Lipins from plants are phosphatidate phosphatases that restore lipid synthesis in a pah1δ mutant strain of Saccharomyces cerevisiae

FEBS Journal

Volumn 278, Issue 5, 2011, Pages 764-775

  Mietkiewska, Elzbieta ^a   Siloto, Rodrigo M P ^a   Dewald, Jay ^a   Shah, Saleh ^b   Brindley, David N ^a   Weselake, Randall J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b Plant Biotechnology   (Canada)

Author keywords

lipin; phosphatidate phosphatase; Saccharomyces cerevisiae; subcellular localization; triacylglycerol

Indexed keywords

GREEN FLUORESCENT PROTEIN; LIPID; OLEIC ACID; PHOSPHATIDATE PHOSPHATASE;

ARABIDOPSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CYTOPLASM; ENZYME ACTIVITY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC CONSERVATION; LIPID COMPOSITION; LIPOGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLANT GROWTH; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MOTIF; RAPESEED; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; TEMPERATURE SENSITIVITY; TRANSCRIPTION REGULATION; YEAST CELL;

ARABIDOPSIS; BRASSICA NAPUS; CELL NUCLEUS; CYTOSOL; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; PHOSPHATIDATE PHOSPHATASE; PLANT PROTEINS; SACCHAROMYCES CEREVISIAE;

ARABIDOPSIS; BRASSICA NAPUS; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 79951904580     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07995.x     Document Type: Article

References (44)

1. Kocsis MG, Weselake RJ, Eng JA, Furukawa-Stoffer TL, &, Pomeroy MK, (1996) Phosphatidate phosphatase from developing seeds and microspore-derived cultures of Brassica napus. Phytochemistry 41, 353-363.
2. Carman GM, &, Han G-S, (2006) Roles of phosphatidate phosphatase enzymes in lipid metabolism. Trends Biochem Sci 31, 694-699. (Pubitemid 44791946)
3. Reue K, &, Brindley DN, (2008) Multiple roles for lipins/phosphatidate phosphatase enzymes in lipid metabolism. J Lipid Res 49, 2493-2503.
4. Kocsis MG, &, Weselake RJ, (1996) Phosphatidate phosphatases of mammals, yeast, and higher plants. Lipids 31, 785-802. (Pubitemid 26275321)
5. Carman GM, &, Henry SA, (2007) Phosphatidic acid plays a central role in the transcriptional regulation of glycerolipid synthesis in Saccharomyces cerevisiae. J Biol Chem 282, 37293-37297.
6. Jamal Z, Martin A, Gomez-Muñoz A, Hales P, Chang E, Russell JC, &, Brindley DN, (1992) Phosphatidate phosphohydrolases in liver, heart and adipose tissue of the JCR:LA corpulent rat and the lean genotypes: implications for glycerolipid synthesis and signal transduction. Int J Obes Relat Metab Disord 16, 789-799.
7. Athenstaedt K, &, Daum G, (1999) Phosphatidic acid, a key intermediate in lipid metabolism. Eur J Biochem 266, 1-16.
8. Carrasco S, &, Merida I, (2006) Diacylglycerol, when simplicity becomes complex. Trends Biochem Sci 32, 27-36.
9. Donkor J, Zhang P, Wong S, O'Loughlin L, Dewald J, Kok BPC, Brindley DN, &, Reue K, (2009) A conserved serine residue is required for the phosphatidate phosphatase activity but not the transcriptional coactivator functions of Lipin-1 and Lipin-2. J Biol Chem 284, 29968-29978.
10. Han GS, &, Carman GM, (2010) Characterization of the human LPIN1-encoded phosphatidate phosphatase isoforms. J Biol Chem 285, 14628-14638.
11. Brindley DN, &, Pilquil C, (2009) Lipid phosphate phosphatases and signaling. J Lipid Res 50 (Suppl), S225-S230.
12. Carman GM, (1997) Phosphatidate phosphatases and diacylglycerol pyrophosphate phosphatases in Saccharomyces cerevisiae and Echerichia coli. Biochim Biophys Acta 1348, 45-55. (Pubitemid 27467076)
13. Pearce ML, &, Slabas AR, (1998) Phosphatidate phosphatase from avocado (Persea americana)-purification, substrate specificity and possible metabolic implications for the Kennedy pathway and cell signalling in plants. Plant J 14, 555-564.
14. Pierrugues O, Brutesco C, Oshiro J, Gouy M, Deveaux Y, Carman GM, Thuriaux P, &, Kazmaier M, (2001) Lipid phosphate phosphatases in Arabidopsis. Regulation of the AtLPP1 gene in response to stress. J Biol Chem 276, 20300-20308.
15. Nakamura Y, Tsuchiya M, &, Ohta H, (2007) Plastidic phosphatidic acid phosphates identified in a distinct subfamily of lipid phosphate phosphatases with prokaryotic origin. J Biol Chem 282, 29013-29021. (Pubitemid 47606041)
16. 2+-dependent phosphatidate phosphatase enzyme. J Biol Chem 281, 9210-9218. (Pubitemid 43864636)
17. Siniossoglou S, (2009) Lipins, lipids and nuclear envelope structure. Traffic 10, 1181-1187.
18. Collet J-F, Stroobant V, Pirard M, Delpierre G, &, Van Schaftingen E, (1998) A new class of phosphotransferases phosphorylated on an aspartate residue in an amino-terminal DXDX(T/V) motif. J Biol Chem 273, 14107-14112. (Pubitemid 28319117)
19. Han GS, Siniossoglou S, &, Carman GM, (2007) The cellular functions of the yeast lipin homolog Pah1p are dependent on its phosphatidate phosphatase activity. J Biol Chem 282, 37026-37035.
20. Santos-Rosa H, Leung J, Grimsey N, Peak-Chew S, &, Siniossoglou S, (2005) The yeast lipin Smp2 couples phospholipid biosynthesis to nuclear membrane growth. EMBO J 24, 1931-1941. (Pubitemid 40896165)
21. 2+-dependent phosphatidate phosphatase. J Biol Chem 281, 34537-34548. (Pubitemid 46036661)
22. Grimsey N, Han GS, O'Hara L, Rochford JJ, Carman GM, &, Siniossoglou S, (2008) Temporal and spatial regulation of the phosphatidate phosphatases lipin 1 and 2. J Biol Chem 283, 29166-29174.
23. Harris TE, Huffman TA, Chi A, Shabanowitz J, Hunt DF, Kumar A, &, Lawrence JC Jr, (2007) Insulin controls subcellular localization and multisite phosphorylation of the phosphatidic acid phosphatase, lipin 1. J Biol Chem 282, 277-286. (Pubitemid 47076630)
24. Nakamura Y, Koizumi R, Shui G, Shimojima M, Wenk MR, Ito T, &, Ohta H, (2009) Arabidopsis lipins mediate eukaryotic pathway of lipid metabolism and cope critically with phosphate starvation. Proc Natl Acad Sci USA 106, 20978-20983.
25. Eastmond PJ, Quettier A-L, Kroon JTM, Craddock C, Adams N, &, Slabas AR, (2010) PHOSPHATIDIC ACID PHOSPHOHYDROLASE1 and 2 regulate phospholipid synthesis at the endoplasmic reticulum in Arabidopsis. Plant Cell 22, 2796-2811.
26. Mietkiewska E, Siloto RMP, Dewald J, Shah S, Brindley DN, &, Weselake RJ, (2010) Arabidopsis thaliana lipins complement pah1δ mutation in Saccharomyces cerevisiae. In Book of Abstracts. 19th International Plant Lipid Symposium. 11-16 July 2010, Cairns, Australia.
27. Reue K, &, Zhang P, (2008) The lipin protein family: dual roles in lipid biosynthesis and gene expression. FEBS Lett 582, 90-96.
28. Stukey J, &, Carman GM, (1997) Identification of a novel phosphatase sequence motif. Protein Sci 6, 469-472. (Pubitemid 27079942)
29. Brindley DN, &, Waggoner DW, (1998) Mammalian lipid phosphate phosphohydrolases. J Biol Chem 273, 24281-24284. (Pubitemid 28454910)
30. Brindley DN, (2004) Lipid phosphate phosphatases and related proteins: signaling functions in development, cell division, and cancer. J Cell Biochem 92, 900-912. (Pubitemid 44264240)
31. Carman GM, &, Han GS, (2009) Phosphatidic acid phosphatase, a key enzyme in the regulation of lipid synthesis. J Biol Chem 284, 2593-2597.
32. Péterfy M, Phan J, Xu P, &, Reue K, (2001) Lipodystrophy in the fld mouse results from mutation of a new gene encoding a nuclear protein, lipin. Nat Genet 2, 121-124. (Pubitemid 32044532)
33. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, &, O'Shea EK, (2003) Global analysis of protein localization in budding yeast. Nature 425, 686-691. (Pubitemid 37314307)
34. Cascales C, Mangiapane EH, &, Brindley DN, (1984) Oleic acid promotes the activation and translocation of phosphatidate phosphohydrolase from the cytosol to particulate fractions of isolated rat hepatocytes. Biochem J 219, 911-916. (Pubitemid 14141749)
35. Gomez-Munoz A, Hatch GM, Martin A, Jamal Z, Vance DE, &, Brindley DN, (1992) Effects of okadaic acid on the activities of two distinct phosphatidate phosphohydrolases in rat hepatocytes. FEBS Lett 301, 103-106.
36. Ichihara K, Murota N, &, Fujii S, (1990) Intracellular translocation of phosphatidate phosphatase in maturing safflower seeds: a possible mechanism of feedforward control of triacylglycerol synthesis by fatty acids. Biochim Biophys Acta 1043, 227-234. (Pubitemid 20103656)
37. Finck BN, Gropler MC, Chen Z, Leone TC, Croce MA, Harris TE, Lawrence JC Jr, &, Kelly DP, (2006) Lipin 1 is an inducible amplifier of the hepatic PGC-1a/PPARa regulatory pathway. Cell Metab 4, 199-210. (Pubitemid 44283957)
38. Mietkiewska E, Brost JM, Giblin EM, Barton DL, &, Taylor DC, (2007) Cloning and functional characterization of the Fatty Acid Elongase 1 (FAE1) gene from high erucic Crambe abyssinica cv. Prophet. Plant Biotechnol J 5, 636-645. (Pubitemid 47196365)
39. Sambrook J, Fritsch EF, &, Maniatis T, (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Czechowski T, Stitt M, Altmann T, Udvardi MK, &, Scheible W-R, (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139, 5-17. (Pubitemid 43951587)
41. Bligh EG, &, Dyer WJ, (1959) A rapid method for total lipid extraction and purification. Can J Biochem Physiol 37, 911-917.
42. Bradford MM, (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
43. Jamal Z, Martin A, Gomez-Muñoz A, &, Brindley DN, (1991) Plasma membrane fractions from rat liver contain a phosphatidate phospohydrolase distinct from that in the endoplasmic reticulum and cytosol. J Biol Chem 266, 2988-2996. (Pubitemid 21909165)
44. Martin A, Gomez-Muñoz A, Jamal Z, &, Brindley DN, (1991) Characterization and assay of phosphatidate phosphatase. Methods Enzymol 197, 553-563.