Mitochondrial phosphatase PTPMT1 is essential for cardiolipin biosynthesis

Cell Metabolism

Volumn 13, Issue 6, 2011, Pages 690-700

  Zhang, Ji ^a   Guan, Ziqiang ^d   Murphy, Anne N ^a   Wiley, Sandra E ^a   Perkins, Guy A ^a   Worby, Carolyn A ^a   Engel, James L ^a   Heacock, Philip ^e   Nguyen, Oanh Kim ^a   Wang, Jonathan H ^a   Raetz, Christian R H ^d   Dowhan, William ^e   Dixon, Jack E ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOLIPIN; GLYCEROPHOSPHATE; PHOSPHATIDYLGLYCEROL; PHOSPHATIDYLGLYCEROL PHOSPHATE; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE MT1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CATALYSIS; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; FIBROBLAST; LIPID ANALYSIS; LIPID STORAGE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NONHUMAN; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CARDIOLIPINS; CELL LINE; CELL RESPIRATION; CLONING, MOLECULAR; EMBRYO, MAMMALIAN; GENETIC ENGINEERING; GENOTYPE; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHOSPHATIDYLGLYCEROLS; PHOSPHORIC MONOESTER HYDROLASES; PTEN PHOSPHOHYDROLASE; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

MAMMALIA; MUS;

EID: 79958034094     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2011.04.007     Document Type: Article

References (52)

1. Alonso, A., Sasin, J., Bottini, N., Friedberg, I., Friedberg, I., Osterman, A., Godzik, A., Hunter, T., Dixon, J., and Mustelin, T. (2004). Protein tyrosine phosphatases in the human genome. Cell 117, 699-711. (Pubitemid 38748887)
2. Bligh, E.G., and Dyer, W.J. (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917.
3. Brachmann, C.B., Davies, A., Cost, G.J., Caputo, E., Li, J., Hieter, P., and Boeke, J.D. (1998). Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132. (Pubitemid 28062863)
4. Cerritelli, S.M., Frolova, E.G., Feng, C., Grinberg, A., Love, P.E., and Crouch, R.J. (2003). Failure to produce mitochondrial DNA results in embryonic lethality in Rnaseh1 null mice. Mol. Cell 11, 807-815. (Pubitemid 36385132)
5. Chicco, A.J., and Sparagna, G.C. (2007). Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am. J. Physiol. Cell Physiol. 292, C33-C44.
6. Daum, G. (1985). Lipids of mitochondria. Biochim. Biophys. Acta 822, 1-42.
7. Denu, J.M., Zhou, G., Wu, L., Zhao, R., Yuvaniyama, J., Saper, M.A., and Dixon, J.E. (1995). The purification and characterization of a human dual-specific protein tyrosine phosphatase. J. Biol. Chem. 270, 3796-3803.
8. Dowhan, W. (1992). Phosphatidylglycerophosphate synthase from Escherichia coli. Methods Enzymol. 209, 313-321.
9. Hance, N., Ekstrand, M.I., and Trifunovic, A. (2005). Mitochondrial DNA polymerase gamma is essential for mammalian embryogenesis. Hum. Mol. Genet. 14, 1775-1783.
10. Hatch, G.M. (1998). Cardiolipin: biosynthesis, remodeling and trafficking in the heart and mammalian cells (Review). Int. J. Mol. Med. 1, 33-41.
11. Houtkooper, R.H., and Vaz, F.M. (2008). Cardiolipin, the heart of mitochondrial metabolism. Cell. Mol. Life Sci. 65, 2493-2506.
12. Icho, T., and Raetz, C.R. (1983). Multiple genes for membrane-bound phosphatases in Escherichia coli and their action on phospholipid precursors. J. Bacteriol. 153, 722-730. (Pubitemid 13163552)
13. Janitor, M., and Subík, J. (1993). Molecular cloning of the PEL1 gene of Saccharomyces cerevisiae that is essential for the viability of petite mutants. Curr. Genet. 24, 307-312.
14. Kerk, D., Templeton, G., and Moorhead, G.B. (2008). Evolutionary radiation pattern of novel protein phosphatases revealed by analysis of protein data from the completely sequenced genomes of humans, green algae, and higher plants. Plant Physiol. 146, 351-367. (Pubitemid 351230768)
15. Kiyasu, J.Y., Pieringer, R.A., Paulus, H., and Kennedy, E.P. (1963). The biosynthesis of phosphatidylglycerol. J. Biol. Chem. 238, 2293-2298.
16. Kletzien, R.F., and Perdue, J.F. (1975). Induction of sugar transport in chick embryo fibroblasts by hexose starvation. Evidence for transcriptional regulation of transport. J. Biol. Chem. 250, 593-600.
17. Klingenberg, M. (1970). Localization of the glycerol-phosphate dehydrogenase in the outer phase of the mitochondrial inner membrane. Eur. J. Biochem. 13, 247-252.
18. Kumaran, D., Bonanno, J.B., Burley, S.K., and Swaminathan, S. (2006). Crystal structure of phosphatidylglycerophosphatase (PGPase), a putative membrane-bound lipid phosphatase, reveals a novel binuclear metal binding site and two "proton wires". Proteins 64, 851-862.
19. Larsson, N.G., Wang, J., Wilhelmsson, H., Oldfors, A., Rustin, P., Lewandoski, M., Barsh, G.S., and Clayton, D.A. (1998). Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet. 18, 231-236.
20. Lu, Y.H., Guan, Z., Zhao, J., and Raetz, C.R. (2011). Three phosphatidylglycerol-phosphate phosphatases in the inner membrane of Escherichia coli. J. Biol. Chem. 286, 5506-5518.
21. MacDonald, P.M., and McMurray, W.C. (1980). Partial purification and properties of mammalian phosphatidylglycerophosphatase. Biochim. Biophys. Acta 620, 80-89.
22. Maehama, T., and Dixon, J.E. (1998). The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 273, 13375-13378.
23. Manning, G., Whyte, D.B., Martinez, R., Hunter, T., and Sudarsanam, S. (2002). The protein kinase complement of the human genome. Science 298, 1912-1934. (Pubitemid 35425239)
24. McKenzie, M., Lazarou, M., Thorburn, D.R., and Ryan, M.T. (2007). Analysis of mitochondrial subunit assembly into respiratory chain complexes using Blue Native polyacrylamide gel electrophoresis. Anal. Biochem. 364, 128-137.
25. Newmeyer, D.D., and Ferguson-Miller, S. (2003). Mitochondria: releasing power for life and unleashing the machineries of death. Cell 112, 481-490. (Pubitemid 36263081)
26. Osman, C., Haag, M., Wieland, F.T., Brügger, B., and Langer, T. (2010). A mitochondrial phosphatase required for cardiolipin biosynthesis: the PGP phosphatase Gep4. EMBO J. 29, 1976-1987.
27. Pagliarini, D.J., Worby, C.A., and Dixon, J.E. (2004). A PTEN-like phosphatase with a novel substrate specificity. J. Biol. Chem. 279, 38590-38596.
28. Pagliarini, D.J., Wiley, S.E., Kimple, M.E., Dixon, J.R., Kelly, P., Worby, C.A., Casey, P.J., and Dixon, J.E. (2005). Involvement of a mitochondrial phosphatase in the regulation of ATP production and insulin secretion in pancreatic beta cells. Mol. Cell 19, 197-207.
29. Pallotti, F., and Lenaz, G. (2001). Isolation and subfractionation of mitochondria from animal cells and tissue culture lines. Methods Cell Biol. 65, 1-35.
30. Parce, J.W., Owicki, J.C., Kercso, K.M., Sigal, G.B., Wada, H.G., Muir, V.C., Bousse, L.J., Ross, K.L., Sikic, B.I., and McConnell, H.M. (1989). Detection of cell-affecting agents with a silicon biosensor. Science 246, 243-247. (Pubitemid 19264637)
31. Rardin, M.J., Wiley, S.E., Murphy, A.N., Pagliarini, D.J., and Dixon, J.E. (2008). Dual specificity phosphatases 18 and 21 target to opposing sides of the mitochondrial inner membrane. J. Biol. Chem. 283, 15440-15450.
32. Rock, C.O. (2008). Fatty acid and phospholipid metabolism in prokaryotes. In Biochemistry of Lipids, Lipoproteins and Membranes, D.E. Vance and J.E. Vance, eds. (Amsterdam: Elsevier), pp. 59-96.
33. Schägger, H., and von Jagow, G. (1991). Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199, 223-231.
34. Schlame, M. (2008). Cardiolipin synthesis for the assembly of bacterial and mitochondrial membranes. J. Lipid Res. 49, 1607-1620.
35. Schlame, M., Rua, D., and Greenberg, M.L. (2000). The biosynthesis and functional role of cardiolipin. Prog. Lipid Res. 39, 257-288.
36. Stukey, J., and Carman, G.M. (1997). Identification of a novel phosphatase sequence motif. Protein Sci. 6, 469-472. (Pubitemid 27079942)
37. Sun, M.G., Williams, J., Munoz-Pinedo, C., Perkins, G.A., Brown, J.M., Ellisman, M.H., Green, D.R., and Frey, T.G. (2007). Correlated three-dimensional light and electron microscopy reveals transformation of mitochondria during apoptosis. Nat. Cell Biol. 9, 1057-1065.
38. Tonks, N.K. (2005). Redox redux: revisiting PTPs and the control of cell signaling. Cell 121, 667-670.
39. Tonks, N.K. (2006). Protein tyrosine phosphatases: from genes, to function, to disease. Nat. Rev. Mol. Cell Biol. 7, 833-846.
40. Tonks, N.K., and Neel, B.G. (2001). Combinatorial control of the specificity of protein tyrosine phosphatases. Curr. Opin. Cell Biol. 13, 182-195.
41. Van Blerkom, J. (2009). Mitochondria in early mammalian development. Semin. Cell Dev. Biol. 20, 354-364.
42. Vance, D., and Vance, J.E. (2008). Phospholipid biosynthesis in eukaryotes. In Biochemistry of Lipids, Lipoproteins and Membranes, D.E. Vance and J.E. Vance, eds. (Amsterdam: Elsevier), pp. 213-244.
43. Voet, D., and Voet, J.G. (2004). Electron transport and oxidative phosphorylation. In Biochemistry, Volume 1 (Hoboken, NJ: Wiley), pp. 797-842.
44. Warburg, O. (1956). On the origin of cancer cells. Science 123, 309-314.
45. Whitman, M., Downes, C.P., Keeler, M., Keller, T., and Cantley, L. (1988). Type I phosphatidylinositol kinase makes a novel inositol phospholipid, phosphatidylinositol- 3-phosphate. Nature 332, 644-646.
46. Wilson, J.E. (2003). Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J. Exp. Biol. 206, 2049-2057.
47. Wittig, I., Karas, M., and Schägger, 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.
48. Worby, C.A., Gentry, M.S., and Dixon, J.E. (2006). Laforin, a dual specificity phosphatase that dephosphorylates complex carbohydrates. J. Biol. Chem. 281, 30412-30418.
49. Wu, M., Neilson, A., Swift, A.L., Moran, R., Tamagnine, J., Parslow, D., Armistead, S., Lemire, K., Orrell, J., Teich, J., et al. (2007). Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 292, C125-C136.
50. Yan, L.J., and Forster, M.J. (2009). Resolving mitochondrial protein complexes using nongradient blue native polyacrylamide gel electrophoresis. Anal. Biochem. 389, 143-149.
51. Zerbetto, E., Vergani, L., and Dabbeni-Sala, F. (1997). Quantification of muscle mitochondrial oxidative phosphorylation enzymes via histochemical staining of blue native polyacrylamide gels. Electrophoresis 18, 2059-2064. (Pubitemid 27501265)
52. Zhong, Q., Gvozdenovic-Jeremic, J., Webster, P., Zhou, J., and Greenberg, M.L. (2005). Loss of function of KRE5 suppresses temperature sensitivity of mutants lacking mitochondrial anionic lipids. Mol. Biol. Cell 16, 665-675.