Complex V TMEM70 deficiency results in mitochondrial nucleoid disorganization

Mitochondrion

Volumn 11, Issue 1, 2011, Pages 191-199

  Cameron, Jessie M ^a   Levandovskiy, Valeriy ^a   MacKay, Nevena ^a   Ackerley, Cameron ^b   Chitayat, David ^b   Raiman, Julian ^b   Halliday, W H ^b   Schulze, Andreas ^b   Robinson, Brian H ^a,c,d  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

ATP synthase; Mitochondria; Nucleoids; TMEM70

Indexed keywords

3 METHYLGLUTACONIC ACID; MITOCHONDRIAL DNA; PROTEIN TMEM70; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG;

ADULT; AORTA ARCH ANOMALY; ARTICLE; CASE REPORT; COMPLEX V TMEM70 DEFICIENCY; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FEMALE; GENE MUTATION; HEART ARRHYTHMIA; HETEROZYGOSITY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERTROPHIC CARDIOMYOPATHY; MALE; MITOCHONDRIAL RESPIRATION; NEWBORN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; UMBILICAL HERNIA;

ACIDOSIS, LACTIC; ADULT; CARDIOMYOPATHIES; DNA, MITOCHONDRIAL; FEMALE; FIBROBLASTS; HETEROZYGOTE; HUMANS; INFANT, NEWBORN; MALE; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL DISEASES; MITOCHONDRIAL PROTEINS; MUTATION; SUBMITOCHONDRIAL PARTICLES; TOMOGRAPHY;

EID: 78650014067     PISSN: 15677249     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mito.2010.09.008     Document Type: Article

References (36)

1. Arnold I., Pfeiffer K., Neupert W., Stuart R.A., Schagger H. Yeast mitochondrial F1F0-ATP synthase exists as a dimer: identification of three dimer-specific subunits. The EMBO journal 1998, 17:7170-7178.
2. Bogenhagen D.F., Rousseau D., Burke S. The layered structure of human mitochondrial DNA nucleoids. The Journal of biological chemistry 2008, 283:3665-3675.
3. Breen G.A., Miller D.L., Holmans P.L., Welch G. Mitochondrial DNA of two independent oligomycin-resistant Chinese hamster ovary cell lines contains a single nucleotide change in the ATPase 6 gene. The Journal of biological chemistry 1986, 261:11680-11685.
4. Carrozzo R., Wittig I., Santorelli F.M., Bertini E., Hofmann S., Brandt U., Schagger H. Subcomplexes of human ATP synthase mark mitochondrial biosynthesis disorders. Annals of neurology 2006, 59:265-275.
5. Cizkova A., Stranecky V., Mayr J.A., Tesarova M., Havlickova V., Paul J., Ivanek R., Kuss A.W., Hansikova H., Kaplanova V., Vrbacky M., Hartmannova H., Noskova L., Honzik T., Drahota Z., Magner M., Hejzlarova K., Sperl W., Zeman J., Houstek J., Kmoch S. TMEM70 mutations cause isolated ATP synthase deficiency and neonatal mitochondrial encephalocardiomyopathy. Nature genetics 2008, 40:1288-1290.
6. De Meirleir L., Seneca S., Lissens W., De Clercq I., Eyskens F., Gerlo E., Smet J., Van Coster R. Respiratory chain complex V deficiency due to a mutation in the assembly gene ATP12. Journal of medical genetics 2004, 41:120-124.
7. Garcia J.J., Ogilvie I., Robinson B.H., Capaldi R.A. Structure, functioning, and assembly of the ATP synthase in cells from patients with the T8993G mitochondrial DNA mutation. Comparison with the enzyme in Rho(0) cells completely lacking mtdna. The Journal of biological chemistry 2000, 275:11075-11081.
8. Gilkerson R.W., Selker J.M., Capaldi R.A. The cristal membrane of mitochondria is the principal site of oxidative phosphorylation. FEBS letters 2003, 546:355-358.
9. Holme E., Greter J., Jacobson C.E., Larsson N.G., Lindstedt S., Nilsson K.O., Oldfors A., Tulinius M. Mitochondrial ATP-synthase deficiency in a child with 3-methylglutaconic aciduria. Pediatric research 1992, 32:731-735.
10. Houstek J., Klement P., Hermanska J., Houstkova H., Hansikova H., Van den Bogert C., Zeman J. Altered properties of mitochondrial ATP-synthase in patients with a T->G mutation in the ATPase 6 (subunit a) gene at position 8993 of mtDNA. Biochimica et biophysica acta 1995, 1271:349-357.
11. Houstek J., Klement P., Floryk D., Antonicka H., Hermanska J., Kalous M., Hansikova H., Hout'kova H., Chowdhury S.K., Rosipal T., Kmoch S., Stratilova L., Zeman J. A novel deficiency of mitochondrial ATPase of nuclear origin. Human molecular genetics 1999, 8:1967-1974.
12. John U.P., Nagley P. Amino acid substitutions in mitochondrial ATPase subunit 6 of Saccharomyces cerevisiae leading to oligomycin resistance. FEBS letters 1986, 207:79-83.
13. John G.B., Shang Y., Li L., Renken C., Mannella C.A., Selker J.M., Rangell L., Bennett M.J., Zha J. The mitochondrial inner membrane protein mitofilin controls cristae morphology. Molecular biology of the cell 2005, 16:1543-1554.
14. Lefebvre-Legendre L., Salin B., Schaeffer J., Brethes D., Dautant A., Ackerman S.H., di Rago J.P. Failure to assemble the alpha 3 beta 3 subcomplex of the ATP synthase leads to accumulation of the alpha and beta subunits within inclusion bodies and the loss of mitochondrial cristae in Saccharomyces cerevisiae. The Journal of biological chemistry 2005, 280:18386-18392.
15. Manfredi G., Gupta N., Vazquez-Memije M.E., Sadlock J.E., Spinazzola A., De Vivo D.C., Schon E.A. Oligomycin induces a decrease in the cellular content of a pathogenic mutation in the human mitochondrial ATPase 6 gene. The Journal of biological chemistry 1999, 274:9386-9391.
16. Margineantu D.H., Brown R.M., Brown G.K., Marcus A.H., Capaldi R.A. Heterogeneous distribution of pyruvate dehydrogenase in the matrix of mitochondria. Mitochondrion 2002, 1:327-338.
17. Mayr J.A., Paul J., Pecina P., Kurnik P., Forster H., Fotschl U., Sperl W., Houstek J. Reduced respiratory control with ADP and changed pattern of respiratory chain enzymes as a result of selective deficiency of the mitochondrial ATP synthase. Pediatric research 2004, 55:988-994.
18. Mun J.Y., Lee T.H., Kim J.H., Yoo B.H., Bahk Y.Y., Koo H.S., Han S.S. Caenorhabditis elegans mitofilin homologs control the morphology of mitochondrial cristae and influence reproduction and physiology. Journal of cellular physiology 2010, 224:748-756.
19. Nijtmans L.G., Henderson N.S., Attardi G., Holt I.J. Impaired ATP synthase assembly associated with a mutation in the human ATP synthase subunit 6 gene. The Journal of biological chemistry 2001, 276:6755-6762.
20. Ozawa T., Asai J. On the relationship between mitochondrial ATPase and the inner membrane. Journal of bioenergetics 1973, 4:507-519.
21. Pitkanen S., Raha S., Robinson B.H. Diagnosis of complex I deficiency in patients with lactic acidemia using skin fibroblast cultures. Biochem Mol Med 1996, 59:134-137.
22. Rak M., Tetaud E., Godard F., Sagot I., Salin B., Duvezin-Caubet S., Slonimski P.P., Rytka J., di Rago J.P. Yeast cells lacking the mitochondrial gene encoding the ATP synthase subunit 6 exhibit a selective loss of complex IV and unusual mitochondrial morphology. The Journal of biological chemistry 2007, 282:10853-10864.
23. Robinson B.H. Use of fibroblast and lymphoblast cultures for detection of respiratory chain defects. Methods in enzymology 1996, 264:454-464.
24. Robinson B.H., Taylor J., Francois B., Beaudet A.L., Peterson D.F. Lactic acidosis, neurological deterioration and compromised cellular pyruvate oxidation due to a defect in the reoxidation of cytoplasmically generated NADH. European journal of pediatrics 1983, 140:98-101.
25. Robinson B.H., Glerum D.M., Chow W., Petrova-Benedict R., Lightowlers R., Capaldi R. The use of skin fibroblast cultures in the detection of respiratory chain defects in patients with lacticacidemia. Pediatr Res 1990, 28:549-555.
26. Spelbrink J.N. Functional organization of mammalian mitochondrial DNA in nucleoids: history, recent developments, and future challenges. IUBMB life 2010, 62:19-32.
27. Sperl W., Jesina P., Zeman J., Mayr J.A., Demeirleir L., VanCoster R., Pickova A., Hansikova H., Houst'kova H., Krejcik Z., Koch J., Smet J., Muss W., Holme E., Houstek J. Deficiency of mitochondrial ATP synthase of nuclear genetic origin. Neuromuscul Disord 2006, 16:821-829.
28. Strauss M., Hofhaus G., Schroder R.R., Kuhlbrandt W. Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. The EMBO journal 2008, 27:1154-1160.
29. Tatuch Y., Christodoulou J., Feigenbaum A., Clarke J.T., Wherret J., Smith C., Rudd N., Petrova-Benedict R., Robinson B.H. Heteroplasmic mtDNA mutation (T-G) at 8993 can cause Leigh disease when the percentage of abnormal mtDNA is high. American journal of human genetics 1992, 50:852-858.
30. Tatuch Y., Pagon R.A., Vlcek B., Roberts R., Korson M., Robinson B.H. The 8993 mtDNA mutation: heteroplasmy and clinical presentation in three families. Eur J Hum Genet 1994, 2:35-43.
31. Wang Y., Bogenhagen D.F. Human mitochondrial DNA nucleoids are linked to protein folding machinery and metabolic enzymes at the mitochondrial inner membrane. The Journal of biological chemistry 2006, 281:25791-25802.
32. Wittig I., Karas M., Schagger H. High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol Cell Proteomics 2007, 6:1215-1225.
33. Xu F., Ackerley C., Maj M.C., Addis J.B., Levandovskiy V., Lee J., Mackay N., Cameron J.M., Robinson B.H. Disruption of a mitochondrial RNA-binding protein gene results in decreased cytochrome b expression and a marked reduction in ubiquinol-cytochrome c reductase activity in mouse heart mitochondria. The Biochemical journal 2008, 416:15-26.
34. Yotsuyanagi Y. Study of yeast mitochondria. II. Mitochondria of respiration-deficient mutants. Journal of ultrastructure research 1962, 7:141-158.
35. Yotsuyanagi Y. Fibrous component of yeast mitochondria. Journal of ultrastructure and molecular structure research 1988, 98:254-266.
36. Zeng X., Neupert W., Tzagoloff A. The metalloprotease encoded by ATP23 has a dual function in processing and assembly of subunit 6 of mitochondrial ATPase. Molecular biology of the cell 2007, 18:617-626.