Lipid partitioning at the nuclear envelope controls membrane biogenesis

Molecular Biology of the Cell

Volumn 26, Issue 20, 2015, Pages 3641-3657

  Barbosa, Antonio Daniel ^a   Sembongi, Hiroshi ^a,d   Su, Wen Min ^b   Abreu, Susana ^c   Reggiori, Fulvio ^c   Carman, George M ^b   Siniossoglou, Symeon ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b RUTGERS UNIVERSITY   (United States)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d DRW Ltd Chesterford Research Park Little Chesterford   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DIACYLGLYCEROL; FAT DROPLET; LIPID; NEM1 PROTEIN; PHOSPHATIDATE PHOSPHATASE; PHOSPHOLIPID; PROTEIN; SPO7 PROTEIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; MEMBRANE LIPID; NUCLEAR PROTEIN; PAH1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ACIDIFICATION; ARTICLE; BIOGENESIS; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM MEMBRANE; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; METABOLIC ACTIVATION; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; MEMBRANE; METABOLISM;

ENDOPLASMIC RETICULUM; LIPID DROPLETS; LIPID METABOLISM; MEMBRANE LIPIDS; MEMBRANES; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; PHOSPHATIDATE PHOSPHATASE; PHOSPHOLIPIDS; SACCHAROMYCES CEREVISIAE PROTEINS; TRIGLYCERIDES;

EID: 84944145535     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-03-0173     Document Type: Article

References (71)

1. Adeyo O, Horn PJ, Lee S, Binns DD, Chandrahas A, Chapman KD, Goodman JM (2011). The yeast lipin orthologue Pah1p is important for biogenesis of lipid droplets. J Cell Biol 192, 1043-1055.
2. Bahmanyar S, Biggs R, Schuh AL, Desai A, Mler-Reichert T, Audhya A, Dixon JE, Oegema K (2014). Spatial control of phospholipid flux restricts endoplasmic reticulum sheet formation to allow nuclear envelope breakdown. Genes Dev 28, 121-126.
3. Bligh EG, Dyer WJ (1959). A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37, 911-917.
4. Campbell JL, Lorenz A, Witkin KL, Hays T, Loidl J, Cohen-Fix O (2006). Yeast nuclear envelope subdomains with distinct abilities to resist membrane expansion. Mol Biol Cell 17, 1768-1778.
5. Choi HS, Su WM, Han GS, Plote D, Xu Z, Carman GM (2012). Pho85p-Pho80p phosphorylation of yeast Pah1p phosphatidate phosphatase regulates its activity, location, abundance, and function in lipid metabolism. J Biol Chem 287, 11290-11301.
6. Choi HS, Su WM, Morgan JM, Han GS, Xu Z, Karanasios E, Siniossoglou S, Carman GM (2011). Phosphorylation of phosphatidate phosphatase regulates its membrane association and physiological functions in Saccharomyces cerevisiae: identification of Ser(602), Thr(723), and Ser(744) as the sites phosphorylated by CDC28 (CDK1)-encoded cyclin-dependent kinase. J Biol Chem 286, 1486-1498.
7. Cornell RB, Northwood IC (2000). Regulation of CTP:phosphocholine cytidylyltransferase by amphitropism and relocalization. Trends Biochem Sci 25, 441-447.
8. Csaki LS, Dwyer JR, Fong LG, Tontonoz P, Young SG, Reue K (2013). Lipins, lipinopathies, and the modulation of cellular lipid storage and signaling. Prog Lipid Res 52, 305-316. 85.
9. Currie E, Guo X, Christiano R, Chitraju C, Kory N, Harrison K, Haas J, Walther TC, Farese RV Jr (2014). High confidence proteomic analysis of yeast LDs identifies additional droplet proteins and reveals connections to dolichol synthesis and sterol acetylation. J Lipid Res 55, 1465-1477.
10. Dawaliby R, Mayer A (2010). Microautophagy of the nucleus coincides with a vacuolar diffusion barrier at nuclear-vacuolar junctions. Mol Biol Cell 21, 4173-4183.
11. Dechant R, Saad S, Ibez AJ, Peter M (2014). Cytosolic pH regulates cell growth through distinct GTPases, Arf1 and Gtr1, to promote Ras/PKA and TORC1 activity. Mol Cell 55, 409-421.
12. de Virgilio C (2012). The essence of yeast quiescence. FEMS Microbiol Rev 36, 306-339.
13. Donkor J, Sariahmetoglu M, Dewald J, Brindley DN, Reue K (2007). Three mammalian lipins act as phosphatidate phosphatases with distinct tissue expression patterns. J Biol Chem 282, 3450-3457.
14. Dubots E, Cottier S, Pi-Gulli MP, Jaquenoud M, Bontron S, Schneiter R, De Virgilio C (2014). TORC1 regulates Pah1 phosphatidate phosphatase activity via the Nem1/Spo7 protein phosphatase complex. PLoS One 9, e104194.
15. Eaton JM, Mullins GR, Brindley DN, Harris TE (2013). Phosphorylation of lipin 1 and charge on the phosphatidic acid head group control its phosphatidic acid phosphatase activity and membrane association. J Biol Chem 288, 9933-9945.
16. Eaton JM, Takkellapati S, Lawrence RT, McQueeney KE, Boroda S, Mullins GR, Sherwood SG, Finck BN, Vill J, Harris TE (2014). Lipin 2 binds phosphatidic acid by the electrostatic hydrogen bond switch mechanism independent of phosphorylation. J Biol Chem 289, 18055-18066.
17. Fakas S, Konstantinou C, Carman GM (2011). DGK1-encoded diacylglycerol kinase activity is required for phospholipid synthesis during growth resumption from stationary phase in Saccharomyces cerevisiae. J Biol Chem 286, 1464-1474.
18. Gaspar ML, Jesch SA, Viswanatha R, Antosh AL, Brown WJ, Kohlwein SD, Henry SA (2008). A block in endoplasmic reticulum-To-Golgi trafficking inhibits phospholipid synthesis and induces neutral lipid accumulation. J Biol Chem 283, 25735-25751.
19. Golden A, Liu J, Cohen-Fix O (2009). Inactivation of the C. elegans lipin homolog leads to ER disorganization and to defects in the breakdown and reassembly of the nuclear envelope. J Cell Sci 122, 1970-1978.
20. Gorjz M, Mattaj IW (2009). Lipin is required for efficient breakdown of the nuclear envelope in Caenorhabditis elegans. J Cell Sci 122, 1963-1969.
21. Griffith J, Mari M, De Maziere A, Reggiori F (2008). A cryosectioning procedure for the ultrastructural analysis and the immunogold labelling of yeast Saccharomyces cerevisiae. Traffic 9, 1060-1072.
22. Grimsey N, Han GS, OHara 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. Han GS, OHara L, Carman GM, Siniossoglou S (2008). An unconventional diacylglycerol kinase that regulates phospholipid synthesis and nuclear membrane growth. J Biol Chem 283, 20433-20442.
24. Han GS, Wu WI, Carman GM (2006). The Saccharomyces cerevisiae Lipin homolog is a Mg2+-dependent phosphatidate phosphatase enzyme. J Biol Chem 281, 9210-9218.
25. 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.
26. Henderson RJ, Tocher DR (1992). Thin-layer chromatography. In: Lipid Analysis, ed. RJ Hamilton and S Hamilton, New York: IRL Press, 65-111.
27. Hsieh LS, Su WM, Han GS, Carman GM (2015). Phosphorylation regulates the ubiquitin-independent degradation of yeast Pah1 phosphatidate phosphatase by the 20S proteasome. J Biol Chem 290, 11467-11478.
28. Huffman TA, Mothe-Satney I, Lawrence JC Jr (2002). Insulin-stimulated phosphorylation of lipin mediated by the mammalian target of rapamycin. Proc Natl Acad Sci USA 99, 1047-1052.
29. Jacquier N, Choudhary V, Mari M, Toulmay A, Reggiori F, Schneiter R (2011). Lipid droplets are functionally connected to the endoplasmic reticulum in Saccharomyces cerevisiae. J Cell Sci 124, 2424-2437.
30. Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, Maekawa H, Moreno-Borchart A, Doenges G, Schwob E, Schiebel E, Knop M (2004). A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947-962.
31. Karanasios E, Barbosa AD, Sembongi H, Mari M, Han GS, Reggiori F, Carman GM, Siniossoglou S (2013). Regulation of lipid droplet and membrane biogenesis by the acidic tail of the phosphatidate phosphatase Pah1p. Mol Biol Cell 24, 2124-2133.
32. Karanasios E, Han GS, Xu X, Carman GM, Siniossoglou S (2010). A phosphorylation-regulated amphipathic helix controls the membrane translocation and function of the yeast phosphatidate phosphatase. Proc Natl Acad Sci USA 107, 17539-17544.
33. Klig LS, Homann MJ, Carman GM, Henry SA (1985). Coordinate regulation of phospholipid biosynthesis in Saccharomyces cerevisiae: pleiotropically constitutive opi1 mutant. J Bacteriol 162, 1135-1141.
34. Kohlwein SD, Eder S, Oh CS, Martin CE, Gable K, Bacikova D, Dunn T (2001). Tsc13p is required for fatty acid elongation and localizes to a novel structure at the nuclear-vacuolar interface in Saccharomyces cerevisiae. Mol Cell Biol 21, 109-125.
35. Kohlwein SD, Veenhuis M, van der Klei IJ (2013). Lipid droplets and peroxisomes: key players in cellular lipid homeostasis or a matter of fat-store em up or burn em down. Genetics 193, 1-50.
36. Kooijman EE, Tieleman DP, Testerink C, Munnik T, Rijkers DT, Burger KN, de Kruijff B (2007). An electrostatic/hydrogen bond switch as the basis for the specific interaction of phosphatidic acid with proteins. J Biol Chem 282, 11356-11364.
37. Kvam E, Goldfarb DS (2007). Nucleus-vacuole junctions and piecemeal microautophagy of the nucleus in S. cerevisiae. Autophagy 3, 85-92.
38. Levine TP, Munro S (2001). Dual targeting of Osh1p, a yeast homologue of oxysterol-binding protein, to both the Golgi and the nucleus-vacuole junction. Mol Biol Cell 12, 1633-1644.
39. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
40. Lopes JM, Hirsch JP, Chorgo PA, Schulze KL, Henry SA (1991). Analysis of sequences in the INO1 promoter that are involved in its regulation by phospholipid precursors. Nucleic Acids Res 19, 1687-1693.
41. MacKinnon MA, Curwin AJ, Gaspard GJ, Suraci AB, Ferndez-Murray JP, McMaster CR (2009). The Kap60-Kap95 karyopherin complex directly regulates phosphatidylcholine synthesis. J Biol Chem 284, 7376-7384.
42. Mall M, Walter T, Gorjz M, Davidson IF, Nga Ly-Hartig TB, Ellenberg J, Mattaj IW (2012). Mitotic lamin disassembly is triggered by lipid-mediated signaling. J Cell Biol 198, 981-990.
43. Mollapour M, Shepherd A, Piper PW (2008). Novel stress responses facilitate Saccharomyces cerevisiae growth in the presence of the monocarboxylate preservatives. Yeast 25, 169-177.
44. Oelkers P, Cromley D, Padamsee M, Billheimer JT, Sturley SL (2002). The DGA1 gene determines a second triglyceride synthetic pathway in yeast. J Biol Chem 277, 8877-8881.
45. Orij R, Urbanus ML, Vizeacoumar FJ, Giaever G, Boone C, Nislow C, Brul S, Smits GJ (2012). Genome-wide analysis of intracellular pH reveals quantitative control of cell division rate by pH(c) in Saccharomyces cerevisiae. Genome Biol 13, R80.
46. OHara L, Han GS, Peak-Chew S, Grimsey N, Carman GM, Siniossoglou S (2006). Control of phospholipid synthesis by phosphorylation of the yeast lipin Pah1p/Smp2p Mg2+-dependent phosphatidate phosphatase. J Biol Chem 281, 34537-34548.
47. Pan X, Roberts P, Chen Y, Kvam E, Shulga N, Huang K, Lemmon S, Goldfarb DS (2000). Nucleus-vacuole junctions in Saccharomyces cerevisiae are formed through the direct interaction of Vac8p with Nvj1p. Mol Biol Cell 11, 2445-2457.
48. Pascual F, Carman GM (2013). Phosphatidate phosphatase, a key regulator of lipid homeostasis. Biochim Biophys Acta 1831, 514-522.
49. Pascual F, Hsieh LS, Soto-Cardalda A, Carman GM (2014). Yeast Pah1p phosphatidate phosphatase is regulated by proteasome-mediated degradation. J Biol Chem 289, 9811-9822.
50. Peterfy 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 27, 121-124.
51. Petschnigg J, Wolinski H, Kolb D, Zellnig G, Kurat CF, Natter K, Kohlwein SD (2009). Good fat, essential cellular requirements for triacylglycerol synthesis to maintain membrane homeostasis in yeast. J Biol Chem 284, 30981-30993.
52. Pol A, Gross SP, Parton RG (2014). Biogenesis of the multifunctional lipid droplet: lipids, proteins, and sites. J Cell Biol 204, 635-646.
53. Reynolds A, Lundblad V, Dorris D, Keaveney M (2001). Yeast vectors and assays for expression of cloned genes. Curr Protoc Mol Biol Chapter 13, Unit 13.6.
54. 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.
55. Shin JJ, Loewen CJ (2011). Putting the pH into phosphatidic acid signaling. BMC Biol 9, 85.
56. Siniossoglou S (2009). Lipins, lipids and nuclear envelope structure. Traffic 10, 1181-1187.
57. Siniossoglou S, Hurt EC, Pelham HR (2000). Psr1p/Psr2p, two plasma membrane phosphatases with an essential DXDX(T/V) motif required for sodium stress response in yeast. J Biol Chem 275, 19352-19360.
58. Siniossoglou S, Santos-Rosa H, Rappsilber J, Mann M, Hurt E (1998). A novel complex of membrane proteins required for formation of a spherical nucleus. EMBO J 17, 6449-6464.
59. Su WM, Han GS, Carman GM (2014). Yeast Nem1-Spo7 protein phosphatase activity on Pah1 phosphatidate phosphatase is specific for the Pho85-Pho80 protein kinase phosphorylation sites. J Biol Chem 289, 34699-34708.
60. Su WM, Han GS, Casciano J, Carman GM (2012). Protein kinase A-mediated phosphorylation of Pah1p phosphatidate phosphatase functions in conjunction with the Pho85p-Pho80p and Cdc28p-cyclin B kinases to regulate lipid synthesis in yeast. J Biol Chem 287, 33364-33376.
61. Tange Y, Hirata A, Niwa O (2002). An evolutionarily conserved fission yeast protein, Ned1, implicated in normal nuclear morphology and chromosome stability, interacts with Dis3, Pim1/RCC1 and an essential nucleoporin. J Cell Sci 115, 4375-4385.
62. Thomas BJ, Rothstein R (1989). Elevated recombination rates in transcriptionally active DNA. Cell 56, 619-630.
63. Toulmay A, Prinz WA (2013). Direct imaging reveals stable, micrometerscale lipid domains that segregate proteins in live cells. J Cell Biol 202, 35-44.
64. Vaden DL, Gohil VM, Gu Z, Greenberg ML (2005). Separation of yeast phospholipids using one-dimensional thin-layer chromatography. Anal Biochem 338, 162-164.
65. Wang CW, Lee SC (2012). The ubiquitin-like (UBX)-domain-containing protein Ubx2/Ubxd8 regulates lipid droplet homeostasis. J Cell Sci 125, 2930-2939.
66. Wang CW, Miao YH, Chang YS (2014). A sterol-enriched vacuolar microdomain mediates stationary phase lipophagy in budding yeast. J Cell Biol 206, 357-366.
67. Wimmer C, Doye V, Grandi P, Nehrbass U, Hurt EC (1992). A new subclass of nucleoporins that functionally interact with nuclear pore protein NSP1. EMBO J 11, 5051-5061.
68. Witkin KL, Chong Y, Shao S, Webster MT, Lahiri S, Walters AD, Lee B, Koh JL, Prinz WA, Andrews BJ, Cohen-Fix O (2012). The budding yeast nuclear envelope adjacent to the nucleolus serves as a membrane sink during mitotic delay. Curr Biol 22, 1128-1133.
69. Yen CL, Stone SJ, Koliwad S, Harris C, Farese RV Jr (2008). Thematic review series: glycerolipids. DGAT enzymes and triacylglycerol biosynthesis. J Lipid Res 49, 2283-2301.
70. Yorimitsu T, Zaman S, Broach JR, Klionsky DJ (2007). Protein kinase A and Sch9 cooperatively regulate induction of autophagy in Saccharomyces cerevisiae. Mol Biol Cell 18, 4180-4189.
71. Zhang P, Verity MA, Reue K (2014). Lipin-1 regulates autophagy clearance and intersects with statin drug effects in skeletal muscle. Cell Metab 20, 267-279.