Defining functional classes of Barth syndrome mutation in humans

Human Molecular Genetics

Volumn 25, Issue 9, 2016, Pages 1754-1770

  Lu, Ya Wen ^a   Galbraith, Laura ^b   Herndon, Jenny D ^c   Lu, Ya Lin ^d   Pras Raves, Mia ^e   Vervaart, Martin ^e   Van Kampen, Antoine ^e   Luyf, Angela ^e   Koehler, Carla M ^c   McCaffery, J Michael ^f   Gottlieb, Eyal ^b   Vaz, Frederic M ^e   Claypool, Steven M ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d WASHINGTON UNIVERSITY   (United States)

^e ACADEMIC MEDICAL CENTER   (Netherlands)

^f JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MESSENGER RNA; MONOCLONAL ANTIBODY; POLYPEPTIDE; PROTEINASE; TAFAZZIN; UNCLASSIFIED DRUG; ISOPROTEIN; TAZ PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ALLELE; ANIMAL TISSUE; ARTICLE; BARTH SYNDROME; CELL CULTURE; CONTROLLED STUDY; EMBRYO; EXON; GENE; GENE EXPRESSION; HEART MITOCHONDRION; HEK293 CELL LINE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; LIVER MITOCHONDRION; LOSS OF FUNCTION MUTATION; MASS SPECTROMETRY; MEMBRANE; MITOCHONDRION; MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SKIN FIBROBLAST; TAZ GENE; ANIMAL; CLASSIFICATION; CYTOLOGY; FIBROBLAST; GENETICS; METABOLISM; MUTATION; PATHOLOGY; SKIN;

ANIMALS; BARTH SYNDROME; CELLS, CULTURED; FIBROBLASTS; HEK293 CELLS; HUMANS; MICE; MITOCHONDRIA, HEART; MITOCHONDRIA, LIVER; MUTATION; PROTEIN ISOFORMS; SKIN; TRANSCRIPTION FACTORS;

EID: 84991408358     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddw046     Document Type: Article

References (55)

1. Claypool, S.M. and Koehler, C.M. (2012) The complexity of cardiolipin in health and disease. Trends Biochem. Sci., 37, 32-41.
2. Zhang, J., Guan, Z., Murphy, A.N., Wiley, S.E., Perkins, G.A., Worby, C.A., Engel, J.L., Heacock, P., Nguyen, O.K., Wang, J.H. et al. (2011) Mitochondrial phosphatase PTPMT1 is essential for cardiolipin biosynthesis. Cell Metab., 13, 690-700.
3. Claypool, S.M. (2009) Cardiolipin, a critical determinant of mitochondrial carrier protein assembly and function. Biochim. Biophys. Acta, 1788, 2059-2068.
4. Gebert, N., Joshi, A.S., Kutik, S., Becker, T., McKenzie, M., Guan, X.L., Mooga, V.P., Stroud, D.A., Kulkarni, G., Wenk, M. R. et al. (2009) Mitochondrial cardiolipin involved in outermembrane protein biogenesis: implications for Barth syndrome. Curr. Biol., 19, 2133-2139.
5. Kutik, S., Rissler, M., Guan, X.L., Guiard, B., Shui, G., Gebert, N., Heacock, P.N., Rehling, P., Dowhan, W., Wenk, M.R. et al. (2008) The translocator maintenance protein Tam41 is required for mitochondrial cardiolipin biosynthesis. J. Cell Biol., 183, 1213-1221.
6. 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.
7. Acín-Pérez, R., Fernández-Silva, P., Peleato, M.L., Pérez-Martos, A. and Enriquez, J.A. (2008) Respiratory Active Mitochondrial Supercomplexes. Mol. Cell, 32, 529-539.
8. Pfeiffer, K., Gohil, V., Stuart, R.A., Hunte, C., Brandt, U., Greenberg, M.L. and Schagger, H. (2003) Cardiolipin stabilizes respiratory chain supercomplexes. J. Biol. Chem., 278, 52873-52880.
9. 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.
10. DeVay, R.M., Dominguez-Ramirez, L., Lackner, L.L., Hoppins, S., Stahlberg, H. and Nunnari, J. (2009) Coassembly of Mgm1 isoforms requires cardiolipin and mediates mitochondrial inner membrane fusion. J. Cell Biol., 186, 793-803.
11. Montessuit, S., Somasekharan, S.P., Terrones, O., Lucken-Ardjomande, S., Herzig, S., Schwarzenbacher, R., Manstein, D.J., Bossy-Wetzel, E., Basanez, G., Meda, P. et al. (2010) Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization. Cell, 142, 889-901.
12. Chu, C.T., Ji, J., Dagda, R.K., Jiang, J.F., Tyurina, Y.Y., Kapralov, A.A., Tyurin, V.A., Yanamala, N., Shrivastava, I.H., Mohammadyani, D. et al. (2013) Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells. Nat. Cell Biol., 15, 1197-1205.
13. Gonzalvez, F., Schug, Z.T., Houtkooper, R.H., MacKenzie, E.D., Brooks, D.G., Wanders, R.J., Petit, P.X., Vaz, F.M. and Gottlieb, E. (2008) Cardiolipin provides an essential activating platform for caspase-8 on mitochondria. J. Cell Biol., 183, 681-696.
14. Baile, M.G., Lu, Y.W. and Claypool, S.M. (2014) The topology and regulation of cardiolipin biosynthesis and remodeling in yeast. Chem. Phys. Lipids, 179, 25-31.
15. Schlame, M., Ren, M., Xu, Y., Greenberg, M.L. and Haller, I. (2005) Molecular symmetry in mitochondrial cardiolipins. Chem. Phys. Lipids, 138, 38-49.
16. Xu, Y., Malhotra, A., Ren, M. and Schlame, M. (2006) The enzymatic function of tafazzin. J. Biol. Chem., 281, 39217-39224.
17. Barth, P.G., Scholte, H.R., Berden, J.A., Van der Klei-Van Moorsel, J.M., Luyt-Houwen, I.E., Van 't Veer-Korthof, E.T., Van der Harten, J.J. and Sobotka-Plojhar, M.A. (1983) An X-linked mitochondrial disease affecting cardiac muscle, skeletal muscle and neutrophil leucocytes. J. Neurol. Sci., 62, 327-355.
18. Bione, S., D'Adamo, P., Maestrini, E., Gedeon, A.K., Bolhuis, P. A. and Toniolo, D. (1996) A novel X-linked gene, G4.5. is responsible for Barth syndrome. Nat. Genet., 12, 385-389.
19. Valianpour, F., Mitsakos, V., Schlemmer, D., Towbin, J.A., Taylor, J.M., Ekert, P.G., Thorburn, D.R., Munnich, A., Wanders, R. J., Barth, P.G. et al. (2005) Monolysocardiolipins accumulate in Barth syndrome but do not lead to enhanced apoptosis. J. Lipid Res., 46, 1182-1195.
20. Houtkooper, R.H., Turkenburg, M., Poll-The, B.T., Karall, D., Perez-Cerda, C., Morrone, A., Malvagia, S., Wanders, R.J., Kulik, W. and Vaz, F.M. (2009) The enigmatic role of tafazzin in cardiolipin metabolism. Biochim. Biophys. Acta, 1788, 2003-2014.
21. Dudek, J., Cheng, I.F., Balleininger, M., Vaz, F.M., Streckfuss-Bomeke, K., Hubscher, D., Vukotic, M., Wanders, R.J., Rehling, P. and Guan, K. (2013) Cardiolipin deficiency affects respiratory chain function and organization in an induced pluripotent stem cell model of Barth syndrome. Stem Cell Res., 11, 806-819.
22. Gonzalvez, F., D'Aurelio, M., Boutant, M., Moustapha, A., Puech, J.P., Landes, T., Arnaune-Pelloquin, L., Vial, G., Taleux, N., Slomianny, C. et al. (2013) Barth syndrome: cellular compensation of mitochondrial dysfunction and apoptosis inhibition due to changes in cardiolipin remodeling linked to tafazzin (TAZ) gene mutation. Biochim. Biophys. Acta, 1832, 1194-1206.
23. McKenzie, M., Lazarou, M., Thorburn, D.R. and Ryan, M.T. (2006) Mitochondrial respiratory chain supercomplexes are destabilized in Barth Syndrome patients. J. Mol. Biol., 361, 462-469.
24. Wang, G., McCain, M.L., Yang, L., He, A., Pasqualini, F.S., Agarwal, A., Yuan, H., Jiang, D., Zhang, D., Zangi, L. et al. (2014) Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-onchip technologies. Nat. Med., 20, 616-623.
25. Lu, Y.W. and Claypool, S.M. (2015) Disorders of phospholipid metabolism: an emerging class of mitochondrial disease due to defects in nuclear genes. Front Genet., 6, 3.
26. Davey, K.M., Parboosingh, J.S., McLeod, D.R., Chan, A., Casey, R., Ferreira, P., Snyder, F.F., Bridge, P.J. and Bernier, F.P. (2006) Mutation of DNAJC19, a human homologue of yeast inner mitochondrial membrane co-chaperones, causes DCMA syndrome, a novel autosomal recessive Barth syndrome-like condition. J. Med. Genet., 43, 385-393.
27. Mayr, J.A., Haack, T.B., Graf, E., Zimmermann, F.A., Wieland, T., Haberberger, B., Superti-Furga, A., Kirschner, J., Steinmann, B., Baumgartner, M.R. et al. (2012) Lack of the mitochondrial protein acylglycerol kinase causes Sengers syndrome. Am. J. Hum. Genet., 90, 314-320.
28. Richter-Dennerlein, R., Korwitz, A., Haag, M., Tatsuta, T., Dargazanli, S., Baker, M., Decker, T., Lamkemeyer, T., Rugarli, E.I. and Langer, T. (2014) DNAJC19, a mitochondrial cochaperone associated with cardiomyopathy, forms a complex with prohibitins to regulate cardiolipin remodeling. Cell Metab., 20, 158-171.
29. Wortmann, S.B., Vaz, F.M., Gardeitchik, T., Vissers, L.E., Renkema, G.H., Schuurs-Hoeijmakers, J.H., Kulik, W., Lammens, M., Christin, C., Kluijtmans, L.A. et al. (2012) Mutations in the phospholipid remodeling gene SERAC1 impair mitochondrial function and intracellular cholesterol trafficking and cause dystonia and deafness. Nat. Genet., 44, 797-802.
30. Claypool, S.M., McCaffery, J.M. and Koehler, C.M. (2006) Mitochondrial mislocalization and altered assembly of a cluster of Barth syndrome mutant tafazzins. J. Cell Biol., 174, 379-390.
31. Claypool, S.M., Whited, K., Srijumnong, S., Han, X. and Koehler, C.M. (2011) Barth syndrome mutations that cause tafazzin complex lability. J. Cell Biol., 192, 447-462.
32. Whited, K., Baile, M.G., Currier, P. and Claypool, S.M. (2013) Seven functional classes of Barth syndrome mutation. Hum. Mol. Genet., 22, 483-492.
33. Gonzalez, I.L. (2005) Barth syndrome: TAZ gene mutations, mRNAs, and evolution. Am. J. Med. Genet. A, 134, 409-414.
34. Vaz, F.M., Houtkooper, R.H., Valianpour, F., Barth, P.G. and Wanders, R.J. (2003) Only one splice variant of the human TAZ gene encodes a functional protein with a role in cardiolipin metabolism. J. Biol. Chem., 278, 43089-43094.
35. Diehl, J.A., Zindy, F. and Sherr, C.J. (1997) Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev., 11, 957-972.
36. Houtkooper, R.H., Rodenburg, R.J., Thiels, C., van Lenthe, H., Stet, F., Poll-The, B.T., Stone, J.E., Steward, C.G., Wanders, R. J., Smeitink, J. et al. (2009) Cardiolipin and monolysocardiolipin analysis in fibroblasts, lymphocytes, and tissues using high-performance liquid chromatography-mass spectrometry as a diagnostic test for Barth syndrome. Anal. Biochem., 387, 230-237.
37. Claypool, S.M., Boontheung, P., McCaffery, J.M., Loo, J.A. and Koehler, C.M. (2008) The cardiolipin transacylase, tafazzin, associates with two distinct respiratory components providing insight into Barth syndrome. Mol. Biol. Cell, 19, 5143-5155.
38. Brandner, K., Mick, D.U., Frazier, A.E., Taylor, R.D., Meisinger, C. and Rehling, P. (2005) Taz1, an outer mitochondrial membrane protein, affects stability and assembly of inner membrane protein complexes: implications for Barth Syndrome. Mol. Biol. Cell, 16, 5202-5214.
39. Hung, V., Zou, P., Rhee, H.W., Udeshi, N.D., Cracan, V., Svinkina, T., Carr, S.A., Mootha, V.K. and Ting, A.Y. (2014) Proteomic mapping of the human mitochondrial intermembrane space in live cells via ratiometric APEX tagging. Mol. Cell, 55, 332-341.
40. Lam, S.S., Martell, J.D., Kamer, K.J., Deerinck, T.J., Ellisman, M. H., Mootha, V.K. and Ting, A.Y. (2015) Directed evolution of APEX2 for electron microscopy and proximity labeling. Nat. Methods, 12, 51-54.
41. Baile, M.G., Whited, K. and Claypool, S.M. (2013) Deacylation on the matrix side of the mitochondrial inner membrane regulates cardiolipin remodeling. Mol. Biol. Cell, 24, 2008-2020.
42. Baile, M.G., Sathappa, M., Lu, Y.W., Pryce, E., Whited, K., McCaffery, J.M., Han, X., Alder, N.N. and Claypool, S.M. (2014) Unremodeled and remodeled cardiolipin are functionally indistinguishable in yeast. J. Biol. Chem., 289, 1768-1778.
43. Schlame, M., Acehan, D., Berno, B., Xu, Y., Valvo, S., Ren, M., Stokes, D.L. and Epand, R.M. (2012) The physical state of lipid substrates provides transacylation specificity for tafazzin. Nat. Chem. Biol., 8, 862-869.
44. Merkwirth, C., Dargazanli, S., Tatsuta, T., Geimer, S., Lower, B., Wunderlich, F.T., von Kleist-Retzow, J.C., Waisman, A., Westermann, B. and Langer, T. (2008) Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev., 22, 476-488.
45. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K. and Pease, L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene, 77, 51-59.
46. Claypool, S.M., Oktay, Y., Boontheung, P., Loo, J.A. and Koehler, C.M. (2008) Cardiolipin defines the interactome of the major ADP/ATP carrier protein of the mitochondrial inner membrane. J. Cell Biol., 182, 937-950.
47. Panneels, V., Schussler, U., Costagliola, S. and Sinning, I. (2003) Choline head groups stabilize the matrix loop regions of the ATP/ADP carrier ScAAC2. Biochem. Biophys. Res. Commun., 300, 65-74.
48. Claypool, S.M., Dickinson, B.L., Yoshida, M., Lencer, W.I. and Blumberg, R.S. (2002) Functional reconstitution of human FcRn in Madin-Darby canine kidney cells requires co-expressed human beta 2-microglobulin. J. Biol. Chem., 277, 28038-28050.
49. Frezza, C., Cipolat, S. and Scorrano, L. (2007) Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat. Protoc., 2, 287-295.
50. O'Shea, K.M., Khairallah, R.J., Sparagna, G.C., Xu, W., Hecker, P. A., Robillard-Frayne, I., Des Rosiers, C., Kristian, T., Murphy, R.C., Fiskum, G. et al. (2009) Dietary omega-3 fatty acids alter cardiac mitochondrial phospholipid composition and delay Ca2+-induced permeability transition. J. Mol. Cell. Cardiol., 47, 819-827.
51. Palmer, J.W., Tandler, B. and Hoppel, C.L. (1977) Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated fromrat cardiac muscle. J. Biol. Chem., 252, 8731-8739.
52. Untergasser, A., Nijveen, H., Rao, X., Bisseling, T., Geurts, R. and Leunissen, J.A. (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res., 35, W71-W74.
53. Chambers, M.C., Maclean, B., Burke, R., Amodei, D., Ruderman, D.L., Neumann, S., Gatto, L., Fischer, B., Pratt, B., Egertson, J. et al. (2012) A cross-platform toolkit for mass spectrometry and proteomics. Nat. Biotech., 30, 918-920.
54. Smith, C.A., Want, E.J., O'Maille, G., Abagyan, R. and Siuzdak, G. (2006) XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal. Chem., 78, 779-787.
55. Schneider, C.A., Rasband, W.S. and Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods, 9, 671-675.