Phosphatidylserine decarboxylase 1 autocatalysis and function does not require a mitochondrial-specific factor

Journal of Biological Chemistry

Volumn 290, Issue 20, 2015, Pages 12744-12752

  Onguka, Ouma ^a   Calzada, Elizabeth ^a   Ogunbona, Oluwaseun B ^a   Claypool, Steven M ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ENZYMES; PHOSPHOLIPIDS; YEAST;

AUTOCATALYTIC PROCESSING; METABOLIC PATHWAYS; MITOCHONDRIAL ENZYMES; MITOCHONDRIAL FUNCTION; OXIDATIVE PHOSPHORYLATION; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLSERINE; SECRETORY PATHWAYS;

MOBILE SECURITY;

PHOSPHATIDYLSERINE; PHOSPHATIDYLSERINE DECARBOXYLASE; PHOSPHATIDYLSERINE DECARBOXYLASE 1; PHOSPHOLIPID; PROTEIN; SERINE; UNCLASSIFIED DRUG; CARBOXYLYASE; MITOCHONDRIAL PROTEIN; PSD1 PROTEIN, S CEREVISIAE;

ALPHA CHAIN; AMINO ACID SEQUENCE; ARTICLE; AUTOCATALYSIS; BETA CHAIN; CATALYSIS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; HUMAN; IN VIVO STUDY; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; SUICIDE SUBSTRATE; YEAST; ENZYME ACTIVATION; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE;

MURINAE;

AMINO ACID MOTIFS; CARBOXY-LYASES; CATALYSIS; ENZYME ACTIVATION; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE;

EID: 84929340864     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.641118     Document Type: Article

References (56)

1. Birner, R., Nebauer, R., Schneiter, R., and Daum, G. (2003) Synthetic lethal interaction of the mitochondrial phosphatidylethanolamine biosynthetic machinery with the prohibitin complex of Saccharomyces cerevisiae. Mol. Biol. Cell 14, 370-383
2. Zborowski, J., Dygas, A., and Wojtczak, L. (1983) Phosphatidylserine decarboxylase is located on the external side of the inner mitochondrial membrane. FEBS Lett. 157, 179-182
3. Choi, J.-Y., Martin, W. E., Murphy, R. C., and Voelker, D. R. (2004) Phosphatidylcholine and N-methylated phospholipids are nonessential in Saccharomyces cerevisiae. J. Biol. Chem. 279, 42321-42330
4. Cui, Z., Vance, J. E., Chen, M. H., Voelker, D. R., and Vance, D. E. (1993) Cloning and expression of a novel phosphatidylethanolamine N-methyltransferase: a specific biochemical and cytological marker for a unique membrane fraction in rat liver. J. Biol. Chem. 268, 16655-16663
5. Summers, E. F., Letts, V. A., McGraw, P., and Henry, S. A. (1988) Saccharomyces cerevisiae cho2 mutants are deficient in phospholipid methylation and cross-pathway regulation of inositol synthesis. Genetics 120, 909-922
6. Waechter, C. J., and Lester, R. L. (1973) Differential regulation of the N-methyl transferases responsible for phosphatidylcholine synthesis in Saccharomyces cerevisiae. Arch. Biochem. Biophys. 158, 401-410
7. Horvath, S. E., Böttinger, L., Vögtle, F. N., Wiedemann, N., Meisinger, C., Becker, T., and Daum, G. (2012) Processing and topology of the yeast mitochondrial phosphatidylserine decarboxylase 1. J. Biol. Chem. 287, 36744-36755
8. Tamura, Y., Onguka, O., Itoh, K., Endo, T., Iijima, M., Claypool, S. M., and Sesaki, H. (2012) Phosphatidylethanolamine biosynthesis in mitochondria: phosphatidylserine (PS) trafficking is independent of a PS decarboxylase and intermembrane space proteins UPS1P and UPS2P. J. Biol. Chem. 287, 43961-43971
9. Zinser, E., Sperka-Gottlieb, C. D., Fasch, E. V., Kohlwein, S. D., Paltauf, F., and Daum, G. (1991) Phospholipid synthesis and lipid composition of subcellular membranes in the unicellular eukaryote Saccharomyces cerevisiae. J. Bacteriol. 173, 2026-2034
10. Trotter, P. J., and Voelker, D. R. (1995) Identification of a non-mitochondrial phosphatidylserine decarboxylase activity (PSD2) in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 270, 6062-6070
11. Birner, R., Bürgermeister, M., Schneiter, R., and Daum, G. (2001) Roles of phosphatidylethanolamine and of its several biosynthetic pathways in Saccharomyces cerevisiae. Mol. Biol. Cell 12, 997-1007
12. Bürgermeister, M., Birner-Grünberger, R., Nebauer, R., and Daum, G. (2004)Contributionofdifferentpathwaystothesupplyofphosphatidylethanolamine and phosphatidylcholine to mitochondrial membranes of the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1686, 161-168
13. Carman, G. M., and Han, G. S. (2011) Regulation of phospholipid synthesis in the yeast Saccharomyces cerevisiae. Annu. Rev. Biochem. 80, 859-883
14. Schuiki, I., and Daum, G. (2009) Phosphatidylserine decarboxylase, key enzymes of lipid metabolism. IUBMB Life 61, 151-162
15. Fullerton, M. D., Hakimuddin, F., and Bakovic, M. (2007) Developmental and metabolic effects of disruption of the mouse CTP:phosphoethanolamine cytidylyltransferase gene (Pcyt2). Mol. Cell Biol. 27, 3327-3336
16. Steenbergen, R., Nanowski, T. S., Beigneux, A., Kulinski, A., Young, S. G., and Vance, J. E. (2005) Disruption of the phosphatidylserine decarboxylase gene in mice causes embryonic lethality and mitochondrial defects. J. Biol. Chem. 280, 40032-40040
17. Shiao, Y. J., Lupo, G., and Vance, J. E. (1995) Evidence that phosphatidylserine is imported into mitochondria via a mitochondria-associated membrane and that the majority of mitochondrial phosphatidylethanolamine is derived from decarboxylation of phosphatidylserine. J. Biol. Chem. 270, 11190-11198
18. Böttinger, L., Horvath, S. E., Kleinschroth, T., Hunte, C., Daum, G., Pfanner, N., and Becker, T. (2012) Phosphatidylethanolamine and cardiolipin differentially affect the stability of mitochondrial respiratory chain supercomplexes. J. Mol. Biol. 423, 677-686
19. Joshi, A. S., Thompson, M. N., Fei, N., Hüttemann, M., and Greenberg, M. L. (2012) Cardiolipin and mitochondrial phosphatidylethanolamine have overlapping functions in mitochondrial fusion in Saccharomyces cerevisiae. J. Biol. Chem. 287, 17589-17597
20. Tasseva, G., Bai, H. D., Davidescu, M., Haromy, A., Michelakis, E., and Vance, J. E. (2013) Phosphatidylethanolamine deficiency in mammalian mitochondria impairs oxidative phosphorylation and alters mitochondrial morphology. J. Biol. Chem. 288, 4158-4173
21. Trotter, P. J., Pedretti, J., and Voelker, D. R. (1993) Phosphatidylserine decarboxylase from Saccharomyces cerevisiae: isolation of mutants, cloning of the gene, and creation of a null allele. J. Biol. Chem. 268, 21416-21424
22. 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
23. Shinzawa-Itoh, K., Aoyama, H., Muramoto, K., Terada, H., Kurauchi, T., Tadehara, Y., Yamasaki, A., Sugimura, T., Kurono, S., Tsujimoto, K., Mizushima, T., Yamashita, E., Tsukihara, T., and Yoshikawa, S. (2007) Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO J. 26, 1713-1725
24. Becker, T., Horvath, S. E., Böttinger, L., Gebert, N., Daum, G., and Pfanner, N. (2013) Role of phosphatidylethanolamine in the biogenesis of mitochondrial outer membrane proteins. J. Biol. Chem. 288, 16451-16459
25. Li, Q. X., and Dowhan, W. (1990) Studies on the mechanism of formation of the pyruvate prosthetic group of phosphatidylserine decarboxylase from Escherichia coli. J. Biol. Chem. 265, 4111-4115
26. Dowhan, W., Wickner, W. T., and Kennedy, E. P. (1974) Purification and properties of phosphatidylserine decarboxylase from Escherichia coli. J. Biol. Chem. 249, 3079-3084
27. Gulshan, K., Schmidt, J. A., Shahi, P., and Moye-Rowley, W. S. (2008) Evidence for the bifunctional nature of mitochondrial phosphatidylserine decarboxylase: role in Pdr3-dependent retrograde regulation of PDR5 expression. Mol. Cell Biol. 28, 5851-5864
28. Kuge, O., Saito, K., Kojima, M., Akamatsu, Y., and Nishijima, M. (1996) Post-translational processing of the phosphatidylserine decarboxylase gene product in Chinese hamster ovary cells. Biochem. J. 319, 33-38
29. Li, Q. X., and Dowhan, W. (1988) Structural characterization of Escherichia coli phosphatidylserine decarboxylase. J. Biol. Chem. 263, 11516-11522
30. Satre, M., and Kennedy, E. P. (1978) Identification of bound pyruvate essential for the activity of phosphatidylserine decarboxylase of Escherichia coli. J. Biol. Chem. 253, 479-483
31. Choi, J. Y., Augagneur, Y., Ben Mamoun, C., and Voelker, D. R. (2012) Identification of gene encoding Plasmodium knowlesi phosphatidylserine decarboxylase by genetic complementation in yeast and characterization of in vitro maturation of encoded enzyme. J. Biol. Chem. 287, 222-232
32. 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
33. Wach, A., Brachat, A., Pöhlmann, R., and Philippsen, P. (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808
34. 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
35. Johnson, L. M., Bankaitis, V. A., and Emr, S. D. (1987) Distinct sequence determinants direct intracellular sorting and modification of a yeast vacuolar protease. Cell 48, 875-885
36. 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
37. Meisinger, C., Pfanner, N., and Truscott, K. N. (2006) Isolation of yeast mitochondria. Methods Mol. Biol. 313, 33-39
38. 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
39. 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 β2-microglobu-lin. J. Biol. Chem. 277, 28038-28050
40. 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
41. 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
42. Riezman, H., Hay, R., Gasser, S., Daum, G., Schneider, G., Witte, C., and Schatz, G. (1983) The outer membrane of yeast mitochondria: isolation of outside-out sealed vesicles. EMBO J. 2, 1105-1111
43. Tamura, Y., Onguka, O., Hobbs, A. E., Jensen, R. E., Iijima, M., Claypool, S. M., and Sesaki, H. (2012) Role for two conserved intermembrane space proteins, Ups1p and Ups2p, [corrected] in intra-mitochondrial phospholipid trafficking. J. Biol. Chem. 287, 15205-15218
44. 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
45. Goujon, M., McWilliam, H., Li, W., Valentin, F., Squizzato, S., Paern, J., and Lopez, R. (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res. 38, W695-699
46. McWilliam, H., Li, W., Uludag, M., Squizzato, S., Park, Y. M., Buso, N., Cowley, A. P., and Lopez, R. (2013) Analysis tool web services from the EMBL-EBI. Nucleic Acids Res. 41, W597-W600
47. Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J. D., and Higgins, D. G. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539
48. Atkinson, K., Fogel, S., and Henry, S. A. (1980) Yeast mutant defective in phosphatidylserine synthesis. J. Biol. Chem. 255, 6653-6661
49. Hovius, R., Faber, B., Brigot, B., Nicolay, K., and de Kruijff, B. (1992)On the mechanism of the mitochondrial decarboxylation of phosphatidylserine. J. Biol. Chem. 267, 16790-16795
50. Kohlwein, S. D., Kuchler, K., Sperka-Gottlieb, C., Henry, S. A., and Paltauf, F. (1988) Identification of mitochondrial and microsomal phosphatidylserine synthase in Saccharomyces cerevisiae as the gene product of the CHO1 structural gene. J. Bacteriol. 170, 3778-3781
51. Letts, V. A., Klig, L. S., Bae-Lee, M., Carman, G. M., and Henry, S. A. (1983) Isolation of the yeast structural gene for the membrane-associated enzyme phosphatidylserine synthase. Proc. Natl. Acad. Sci. 80, 7279-7283
52. Stone, S. J., and Vance, J. E. (2000) Phosphatidylserine synthase-1 and-2 are localized to mitochondria-associated membranes. J. Biol. Chem. 275, 34534-34540
53. Atkinson, K. D., Jensen, B., Kolat, A. I., Storm, E. M., Henry, S. A., and Fogel, S. (1980) Yeast mutants auxotrophic for choline or ethanolamine. J. Bacteriol. 141, 558-564
54. Claypool, S. M., and Koehler, C. M. (2012) The complexity of cardiolipin in health and disease. Trends Biochem. Sci. 37, 32-41
55. Chang, S. C., Heacock, P. N., Clancey, C. J., and Dowhan, W. (1998) The PEL1 gene (renamed PGS1) encodes the phosphatidylglycerophosphate synthase of Saccharomyces cerevisiae. J. Biol. Chem. 273, 9829-9836
56. Choi, J. Y., Duraisingh, M. T., Marti, M., Ben Mamoun, C., and Voelker, D. R. (2015) From protease to decarboxylase: the molecular metamorphosis of phosphatidylserine decarboxylase. J. Biol. Chem. 290, 10972-10980