerum D, Hoffbuhr KC, Leary SC, Kennaway NG, Shoubridge EA (2003) Mutations in COX15 produce a defect in the mitochondrial heme biosynthetic pathway, causing early-onset fatal hypertrophic cardiomyopathy. Am J Hum Genet 72:101-114
9. Comi GP, Bordoni A, Salani S, Franceschina L, Sciacco M, Prelle A, Fortunato F, Zeviani M, Napoli L, Bresolin N, Moggio M, Ausenda CD, Taanman JW, Scarlato G (1998) Cytochrome c oxidase subunit I microdeletion in a patient with motor neuron disease. Ann Neurol 43:110-116
10. Bruno C, Martinuzzi A, Tang Y, Andreu AL, Pallotti F, Bonilla E, Shanske S, Fu J, Sue CM, Angelini C, DiMauro S, Manfredi G (1999) A stop-codon mutation in the human mtDNA cytochrome c oxidase I gene disrupts the functional structure of complex IV. Am J Hum Genet 65:611-620
11. Karadimas CL, Greenstein P, Sue CM, Joseph JT, Tanji K, Haller RG, Taivassalo T, Davidson MM, Shanske S, Bonilla E, DiMauro S (2000) Recurrent myoglobinuria due to a nonsense mutation in the COX I gene of mitochondrial DNA. Neurology 55:644-649
12. Clark KM, Taylor RW, Johnson MA, Chinnery PF, Chrzanowska-Lightowlers ZM, Andrews RM, Nelson IP, Wood NW, Lamont PJ, Hanna MG, Lightowlers RN, Turnbull DM (1999) An mtDNA mutation in the initiation codon of the cytochrome C oxidase subunit II gene results in lower levels of the protein and a mitochondrial encephalomyopathy. Am J Hum Genet 64:1330-1339
13. Rahman S, Taanman JW, Cooper JM, Nelson I, Hargreaves I, Meunier B, Hanna MG, Garcia JJ, Capaldi RA, Lake BD, Leonard JV, Schapira AH (1999) A missense mutation of cytochrome oxidase subunit II causes defective assembly and myopathy. Am J Hum Genet 65:1030-1039
14. Campos Y, Garcia-Redondo A, Fernandez-Moreno MA, Martinez-Pardo M, Goda G, Rubio JC, Martin MA, del Hoyo P, Cabello A, Bornstein B, Garesse R, Arenas J (2001) Early-onset multisystem mitochondrial disorder caused by a nonsense mutation in the mitochondrial DNA cytochrome c oxidase II gene. Ann Neurol 50:409-413
15. Keightley JA, Hoffbuhr KC, Burton MD, Salas VM, Johnston WS, Penn AM, Buist NR, Kennaway NG (1996) A microdeletion in cytochrome c oxidase (COX) subunit III associated with COX deficiency and recurrent myoglobinuria. Nat Genet 12:410-416
16. Manfredi G, Schon EA, Moraes CT, Bonilla E, Berry GT, Sladky JT, DiMauro S (1995) A new mutation associated with MELAS is located in a mitochondrial DNA polypeptide coding gene. Neuromuscul Disord 5:391-398
17. Hanna MG, Nelson IP, Rahman S, Lane RJ, Land J, Heales S, Cooper MJ, Schapira AH, Morgan-Hughes JA, Wood NW (1998) Cytochrome c oxidase deficiency associated with the first stop-codon point mutation in human mtDNA. Am J Hum Genet 63:29-36
18. Tiranti V, Corona P, Greco M, Taanman JW, Carrara F, Lamantea E, Nijtmans L, Uziel G, Zeviani M (2000) A novel frameshift mutation of the mtDNA COIII gene leads to impaired assembly of cytochrome c oxidase in a patient affected by Leigh-like syndrome. Hum Mol Genet 9:2733-2742
19. Hoffbuhr KC, Davidson E, Filiano BA, Davidson M, Kennaway NG, King MP (2000) A pathogenic 15-base pair deletion in mitochondrial DNA-encoded cytochrome c oxidase subunit III results in the absence of functional cytochrome c oxidase. J Biol Chem 275:13994-14003
20. Iwata S, Ostermeier C, Ludwig B, Michel H (1995) Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376:660-669
21. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272:1136-1144
22. Sambrook J, Russel DW (2004) Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
23. Pfitzner U, Odenwald A, Ostermann T, Weingard L, Ludwig B, Richter OMH (1998) Cytochrome c oxidase (heme aa3) from Paracoccus denitrificans: analysis of mutations in putative proton channels of subunit I. J Bioenerg Biomembr 30:89-97
24. Pfitzner U, Hoffmeier K, Harrenga A, Kannt A, Michel H, Bamberg E, Richter OMH, Ludwig B (2000) Tracing the D-pathway in reconstituted site-directed mutants of cytochrome c oxidase from Paracoccus denitrificans. Biochemistry 39:6756-6762
25. Ludwig B (1986) Cytochrome c oxidase from Paracoccus denitrificans. Methods Enzymol 126:153-159
26. 3) from Paracoccus denitrificans. Proc Natl Acad Sci U S A 77:196-200
27. Markwell MA, Haas SM, Bieber LL, Tolbert NE (1978) A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87:206-210
28. Berry EA, Trumpower BL (1987) Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra. Anal Biochem 161:1-15
29. Zhen Y, Qian J, Follmann K, Hayward T, Nilsson T, Dahn M, Hilmi Y, Hamer AG, Hosler JP, Ferguson-Miller S (1998) Overexpression and purification of cytochrome c oxidase from Rhodobacter sphaeroides. Protein Expr Purif 13:326-336
30. 3 of Rhodobacter sphaeroides as a model for mitochondrial cytochrome c oxidase. Purification, kinetics, proton pumping, and spectral analysis. J Biol Chem 5(267):24264-24272
31. Varlamov DA, Kudin AP, Vielhaber S, Schröder R, Sassen R, Becker A, Kunz D, Haug K, Rebstock J, Heils A, Elger CE, Kunz WS (2002) Metabolic consequences of a novel missense mutation of the mtDNA CO I gene. Hum Mol Genet 11:1797-1805
32. Bratton M, Mills D, Castleden CK, Hosler J, Meunier B (2003) Disease-related mutations in cytochrome c oxidase studied in yeast and bacterial models. Eur J Biochem 270:1222-1230
33. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31:3381-3385
34. Lunardi J, Darrouzet E, Dupuis A, Issartel JP (2004) The nuoM arg368his mutation in NADH:ubiquinone oxidoreductase from Rhodobacter capsulatus: a model for the human nd4-11778 mtDNA mutation associated with Leber's hereditary optic neuropathy. Biochim Biophys Acta 1407:114-124
35. Kerscher S, Grgic L, Garofano A, Brandt U (2004) Application of the yeast Yarrowia lipolytica as a model to analyse human pathogenic mutations in mitochondrial complex I (NADH: ubiquinone oxidoreductase). Biochim Biophys Acta 1659:197-205
36. Carrozzo R, Murray J, Santorelli FM, Capaldi RA (2000) The T9176G mutation of human mtDNA gives a fully assembled but inactive ATP synthase when modeled in Escherichia coli. FEBS Lett 486:297-299