Dictyostelium uses ether-linked inositol phospholipids for intracellular signalling

EMBO Journal

Volumn 33, Issue 19, 2014, Pages 2188-2200

  Clark, Jonathan ^a   Kay, Robert R ^b   Kielkowska, Anna ^a   Niewczas, Izabella ^a   Fets, Louise ^b,d   Oxley, David ^c   Stephens, Len R ^c   Hawkins, Phillip T ^c  

^a Babraham Biosciences Technologies Ltd   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c Signalling Programme Babraham Research Campus   (United Kingdom)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Dictyostelium; Ether lipids; Phosphoinositides; PI3K; Plasmanylinositol

Indexed keywords

CHEMOATTRACTANT; ETHER LIPID; HYDROCARBON; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PLASMANYLINOSITOL; UNCLASSIFIED DRUG; ETHER PHOSPHOLIPID; PHOSPHATIDYLINOSITOL;

ARTICLE; CELL STIMULATION; CONTROLLED STUDY; DICTYOSTELIUM DISCOIDEUM; ENZYME PHOSPHORYLATION; ENZYME REGULATION; INTRACELLULAR SIGNALING; MASS SPECTROMETRY; NONHUMAN; ANIMAL; DICTYOSTELIUM; ELECTROSPRAY MASS SPECTROMETRY; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; DICTYOSTELIUM; PHOSPHATIDYLINOSITOLS; PHOSPHOLIPID ETHERS; SIGNAL TRANSDUCTION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 84908099376     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201488677     Document Type: Article

References (63)

1. Anderson KE, Kielkowska A, Durrant TN, Juvin V, Clark J, Stephens LR, Hawkins PT (2013) Lysophosphatidylinositol-acyltransferase-1 (LPIAT1) is required to maintain physiological levels of PtdIns and PtdInsP(2) in the mouse. PLoS One 8: e58425
2. Balla T (2013) Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol Rev 93: 1019-1137
3. Blacklock BJ, Kelley D, Patel S (2008) A fatty acid elongase ELO with novel activity from Dictyostelium discoideum. Biochem Biophysl Res Comm 374: 226-230
4. Brites P, Waterham HR, Wanders RJ (2004) Functions and biosynthesis of plasmalogens in health and disease. Biochim Biophys Acta 1636: 219-231
5. Brown JR, Auger KR (2011) Phylogenomics of phosphoinositide lipid kinases: perspectives on the evolution of second messenger signaling and drug discovery. BMC Evol Biol 11: 4
6. Buczynski G, Grove B, Nomura A, Kleve M, Bush J, Firtel RA, Cardelli J (1997) Inactivation of two Dictyostelium discoideum genes, DdPIK1 and DdPIK2, encoding proteins related to mammalian phosphatidylinositide 3-kinases, results in defects in endocytosis, lysosome to postlysosome transport, and actin cytoskeleton organization. J Cell Biol 136: 1271-1286
7. Burman C, Ktistakis NT (2010) Regulation of autophagy by phosphatidylinositol 3-phosphate. FEBS Lett 584: 1302-1312
8. Clark J, Anderson KE, Juvin V, Smith TS, Karpe F, Wakelam MJ, Stephens LR, Hawkins PT (2011) Quantification of PtdInsP3 molecular species in cells and tissues by mass spectrometry. Nat Meth 8: 267-272
9. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443: 651-657
10. Dormann D, Weijer G, Dowler S, Weijer CJ (2004) In vivo analysis of 3-phosphoinositide dynamics during Dictyostelium phagocytosis and chemotaxis. J Cell Sci 117: 6497-6509
11. D'Souza K, Epand RM (2013) Enrichment of phosphatidylinositols with specific acyl chains. Biochim Biophys Acta 1838: 1501-1508
12. Engelman JA, Luo J, Cantley LC (2006) The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet 7: 606-619
13. Fets L, Nichols JM, Kay RR (2014) A PIP5 kinase essential for efficient chemotactic signaling. Curr Biol 24: 415-421
14. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509
15. Funamoto S, Milan K, Meili R, Firtel RA (2001) Role of phosphatidylinositol 30 kinase and a downstream pleckstrin homology domain-containing protein in controlling chemotaxis in Dictyostelium. J Cell Biol 153: 795-810
16. Gijon MA, Riekhof WR, Zarini S, Murphy RC, Voelker DR (2008) Lysophospholipid acyltransferases and arachidonate recycling in human neutrophils. J Biol Chem 283: 30235-30245
17. Guillou H, Stephens LR, Hawkins PT (2007) Quantitative measurement of phosphatidylinositol 3,4,5-trisphosphate. Meth Enzymol 434: 117-130
18. Han SI, Friehs K, Flaschel E (2004) Improvement of a synthetic medium for Dictyostelium discoideum. Process Biochem 39: 925-930
19. Hawkins PT, Anderson KE, Davidson K, Stephens LR (2006) Signalling through Class I PI3Ks in mammalian cells. Biochem Soc Trans 34: 647-662
20. Hoeller O, Kay RR (2007) Chemotaxis in the absence of PIP3 gradients. Curr Biol 17: 813-817
21. Hoeller O, Bolourani P, Clark J, Stephens LR, Hawkins PT, Weiner OD, Weeks G, Kay RR (2013) Two distinct functions for PI3-kinases in macropinocytosis. J Cell Sci 126: 4296-4307
22. Holub BJ (1984) 1982 Borden Award lecture. Nutritional, biochemical, and clinical aspects of inositol and phosphatidylinositol metabolism. Can J Physiol Pharmacol 62: 1-8
23. Holub BJ (1986) Metabolism and function of myo-inositol and inositol phospholipids. Ann Rev Nutr 6: 563-597
24. Iijima M, Devreotes P (2002) Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Cell 109: 599-610
25. Insall R, Kuspa A, Lilly PJ, Shaulsky G, Levin LR, Loomis WF, Devreotes P (1994) CRAC, a cytosolic protein containing a pleckstrin homology domain, is required for receptor and G protein-mediated activation of adenylyl cyclase in Dictyostelium. J Cell Biol 126: 1537-1545
26. Ivanova PT, Milne SB, Brown HA (2010) Identification of atypical ether-linked glycerophospholipid species in macrophages by mass spectrometry. J Lipid Res 51: 1581-1590
27. Kadamur G, Ross EM (2013) Mammalian phospholipase C. Ann Rev Physiol 75: 127-154
28. Kanzawa N, Maeda Y, Ogiso H, Murakami Y, Taguchi R, Kinoshita T (2009) Peroxisome dependency of alkyl-containing GPI-anchor biosynthesis in the endoplasmic reticulum. Proc Natl Acad Sci USA 106: 17711-17716
29. Kay RR (1987) Cell differentiation in monolayers and the investigation of slime mold morphogens. Meth Cell Biol 28: 433-448
30. Kay RR, Langridge P, Traynor D, Hoeller O (2008) Changing directions in the study of chemotaxis. Nat Rev Mol Cell Biol 9: 455-463
31. Kent C (1995) Eukaryotic phospholipid biosynthesis. Annu Rev Biochem 64: 315-343
32. Kielkowska A, Niewczas I, Anderson KE, Durrant TN, Clark J, Stephens LR, Hawkins PT (2014) A new approach to measuring phosphoinositides in cells by mass spectrometry. Adv Biol Reg 54: 131-141
33. King JS, Insall RH (2009) Chemotaxis: finding the way forward with Dictyostelium. Trend Cell Biol 19: 523-530
34. Kortholt A, King JS, Keizer-Gunnink I, Harwood AJ, Van Haastert PJ (2007) Phospholipase C regulation of phosphatidylinositol 3,4,5-trisphosphate-mediated chemotaxis. Mol Biol Cell 18: 4772-4779
35. Lee HC, Inoue T, Sasaki J, Kubo T, Matsuda S, Nakasaki Y, Hattori M, Tanaka F, Udagawa O, Kono N, Itoh T, Ogiso H, Taguchi R, Arita M, Sasaki T, Arai H (2012) LPIAT1 regulates arachidonic acid content in phosphatidylinositol and is required for cortical lamination in mice. Mol Biol Cell 23: 4689-4700
36. Lemmon MA (2008) Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 9: 99-111
37. Loovers HM, Postma M, Keizer-Gunnink I, Huang YE, Devreotes PN, van Haastert PJ (2006) Distinct roles of PI(3,4,5)P3 during chemoattractant signaling in Dictyostelium: a quantitative in vivo analysis by inhibition of PI3-kinase. Mol Biol Cel 17: 1503-1513
38. MacDonald G, Baker RR, Thompson W (1975) Selective synthesis of molecular classes of phosphatidic acid, diacylglycerol and phosphatidylinositol in rat brain. J Neurochem 24: 655-661
39. Madani S, Hichami A, Legrand A, Belleville J, Khan NA (2001) Implication of acyl chain of diacylglycerols in activation of different isoforms of protein kinase C. FASEB J 15: 2595-2601
40. Meili R, Ellsworth C, Firtel RA (2000) A novel Akt/PKB-related kinase is essential for morphogenesis in Dictyostelium. Curr Biol: CB 10: 708-717
41. Michell RH (2008) Inositol derivatives: evolution and functions. Nat Rev Mol Cell Biol 9: 151-161
42. Milne SB, Ivanova PT, DeCamp D, Hsueh RC, Brown HA (2005) A targeted mass spectrometric analysis of phosphatidylinositol phosphate species. J Lipid Res 46: 1796-1802
43. Montrucchio G, Alloatti G, Camussi G (2000) Role of platelet-activating factor in cardiovascular pathophysiology. Physiol Rev 80: 1669-1699
44. Muller-Taubenberger A, Kortholt A, Eichinger L (2013) Simple system- substantial share: the use of Dictyostelium in cell biology and molecular medicine. Eur J Cell Biol 92: 45-53
45. Nenci S, Piano V, Rosati S, Aliverti A, Pandini V, Fraaije MW, Heck AJ, Edmondson DE, Mattevi A (2012) Precursor of ether phospholipids is synthesized by a flavoenzyme through covalent catalysis. Proc Natl Acad Sci USA 109: 18791-18796
46. Parent CA, Blacklock BJ, Froelich WM, Murphy DB, Devreotes PN (1998) G Protein signaling events are activated at the leading edge of chemotactic cells. Cell 95: 81-91
47. Paulus H, Kennedy EP (1960) The enzymatic synthesis of inositol monophosphatide. J Biol Chem 235: 1303-1311
48. Pettitt TR, Dove SK, Lubben A, Calaminus SD, Wakelam MJ (2006) Analysis of intact phosphoinositides in biological samples. J Lipid Res 47: 1588-1596
49. Raiborg C, Schink KO, Stenmark H (2013) Class III phosphatidylinositol 3-kinase and its catalytic product PtdIns3P in regulation of endocytic membrane traffic. FEBS J 280: 2730-2742
50. Rouzer CA, Ivanova PT, Byrne MO, Milne SB, Marnett LJ, Brown HA (2006) Lipid profiling reveals arachidonate deficiency in RAW264.7 cells: structural and functional implications. Biochem 45: 14795-14808
51. Saarikangas J, Zhao H, Lappalainen P (2010) Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides. Physiol Rev 90: 259-289
52. Saito S, Goto K, Tonosaki A, Kondo H (1997) Gene cloning and characterization of CDP-diacylglycerol synthase from rat brain. J Biol Chem 272: 9503-9509
53. Scott DL, Otwinowski Z, Gelb MH, Sigler PB (1990) Crystal structure of bee-venom phospholipase A2 in a complex with a transition-state analogue. Science 250: 1563-1566
54. Shindou H, Hishikawa D, Harayama T, Yuki K, Shimizu T (2009) Recent progress on acyl CoA: lysophospholipid acyltransferase research. J Lipid Res 50(Suppl): S46-S51
55. Takeda K, Sasaki AT, Ha H, Seung HA, Firtel RA (2007) Role of phosphatidylinositol 3-kinases in chemotaxis in Dictyostelium. J Biol Chem 282: 11874-11884
56. Vance JE, Vance DE (2004) Phospholipid biosynthesis in mammalian cells. Biochem Cell Biol 82: 113-128
57. Veltman DM, Lemieux MG, Knecht DA, Insall RH (2014) PIP3-dependent macropinocytosis is incompatible with chemotaxis. J Cell Biol 204: 497-505
58. Wanders RJ, Waterham HR (2006) Biochemistry of mammalian peroxisomes revisited. Ann Rev Biochem 75: 295-332
59. Zatulovskiy E, Tyson R, Bretschneider T, Kay RR (2014) Bleb-driven chemotaxis of Dictyostelium cells. J Cell Biol 204: 1027-1044
60. Zhang P, Wang Y, Sesaki H, Iijima M (2010) Proteomic identification of phosphatidylinositol (3,4,5) triphosphate-binding proteins in Dictyostelium discoideum. Proc Natl Acad Sci USA 107: 11829-11834
61. Zhou KM, Takegawa K, Emr SD, Firtel RA (1995) A phosphatidylinositol (PI) kinase gene family in Dictyostelium discoideum: biological roles of putative mammalian p110 and yeast Vps34p PI 3-kinase homologs during growth and development. Mol Cell Biol 15: 5645-5656
62. Zhou K, Pandol S, Bokoch G, Traynor KA (1998) Disruption of Dictyostelium PI3K genes reduces [32P]phosphatidylinositol 3,4 bisphosphate and [32P] phosphatidylinositol trisphosphate levels, alters F-actin distribution and impairs pinocytosis. J Cell Sci 111: 283-294
63. Zoeller RA, Lake AC, Nagan N, Gaposchkin DP, Legner MA, Lieberthal W (1999) Plasmalogens as endogenous antioxidants: somatic cell mutants reveal the importance of the vinyl ether. Biochem J 338: 769-776