Biophysics and function of phosphatidic acid: A molecular perspective

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1791, Issue 9, 2009, Pages 881-888

  Kooijman, Edgar Eduard ^a   Burger, Koert N J ^b  

^a KENT STATE UNIVERSITY   (United States)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Anionic lipid; Electrostatic hydrogen bond switch; Hydrogen bond; Lipid protein interaction; MAS NMR; Model membrane; Phosphomonoester

Indexed keywords

PHOSPHATIDIC ACID;

BIOPHYSICS; ELECTRICITY; EUKARYOTIC CELL; HYDROGEN BOND; IONIZATION; LIPID MEMBRANE; MOLECULAR MODEL; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; REVIEW; SECOND MESSENGER;

BIOPHYSICAL PHENOMENA; HYDROGEN BONDING; LIPID BILAYERS; MODELS, BIOLOGICAL; PHOSPHATIDIC ACIDS; STATIC ELECTRICITY;

EUKARYOTA;

EID: 68949125160     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2009.04.001     Document Type: Review

References (71)

1. Athenstaedt K., and Daum G. Phosphatidic acid, a key intermediate in lipid metabolism. Eur. J. Biochem. 266 (1999) 1-16
2. Bargmann B.O., and Munnik T. The role of phospholipase D in plant stress responses. Curr. Opin. Plant. Biol. 9 (2006) 515-522
3. Cazzolli R., Shemon A.N., Fang M.Q., and Hughes W.E. Phospholipid signalling through phospholipase D and phosphatidic acid. IUBMB Life 58 (2006) 457-461
4. Roth M.G. Molecular mechanisms of PLD function in membrane traffic. Traffic 9 (2008) 1233-1239
5. Wang X., Devaiah S.P., Zhang W., and Welti R. Signaling functions of phosphatidic acid. Prog. Lipid Res. 45 (2006) 250-278
6. Stace C.L., and Ktistakis N.T. Phosphatidic acid- and phosphatidylserine-binding proteins. Biochim. Biophys. Acta 1761 (2006) 913-926
7. Testerink C., and Munnik T. Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci. 10 (2005) 368-375
8. Op den Kamp J.A. Lipid asymmetry in membranes. Annu. Rev. Biochem. 48 (1979) 47-71
9. van Meer G. Lipids of the Golgi membrane. Trends Cell Biol. 8 (1998) 29-33
10. Vance J.E., and Steenbergen R. Metabolism and functions of phosphatidylserine. Prog. Lipid Res. 44 (2005) 207-234
11. Yeung T., Gilbert G.E., Shi J., Silvius J., Kapus A., and Grinstein S. Membrane phosphatidylserine regulates surface charge and protein localization. Science 319 (2008) 210-213
12. Kim J., Mosior M., Chung L.A., Wu H., and McLaughlin S. Binding of peptides with basic residues to membranes containing acidic phospholipids. Biophys. J. 60 (1991) 135-148
13. Montich G., Scarlata S., McLaughlin S., Lehrmann R., and Seelig J. Thermodynamic characterization of the association of small basic peptides with membranes containing acidic lipids. Biochim. Biophys. Acta 1146 (1993) 17-24
14. Roy M.O., Leventis R., and Silvius J.R. Mutational and biochemical analysis of plasma membrane targeting mediated by the farnesylated, polybasic carboxy terminus of K-ras4B. Biochemistry 39 (2000) 8298-8307
15. Arbuzova A., Murray D., and McLaughlin S. MARCKS, membranes, and calmodulin: kinetics of their interaction. Biochim. Biophys. Acta 1376 (1998) 369-379
16. Lemmon M.A. Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9 (2008) 99-111
17. Killian J.A., and von Heijne G. How proteins adapt to a membrane-water interface. Trends Biochem. Sci. 25 (2000) 429-434
18. van Klompenburg W., Nilsson I., von Heijne G., and de Kruijff B. Anionic phospholipids are determinants of membrane protein topology. EMBO J. 16 (1997) 4261-4266
19. McLaughlin S. The electrostatic properties of membranes. Annu. Rev. Biophys. Biophys. Chem. 18 (1989) 113-136
20. Cevc G. Membrane electrostatics. Biochim. Biophys. Acta 1031 (1990) 311-382
21. Tocanne J.F., and Teissie J. Ionization of phospholipids and phospholipid-supported interfacial lateral diffusion of protons in membrane model systems. Biochim. Biophys. Acta 1031 (1990) 111-142
22. Kooijman E.E., Carter K.M., van Laar E.G., Chupin V., Burger K.N.J., and de Kruijff B. What makes the bioactive lipids phosphatidic acid and lysophosphatidic acid so special?. Biochemistry 44 (2005) 17007-17015
23. Boggs J.M. Lipid intermolecular hydrogen bonding: influence on structural organization and membrane function. Biochim. Biophys. Acta 906 (1987) 353-404
24. Kates M., Syz J.Y., Gosser D., and Haines T.H. pH-dissociation characteristics of cardiolipin and its 2′-deoxy analogue. Lipids 28 (1993) 877-882
25. a values for phosphatidylcholine, phosphatidylethanolamine, and phosphatidylserine in monolayers deposited on mercury electrodes. Biophys. J. 66 (1994) 1969-1980
26. Haines T.H., and Dencher N.A. Cardiolipin: a proton trap for oxidative phosphorylation. FEBS Lett. 528 (2002) 35-39
27. Hauser H. Mechanism of spontaneous vesiculation. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 5351-5355
28. Koter M., de Kruijff B., and van Deenen L.L. Calcium-induced aggregation and fusion of mixed phosphatidylcholine-phosphatidic acid vesicles as studied by 31P NMR. Biochim. Biophys. Acta 514 (1978) 255-263
29. Swairjo M.A., Seaton B.A., and Roberts M.F. Effect of vesicle composition and curvature on the dissociation of phosphatidic acid in small unilamellar vesicles-a 31P-NMR study. Biochim. Biophys. Acta 1191 (1994) 354-361
30. Watts A. Solid-state NMR approaches for studying the interaction of peptides and proteins with membranes. Biochim. Biophys. Acta 1376 (1998) 297-318
31. Kooijman E.E., Chupin V., Fuller N.L., Kozlov M.M., de Kruijff B., Burger K.N.J., and Rand P.R. Spontaneous curvature of phosphatidic acid and lysophosphatidic acid. Biochemistry 44 (2005) 2097-2102
32. Appleton T.G., Hall J.R., Ralph S.F., and Thompson C.S.M. NMR-study of acid-base equilibria and other reactions of ammineplatinum complexes with aqua and hydroxo ligands. Inorg. Chem. 28 (1989) 1989-1993
33. Pascher I., and Sundell S. Interactions and space requirements of the phosphate head group in membrane lipids. The crystal structure of disodium lysophosphatidate dihydrate. Chem. Phys. Lipids 37 (1985) 241-250
34. Kooijman E.E., Tieleman D.P., Testerink C., Munnik T., Rijkers D.T., Burger K.N.J., and de Kruijff B. An electrostatic/hydrogen bond switch as the basis for the specific interaction of phosphatidic acid with proteins. J. Biol. Chem. 282 (2007) 11356-11364
35. Kooijman E.E., Sot J., Montes L.R., Alonso A., Gericke A., De Kruijff B., Kumar S., and Goni F.M. Membrane organization and ionization properties of the minor but crucial lipid ceramide-1-phosphate. Biophys. J. (2008) accepted for publication
36. a and binding constants: intramolecular and intermolecular influences. J. Mol. Graph. Model. 26 (2007) 519-528
37. Lynch K.R., and Macdonald T.L. Structure-activity relationships of lysophosphatidic acid analogs. Biochim. Biophys. Acta 1582 (2002) 289-294
38. Sardar V.M., Bautista D.L., Fischer D.J., Yokoyama K., Nusser N., Virag T., Wang D.A., Baker D.L., Tigyi G., and Parrill A.L. Molecular basis for lysophosphatidic acid receptor antagonist selectivity. Biochim. Biophys. Acta 1582 (2002) 309-317
39. Felemez M., and Spiess B. 1H NMR titrations of hydroxy protons in aqueous solution as a method of investigation of intramolecular hydrogen-bonding in phosphorylated compounds: examples of myo-inositol 2-phosphate and myo-inositol 1,2,6-tris(phosphates). J. Am. Chem. Soc. 125 (2003) 7768-7769
40. a. J. Am. Chem. Soc. 127 (2005) 15848-15861
41. Lee A.G. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta 1666 (2004) 62-87
42. Lee A.G. Ion channels: a paddle in oil. Nature 444 (2006) 697
43. Schmidt D., Jiang Q.X., and MacKinnon R. Phospholipids and the origin of cationic gating charges in voltage sensors. Nature 444 (2006) 775-779
44. Zimmerberg J., and Kozlov M.M. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7 (2006) 9-19
45. Deol S.S., Domene C., Bond P.J., and Sansom M.S. Anionic phospholipid interactions with the potassium channel KcsA: simulation studies. Biophys. J. 90 (2006) 822-830
46. Powl A.M., East J.M., and Lee A.G. Heterogeneity in the binding of lipid molecules to the surface of a membrane protein: hot spots for anionic lipids on the mechanosensitive channel of large conductance MscL and effects on conformation. Biochemistry 44 (2005) 5873-5883
47. Raja M., Spelbrink R.E., de Kruijff B., and Killian J.A. Phosphatidic acid plays a special role in stabilizing and folding of the tetrameric potassium channel KcsA. FEBS Lett. 581 (2007) 5715-5722
48. Ochoa W.F., Corbalan-Garcia S., Eritja R., Rodriguez-Alfaro J.A., Gomez-Fernandez J.C., Fita I., and Verdaguer N. Additional binding sites for anionic phospholipids and calcium ions in the crystal structures of complexes of the C2 domain of protein kinase calpha. J. Mol. Biol. 320 (2002) 277-291
49. Sanchez-Bautista S., de Godos A., Rodriguez-Alfaro J.A., Torrecillas A., Corbalan-Garcia S., and Gomez-Fernandez J.C. Interaction of the C2 domain from protein kinase C(epsilon) with model membranes. Biochemistry 46 (2007) 3183-3192
50. Cho W., and Stahelin R.V. Membrane binding and subcellular targeting of C2 domains. Biochim. Biophys. Acta 1761 (2006) 838-849
51. Corbalan-Garcia S., Guerrero-Valero M., Marin-Vicente C., and Gomez-Fernandez J.C. The C2 domains of classical/conventional PKCs are specific PtdIns(4,5)P(2)-sensing domains. Biochem. Soc. Trans. 35 (2007) 1046-1048
52. Corbalan-Garcia S., Sanchez-Carrillo S., Garcia-Garcia J., and Gomez-Fernandez J.C. Characterization of the membrane binding mode of the C2 domain of PKC epsilon. Biochemistry 42 (2003) 11661-11668
53. Jose Lopez-Andreo M., Gomez-Fernandez J.C., and Corbalan-Garcia S. The simultaneous production of phosphatidic acid and diacylglycerol is essential for the translocation of protein kinase Cepsilon to the plasma membrane in RBL-2H3 cells. Mol. Biol. Cell 14 (2003) 4885-4895
54. Parry M.J., Alakoskela J.M., Khandelia H., Kumar S.A., Jaattela M., Mahalka A.K., and Kinnunen P.K. High-affinity small molecule-phospholipid complex formation: binding of siramesine to phosphatidic acid. J. Am. Chem. Soc. 130 (2008) 12953-12960
55. Ostenfeld M.S., Fehrenbacher N., Hoyer-Hansen M., Thomsen C., Farkas T., and Jaattela M. Effective tumor cell death by sigma-2 receptor ligand siramesine involves lysosomal leakage and oxidative stress. Cancer Res. 65 (2005) 8975-8983
56. Soby K.K., Mikkelsen J.D., Meier E., and Thomsen C. Lu 28-179 labels a sigma(2)-site in rat and human brain. Neuropharmacology 43 (2002) 95-100
57. Jones J.A., Rawles R., and Hannun Y.A. Identification of a novel phosphatidic acid binding domain in protein phosphatase-1. Biochemistry 44 (2005) 13235-13245
58. Burger K.N., Demel R.A., Schmid S.L., and de Kruijff B. Dynamin is membrane-active: lipid insertion is induced by phosphoinositides and phosphatidic acid. Biochemistry 39 (2000) 12485-12493
59. Kooijman E.E., Chupin V., de Kruijff B., and Burger K.N.J. Modulation of membrane curvature by phosphatidic acid and lysophosphatidic acid. Traffic 4 (2003) 162-174
60. Mouritsen O.G. Life as a Matter of Fat (2005)
61. van den Brink-van der Laan E., Killian J.A., and de Kruijff B. Nonbilayer lipids affect peripheral and integral membrane proteins via changes in the lateral pressure profile. Biochim. Biophys. Acta 1666 (2004) 275-288
62. Ghosh S., Moore S., Bell R.M., and Dush M. Functional analysis of a phosphatidic acid binding domain in human Raf-1 kinase: mutations in the phosphatidate binding domain lead to tail and trunk abnormalities in developing zebrafish embryos. J. Biol. Chem. 278 (2003) 45690-45696
63. Ghosh S., Strum J.C., Sciorra V.A., Daniel L., and Bell R.M. Raf-1 kinase possesses distinct binding domains for phosphatidylserine and phosphatidic acid. Phosphatidic acid regulates the translocation of Raf-1 in 12-O-tetradecanoylphorbol-13-acetate-stimulated Madin-Darby canine kidney cells. J. Biol. Chem. 271 (1996) 8472-8480
64. Rizzo M.A., Shome K., Watkins S.C., and Romero G. The recruitment of Raf-1 to membranes is mediated by direct interaction with phosphatidic acid and is independent of association with Ras. J. Biol. Chem. 275 (2000) 23911-23918
65. Testerink C., Larsen P.B., van der Does D., van Himbergen J.A., and Munnik T. Phosphatidic acid binds to and inhibits the activity of Arabidopsis CTR1. J. Exp. Bot. 58 (2007) 3905-3914
66. Chen Y.F., Etheridge N., and Schaller G.E. Ethylene signal transduction. Ann. Bot. (Lond). 95 (2005) 901-915
67. Guo H., and Ecker J.R. The ethylene signaling pathway: new insights. Curr. Opin. Plant Biol. 7 (2004) 40-49
68. Kieber J.J., Rothenberg M., Roman G., Feldmann K.A., and Ecker J.R. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72 (1993) 427-441
69. Redfern R.E., Redfern D., Furgason M.L., Munson M., Ross A.H., and Gericke A. PTEN phosphatase selectively binds phosphoinositides and undergoes structural changes. Biochemistry 47 (2008) 2162-2171
70. Epand R.F., Sayer B.G., and Epand R.M. Induction of raft-like domains by a myristoylated NAP-22 peptide and its Tyr mutant. FEBS J. 272 (2005) 1792-1803
71. Epand R.M. Proteins and cholesterol-rich domains. Biochim. Biophys. Acta 1778 (2008) 1576-1582