Restoration of complex V deficiency caused by a novel deletion in the human TMEM70 gene normalizes mitochondrial morphology

Mitochondrion

Volumn 11, Issue 6, 2011, Pages 954-963

  Jonckheere, An I ^a   Huigsloot, Merei ^a   Lammens, Martin ^a   Jansen, Jitske ^a   van den Heuvel, Lambert P ^a   Spiekerkoetter, Ute ^b   von Kleist Retzow, Jürgen Christoph ^c   Forkink, Marleen ^d   Koopman, Werner J H ^d   Szklarczyk, Radek ^d   Huynen, Martijn A ^d   Fransen, Jack A ^d   Smeitink, Jan A M ^a   Rodenburg, Richard J T ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^c UNIVERSITY OF COLOGNE   (Germany)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Complex V; Mitochondrial morphology; TMEM70

Indexed keywords

PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ARTICLE; CASE REPORT; CELL STRUCTURE; CHILD; COMPLEX V DEFICIENCY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEFICIENCY; FIBROBLAST; GENE; GENE DELETION; GENETIC ANALYSIS; HOMOZYGOSITY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERAMMONEMIA; HYPERORNITHINEMIA HYPERAMMONEMIA HOMOCITRULLINURIA SYNDROME; HYPERTROPHIC CARDIOMYOPATHY; IMMUNOGOLD LABELING; LACTIC ACIDOSIS; MALE; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOLECULAR CLONING; MUSCLE BIOPSY; PRESCHOOL CHILD; PRIORITY JOURNAL; SKIN BIOPSY; TMEM70 GENE;

ADENOSINE TRIPHOSPHATASES; CARRIER PROTEINS; CELLS, CULTURED; FIBROBLASTS; GENETIC COMPLEMENTATION TEST; HUMANS; INFANT, NEWBORN; MALE; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; SEQUENCE DELETION;

EUKARYOTA;

EID: 82755160668     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2011.08.012     Document Type: Article

References (55)

1. Alexeyenko A., Sonnhammer E.L. Global networks of functional coupling in eukaryotes from comprehensive data integration. Genome Res. 2009, 19:1107-1116.
2. Allen R.D. Membrane tubulation and proton pumps. Protoplasma 1995, 189:1-8.
3. Arselin G., Vaillier J., Salin B., Schaeffer J., Giraud M.F., Dautant A., Brethes D., Velours J. The modulation in subunits e and g amounts of yeast ATP synthase modifies mitochondrial cristae morphology. J. Biol. Chem. 2004, 279:40392-40399.
4. Bronnikov G., Houstek J., Nedergaard J. Beta-adrenergic, cAMP-mediated stimulation of proliferation of brown fat cells in primary culture. Mediation via beta 1 but not via beta 3 adrenoceptors. J. Biol. Chem. 1992, 267:2006-2013.
5. Calvo S., Jain M., Xie X., Sheth S.A., Chang B., Goldberger O.A., Spinazzola A., Zeviani M., Carr S.A., Mootha V.K. Systematic identification of human mitochondrial disease genes through integrative genomics. Nat. Genet. 2006, 38:576-582.
6. Cameron J.M., Levandovskiy V., Mackay N., Ackerley C., Chitayat D., Raiman J., Halliday W.H., Schulze A., Robinson B.H. Complex V TMEM70 deficiency results in mitochondrial nucleoid disorganization. Mitochondrion 2011, 11:191-199.
7. Campanella M., Casswell E., Chong S., Farah Z., Wieckowski M.R., Abramov A.Y., Tinker A., Duchen M.R. Regulation of mitochondrial structure and function by the F1Fo-ATPase inhibitor protein, IF1. Cell Metab. 2008, 8:13-25.
8. 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. Nat. Genet. 2008, 40:1288-1290.
9. Collinson I.R., Skehel J.M., Fearnley I.M., Runswick M.J., Walker J.E. The F1F0-ATPase complex from bovine heart mitochondria: the molar ratio of the subunits in the stalk region linking the F1 and F0 domains. Biochemistry 1996, 35:12640-12646.
10. Cortes-Hernandez P., Vazquez-Memije M.E., Garcia J.J. ATP6 homoplasmic mutations inhibit and destabilize the human F1F0-ATP synthase without preventing enzyme assembly and oligomerization. J. Biol. Chem. 2007, 282:1051-1058.
11. Cuppen E., Wijers M., Schepens J., Fransen J., Wieringa B., Hendriks W. A FERM domain governs apical confinement of PTP-BL in epithelial cells. J. Cell Sci. 1999, 112(Pt 19):3299-3308.
12. 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. J. Med. Genet. 2004, 41:120-124.
13. Dieteren C.E., Willems P.H., Vogel R.O., Swarts H.G., Fransen J., Roepman R., Crienen G., Smeitink J.A., Nijtmans L.G., Koopman W.J. Subunits of mitochondrial complex I exist as part of matrix- and membrane-associated subcomplexes in living cells. J. Biol. Chem. 2008, 283:34753-34761.
14. Dinopoulos A., Smeitink J., ter Laak H. Unusual features of mitochondrial degeneration in skeletal muscle of patients with nuclear complex I mutation. Acta Neuropathol. 2005, 110:199-202.
15. Fransen J.A., Ginsel L.A., Hauri H.P., Sterchi E., Blok J. Immuno-electronmicroscopical localization of a microvillus membrane disaccharidase in the human small-intestinal epithelium with monoclonal antibodies. Eur. J. Cell Biol. 1985, 38:6-15.
16. Frey T.G., Renken C.W., Perkins G.A. Insight into mitochondrial structure and function from electron tomography. Biochim. Biophys. Acta 2002, 1555:196-203.
17. Gavin P.D., Prescott M., Luff S.E., Devenish R.J. Cross-linking ATP synthase complexes in vivo eliminates mitochondrial cristae. J. Cell Sci. 2004, 117:2333-2343.
18. Guillery O., Malka F., Frachon P., Milea D., Rojo M., Lombes A. Modulation of mitochondrial morphology by bioenergetics defects in primary human fibroblasts. Neuromuscul. Disord. 2008, 18:319-330.
19. Hejzlarova K., Tesarova M., Vrbacka-Cizkova A., Vrbacky M., Hartmannova H., Kaplanova V., Noskova L., Kratochvilova H., Buzkova J., Havlickova V., Zeman J., Kmoch S., Houstek J. Expression and processing of the TMEM70 protein. Biochim. Biophys. Acta 2011, 1807:144-149.
20. Houstek J., Tvrdik P., Pavelka S., Baudysova M. Low content of mitochondrial ATPase in brown adipose tissue is the result of post-transcriptional regulation. FEBS Lett. 1991, 294:191-194.
21. Houstek J., Andersson U., Tvrdik P., Nedergaard J., Cannon B. The expression of subunit c correlates with and thus may limit the biosynthesis of the mitochondrial F0F1-ATPase in brown adipose tissue. J. Biol. Chem. 1995, 270:7689-7694.
22. Houstek J., Kmoch S., Zeman J. TMEM70 protein - a novel ancillary factor of mammalian ATP synthase. Biochim. Biophys. Acta 2009, 1787:529-532.
23. Janssen A.J., Smeitink J.A., van den Heuvel L.P. Some practical aspects of providing a diagnostic service for respiratory chain defects. Ann. Clin. Biochem. 2003, 40:3-8.
24. Janssen A.J., Trijbels F.J., Sengers R.C., Wintjes L.T., Ruitenbeek W., Smeitink J.A., Morava E., van Engelen B.G., van den Heuvel L.P., Rodenburg R.J. Measurement of the energy-generating capacity of human muscle mitochondria: diagnostic procedure and application to human pathology. Clin. Chem. 2006, 52:860-871.
25. Jonckheere A.I., Hogeveen M., Nijtmans L.G., van den Brand M.A., Janssen A.J., Diepstra J.H., van den Brandt F.C., van den Heuvel L.P., Hol F.A., Hofste T.G., Kapusta L., Dillmann U., Shamdeen M.G., Smeitink J.A., Rodenburg R.J. A novel mitochondrial ATP8 gene mutation in a patient with apical hypertrophic cardiomyopathy and neuropathy. J. Med. Genet. 2008, 45:129-133.
26. Klammer M., Messina D.N., Schmitt T., Sonnhammer E.L. MetaTM - a consensus method for transmembrane protein topology prediction. BMC Bioinformatics 2009, 10:314.
27. Koopman W.J., Distelmaier F., Esseling J.J., Smeitink J.A., Willems P.H. Computer-assisted live cell analysis of mitochondrial membrane potential, morphology and calcium handling. Methods 2008, 46:304-311.
28. Kramarova T.V., Shabalina I.G., Andersson U., Westerberg R., Carlberg I., Houstek J., Nedergaard J., Cannon B. Mitochondrial ATP synthase levels in brown adipose tissue are governed by the c-Fo subunit P1 isoform. FASEB J. 2008, 22:55-63.
29. Kucharczyk R., Salin B., di Rago J.P. Introducing the human Leigh syndrome mutation T9176G into Saccharomyces cerevisiae mitochondrial DNA leads to severe defects in the incorporation of Atp6p into the ATP synthase and in the mitochondrial morphology. Hum. Mol. Genet. 2009, 18:2889-2898.
30. 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. J. Biol. Chem. 2005, 280:18386-18392.
31. Li J., Cai T., Wu P., Cui Z., Chen X., Hou J., Xie Z., Xue P., Shi L., Liu P., Yates J.R., Yang F. Proteomic analysis of mitochondria from Caenorhabditis elegans. Proteomics 2009, 9:4539-4553.
32. Loncar D. Convertible adipose tissue in mice. Cell Tissue Res. 1991, 266:149-161.
33. Matsuyama A., Arai R., Yashiroda Y., Shirai A., Kamata A., Sekido S., Kobayashi Y., Hashimoto A., Hamamoto M., Hiraoka Y., Horinouchi S., Yoshida M. ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat. Biotechnol. 2006, 24:841-847.
34. Mayr J.A., Havlickova V., Zimmermann F., Magler I., Kaplanova V., Jesina P., Pecinova A., Nuskova H., Koch J., Sperl W., Houstek J. Mitochondrial ATP synthase deficiency due to a mutation in the ATP5E gene for the F1 epsilon subunit. Hum. Mol. Genet. 2010, 19:3430-3439.
35. Miller S.A., Dykes D.D., Polesky H.F. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988, 16:1215.
36. Miller A.D., Miller D.G., Garcia J.V., Lynch C.M. Use of retroviral vectors for gene transfer and expression. Methods Enzymol. 1993, 217:581-599.
37. Morava E., Rodenburg R.J., Hol F., de Vries M., Janssen A., van den Heuvel L., Nijtmans L., Smeitink J. Clinical and biochemical characteristics in patients with a high mutant load of the mitochondrial T8993G/C mutations. Am. J. Med. Genet. A 2006, 140:863-868.
38. Murray J.I., Whitfield M.L., Trinklein N.D., Myers R.M., Brown P.O., Botstein D. Diverse and specific gene expression responses to stresses in cultured human cells. Mol. Biol. Cell 2004, 15:2361-2374.
39. Nijtmans L.G., Henderson N.S., Holt I.J. Blue Native electrophoresis to study mitochondrial and other protein complexes. Methods 2002, 26:327-334.
40. Paumard P., Vaillier J., Coulary B., Schaeffer J., Soubannier V., Mueller D.M., Brethes D., di Rago J.P., Velours J. The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 2002, 21:221-230.
41. Rabl R., Soubannier V., Scholz R., Vogel F., Mendl N., Vasiljev-Neumeyer A., Korner C., Jagasia R., Keil T., Baumeister W., Cyrklaff M., Neupert W., Reichert A.S. Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g. J. Cell Biol. 2009, 185:1047-1063.
42. Rodriguez-Cuenca S., Pujol E., Justo R., Frontera M., Oliver J., Gianotti M., Roca P. Sex-dependent thermogenesis, differences in mitochondrial morphology and function, and adrenergic response in brown adipose tissue. J. Biol. Chem. 2002, 277:42958-42963.
43. Sauvanet C., Duvezin-Caubet S., di Rago J.P., Rojo M. Energetic requirements and bioenergetic modulation of mitochondrial morphology and dynamics. Semin. Cell Dev. Biol. 2010, 21:558-565.
44. Shchelochkov O.A., Li F.Y., Wang J., Zhan H., Towbin J.A., Jefferies J.L., Wong L.J., Scaglia F. Milder clinical course of Type IV 3-methylglutaconic aciduria due to a novel mutation in TMEM70. Mol. Genet. Metab. 2010, 101:282-285.
45. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., Fujimoto E.K., Goeke N.M., Olson B.J., Klenk D.C. Measurement of protein using bicinchoninic acid. Anal. Biochem. 1985, 150:76-85.
46. Spiegel R., Khayat M., Shalev S.A., Horovitz Y., Mandel H., Hershkovitz E., Barghuti F., Shaag A., Saada A., Korman S.H., Elpeleg O., Yatsiv I. TMEM70 mutations are a common cause of nuclear encoded ATP synthase assembly defect: further delineation of a new syndrome. J. Med. Genet. 2011, 48:177-182.
47. Srere P.A. Citrate Synthase, Methods Enzymology 1969, 3-11.
48. Stadhouders A.M., Sengers R.C. Morphological observations in skeletal muscle from patients with a mitochondrial myopathy. J. Inherit. Metab. Dis. 1987, 10(Suppl 1):62-80.
49. Strauss M., Hofhaus G., Schroder R.R., Kuhlbrandt W. Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO J. 2008, 27:1154-1160.
50. Su A.I., Wiltshire T., Batalov S., Lapp H., Ching K.A., Block D., Zhang J., Soden R., Hayakawa M., Kreiman G., Cooke M.P., Walker J.R., Hogenesch J.B. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:6062-6067.
51. Thomas D., Bron P., Weimann T., Dautant A., Giraud M.F., Paumard P., Salin B., Cavalier A., Velours J., Brethes D. Supramolecular organization of the yeast F1Fo-ATP synthase. Biol. Cell 2008, 100:591-601.
52. Wagner K., Perschil I., Fichter C.D., van der Laan M. Stepwise assembly of dimeric F(1)F(o)-ATP synthase in mitochondria involves the small F(o)-subunits k and i. Mol. Biol. Cell 2010, 21:1494-1504.
53. Wittig I., Meyer B., Heide H., Steger M., Bleier L., Wumaier Z., Karas M., Schagger H. Assembly and oligomerization of human ATP synthase lacking mitochondrial subunits a and A6L. Biochim. Biophys. Acta 2010, 1797:1004-1011.
54. Wortmann S.B., Rodenburg R.J., Jonckheere A., de Vries M.C., Huizing M., Heldt K., van den Heuvel L.P., Wendel U., Kluijtmans L.A., Engelke U.F., Wevers R.A., Smeitink J.A., Morava E. Biochemical and genetic analysis of 3-methylglutaconic aciduria type IV: a diagnostic strategy. Brain 2009, 132:136-146.
55. Zick M., Rabl R., Reichert A.S. Cristae formation-linking ultrastructure and function of mitochondria. Biochim. Biophys. Acta 2009, 1793:5-19.