Muscle choline kinase beta defect causes mitochondrial dysfunction and increased mitophagy

Human Molecular Genetics

Volumn 20, Issue 19, 2011, Pages 3841-3851

  Mitsuhashi, Satomi ^a   Hatakeyama, Hideyuki ^a   Karahashi, Minako ^b   Koumura, Tomoko ^b   Nonaka, Ikuya ^a   Hayashi, Yukiko K ^a   Noguchi, Satoru ^a   Sher, Roger B ^c   Nakagawa, Yasuhito ^b   Manfredi, Giovanni ^d   Goto, Yu ichi ^a   Cox, Gregory A ^c   Nishino, Ichizo ^a  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^b KITASATO UNIVERSITY   (Japan)

^c JACKSON LABORATORY   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINE KINASE; CHOLINE KINASE BETA; MALONALDEHYDE; MITOCHONDRIAL DNA; MOLECULAR MARKER; PARKIN; PHOSPHATIDYLCHOLINE; POLYUBIQUITIN; PROTEIN P62; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SUPEROXIDE; UBIQUINONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BIOCHEMISTRY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ELECTRON MICROSCOPY; ENZYME ACTIVITY; ENZYME SYNTHESIS; GENE DOSAGE; MOUSE; MUSCLE LEVEL; MUSCLE MITOCHONDRION; MUSCULAR DYSTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RESPIRATORY CHAIN; SKELETAL MUSCLE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CHOLINE KINASE; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MUSCLE, SKELETAL; MUSCULAR DYSTROPHIES;

MUS;

EID: 80052729571     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr305     Document Type: Article

References (41)

1. Mitsuhashi, S., Ohkuma, A., Talim, B., Karahashi, M., Koumura, T., Aoyama, C., Kurihara, M., Quinlivan, R., Sewry, C., Mitsuhashi, H. et al. (2011) A congenital muscular dystrophy with mitochondrial structural abnormalities caused by defective de novo phosphatidylcholine biosynthesis. Am. J. Hum. Genet., 88, 845-851.
2. Sher, R.B., Aoyama, C., Huebsch, K.A., Ji, S., Kerner, J., Yang, Y., Frankel, W.A., Hoppel, C.A., Wood, P.A., Vance, D.E. et al. (2006) A rostrocaudal muscular dystrophy caused by a defect in choline kinase beta, the first enzyme in phosphatidylcholine biosynthesis. J. Biol. Chem., 281, 4938-4948.
3. Saraste, M. (1999) Oxidative phosphorylation at the fin de siècle. Science, 283, 1488-1493.
4. Spierings, D., McStay, G., Saleh, M., Bender, C., Chipuk, J., Maurer, U. and Green, D.R. (2005) Connected to death: the (unexpurgated) mitochondrial pathway of apoptosis. Science, 310, 66-67.
5. Wakabayashi, T. (2002) Megamitochondria formation-physiology and pathology. J. Cell Mol. Med., 6, 497-538.
6. Benard, G., Bellance, N., James, D., Parrone, P., Fernandez, H. and Letellier, T. (2007) Mitochondrial bioenergetics and structural network organization. J. Cell Sci., 120, 838-848.
7. Yoon, Y.S., Yoon, D.S., Lim, I.K., Yoon, S.H., Chung, H.Y., Rojo, M., Malka, F., Jou, M.J., Martinou, J.C. and Yoon, G. (2006) Formation of elongated giant mitochondria in DFO-induced cellular senescence: involvement of enhanced fusion process through modulation of Fis1. J. Cell Physiol., 209, 468-480.
8. Karbowski, M., Kurono, C., Wozniak, M., Ostrowski, M., Teranishi, M., Nishizawa, Y., Usukura, J., Soji, T. and Wakabayashi, T. (1999) Free radical-induced megamitochondria formation and apoptosis. Free Radic. Biol. Med., 26, 396-409.
9. Chen, H., Detmer, S.A., Ewald, A.J., Griffin, E.E., Fraser, S.E. and Chan, D.C. (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol., 160, 189-200.
10. Chen, H., Chomyn, A. and Chan, D.C. (2005) Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem., 280, 26185-26192.
11. Wu, G., Sher, R.B., Cox, G.A. and Vance, D.E. (2009) Understanding the muscular dystrophy caused by deletion of choline kinase beta in mice. Biochim. Biophys. Acta, 1791, 347-356.
12. Daum, G. (1985) Lipids of mitochondria. Biochim. Biophys. Acta, 822, 1-42.
13. Hayashi, Y.K., Matsuda, C., Ogawa, M., Goto, K., Tominaga, K., Mitsuhashi, S., Park, Y.E., Nonaka, I., Hino-Fukuyo, N., Haginoya, K. et al. (2009) Human PTRF mutations cause secondary deficiency of caveolins resulting in muscular dystrophy with generalized lipodystrophy. J. Clin. Invest., 119, 2623-2633.
14. Bligh, E.G. and Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol., 37, 911-917.
15. Rouser, G., Fkeischer, S. and Yamamoto, A. (1970) Two dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids, 5, 494-496.
16. Mimaki, M., Hatakeyama, H., Ichiyama, T., Isumi, H., Furukawa, S., Akasaka, M., Kamei, A., Komaki, H., Nishino, I., Nonaka, I. et al. (2009) Different effects of novel mtDNA G3242A and G3244A base changes adjacent to a common A3243G mutation in patients with mitochondrial disorders. Mitochondrion, 9, 115-122.
17. Trounce, I.A., Kim, Y.L., Jun, A.S. and Wallace, D.C. (1996) Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and tranmitochondrial cell lines. Methods enzymol., 264, 484-509.
18. Vives-Bauza, C., Yang, L. and Manfredi, G. Methods in Cell Biology. Mitochondria, 2nd edn. Academic Press, London, UK, Vol. 80, Part 2, 7, 155-171.
19. Tang, P.H., Miles, M.V., Miles, L., Quinlan, J., Wong, B., Wenisch, A. and Bove, K. (2004) Measurement of reduced and oxidized coenzyme Q9 and coenzyme Q10 levels in mouse tissues by HPLC with coulometric detection. Clin. Chim. Acta, 341, 173-184.
20. Wittig, I., Karas, M. and Schagger, H. (2007) High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol. Cell Proteomics, 6, 1215-1225.
21. Armstrong, J.S. and Whiteman, M. Methods in Cell Biology. Mitochondria, 2nd edn. Academic Press, London, UK, Vol. 80, 18, 355-377.
22. Naini, A. and Shanske, S. Methods in Cell Biology. Mitochondria, 2nd edn. Academic Press, London, UK, Vol. 80, Part2, 22, 448-449.
23. Abramoff, M.D., Magelhaes, P.J. and Ram, S.J. (2004) Image processing with Image J. Biophotonics Int., 11, 36-42.
24. Zhang, M., Mileykovskaya, E. and Dowhan, W. (2002) Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J. Biol. Chem., 277, 43553-43556.
25. Geisler, S., Holmström, K.M., Skujat, D., Fiesel, F.C., Rothfuss, O.C., Kahle, P.J. and Springer, W. (2010) PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol., 12, 119-131.
26. Narendra, D., Tanaka, A., Suen, D.F. and Youle, R.J. (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol., 183, 795-803.
27. Lee, A.G. (2003) Lipid-protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta, 1612, 1-40.
28. Lange, C., Nett, J.H., Trumpower, B.L. and Hunte, C. (2001) Specific roles of protein-phospholipid interactions in the yeast cytochrome bc1 complex structure. EMBO J., 20, 6591-6600.
29. Hagopian, K., Weber, K.L., Hwee, D.T., Van Eenennaam, A.L., López-Lluch, G., Villalba, J.M., Burón, I., Navas, P., German, J.B., Watkins, S.M. et al. (2010) Complex I-associated hydrogen peroxide production is decreased and electron transport chain enzyme activities are altered in n-3 enriched fat-1 mice. PLoS ONE, 5, e12696.
30. Balaban, R.S., Nemoto, S. and Finkel, T. (2005) Mitochondria, oxidants, and aging. Cell, 120, 483-495.
31. St-Pierre, J., Buckingham, J.A., Roebuck, S.J. and Brand, M.D. (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem., 277, 44784-44790.
32. Osaki, Y., Nishino, I., Murakami, N., Matsubayashi, K., Tsuda, K., Yokoyama, Y.I., Morita, M., Onishi, S., Goto, Y.I. and Nonaka, I. (1998) Mitochondrial abnormalities in selenium-deficient myopathy. Muscle Nerve, 21, 637-639.
33. Hill, K.E., Motley, A.K., Li, X., May, J.M. and Burk, R.F. (2001) Combined selenium and vitamin E deficiency causes fatal myopathy in guinea pigs. J. Nutr., 131, 1798-1802.
34. Rederstorff, M., Krol, A. and Lescure, A. (2006) Understanding the importance of selenium and selenoproteins in muscle function. Cell Mol. Life Sci., 63, 52-59.
35. Martensson, J. and Meister, A. (1989) Mitochondrial damage in muscle occurs after marked depletion of glutathione and is prevented by giving glutathione monoester. Proc. Natl Acad. Sci. USA, 86, 471-475.
36. Choksi, K.B., Boylston, W.H., Rabek, J.P., Widger, W.R. and Papaconstantinou, J. (2004) Oxidatively damaged proteins of heart mitochondrial electron transport complexes. Biochim. Biophys. Acta, 1688, 95-101.
37. Kim, I., Rodriguez-Enriquez, S. and Lemasters, J. (2007) Selective degradation of mitochondria by mitophagy. Arch. Biochem. Biophys., 462, 245-253.
38. Tatsuta, T. and Langer, T. (2008) Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J., 27, 306-314.
39. Ding, W.X., Ni, H.M., Li, M., Liao, Y., Chen, X., Stolz, D.B., Dorn, G.W. 2nd. and Yin, X.M. (2010) Nix is critical to two distinct phases of mitophagy, reactive oxygen species-mediated autophagy induction and Parkin-ubiquitin-p62-mediated mitochondrial priming. J. Biol. Chem., 285, 27879-27890.
40. Moraes, C.T., Shanske, S., Tritschler, H.J., Aprille, J.R., Andreetta, F., Bonilla, E., Schon, E.A. and DiMauro, S. (1991) mtDNA depletion with variable tissue expression: a novel genetic abnormality in mitochondrial diseases. Am. J. Hum. Genet., 48, 492-501.
41. Kim, I. and Lemasters, J.J. (2011) Mitochondrial degradation by autophagy (mitophagy) in GFP-LC3 transgenic hepatocytes during nutrient deprivation. Am. J. Physiol. Cell Physiol., 300, C308-C317.