Abstract
PH-PLCdelta1 [the PH domain (pleckstrin homology domain) of PLCdelta1 (phospholipase C-delta1)] is among the best-characterized phosphoinositide-binding domains. PH-PLCdelta1 binds with high specificity to the headgroup of PtdIns(4,5)P2, but little is known about its interfacial properties. In the present study, we show that PH-PLCdelta1 is also membrane-active and can insert significantly into PtdIns(4,5)P2-containing monolayers at physiological (bilayer-equivalent) surface pressures. However, this membrane activity appears to involve interactions distinct from those that target PH-PLCdelta1 to the PtdIns(4,5)P2 headgroup. Whereas the majority of PtdIns(4,5)P2-bound PH-PLCdelta1 can be displaced by adding excess of soluble headgroup [Ins(1,4,5)P3], membrane activity of PH-PLCdelta1 cannot. PH-PLCdelta1 differs from other phosphoinositide-binding domains in that its membrane insertion does not require that the phosphoinositide-binding site be occupied. Significant monolayer insertion remains when the phosphoinositide-binding site is mutated, and PH-PLCdelta1 can insert into monolayers that contain no PtdIns(4,5)P2 at all. Our results suggest a model in which reversible membrane binding of PH-PLCdelta1, mediated by PtdIns(4,5)P2 or other acidic phospholipids, occurs without membrane insertion. Accumulation of the PH domain at the membrane surface enhances the efficiency of insertion, but does not significantly affect its extent, whereas the presence of phosphatidylethanolamine and cholesterol in the lipid mixture promotes the extent of insertion. This is the first report of membrane activity in an isolated PH domain and has implications for understanding the membrane targeting by this common type of domain.
MeSH Terms
Animals
Binding Sites
Cattle
Cell Membrane/chemistry,metabolism
Isoenzymes/chemistry,metabolism
Phosphatidylcholines/metabolism
Phosphatidylinositol 4,5-Diphosphate/metabolism
Phosphatidylinositol Phosphates/metabolism
Phosphatidylserines/metabolism
Phospholipase C delta
Protein Binding
Protein Structure, Tertiary
Rats
Substrate Specificity
Type C Phospholipases/chemistry,metabolism
Chemicals
Isoenzymes
Phosphatidylcholines
Phosphatidylinositol 4,5-Diphosphate
Phosphatidylinositol Phosphates
Phosphatidylserines
phosphatidylinositol 4-phosphate
Type C Phospholipases
Phospholipase C delta
Plcd1 protein, rat
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Flesch Frits M
Department of Molecular Cell Biology, Faculty of Biology, Institute of Biomembranes, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands.
Yu Jong W
Lemmon Mark A
Burger Koert N J
References (35)
35 references, click to expand
-
Membrane binding mechanisms of the PX domains of NADPH oxidase p40phox and p47phox.
J Biol Chem. 2003 Apr 18;278(16):14469-79
PMID: 12556460
-
Nonbilayer lipids affect peripheral and integral membrane proteins via changes in the lateral pressure profile.
Biochim Biophys Acta. 2004 Nov 3;1666(1-2):275-88
PMID: 15519321
-
Structure and dynamics of the phospholipase C-delta1 pleckstrin homology domain located at the lipid bilayer surface.
J Biol Chem. 2003 Jul 25;278(30):28019-25
PMID: 12736268
-
Contrasting membrane interaction mechanisms of AP180 N-terminal homology (ANTH) and epsin N-terminal homology (ENTH) domains.
J Biol Chem. 2003 Aug 1;278(31):28993-9
PMID: 12740367
-
Molecular modeling of the membrane targeting of phospholipase C pleckstrin homology domains.
Protein Sci. 2003 Sep;12(9):1934-53
PMID: 12930993
-
Sensing membrane curvature.
Dev Cell. 2003 Dec;5(6):821-2
PMID: 14667402
-
Membrane recognition and targeting by lipid-binding domains.
Sci STKE. 2003 Dec 16;2003(213):re16
PMID: 14679290
-
Multivalent mechanism of membrane insertion by the FYVE domain.
J Biol Chem. 2004 Jan 23;279(4):3050-7
PMID: 14578346
-
Genome-wide analysis of membrane targeting by S. cerevisiae pleckstrin homology domains.
Mol Cell. 2004 Mar 12;13(5):677-88
PMID: 15023338
-
Phosphoinositide-specific phospholipase C-delta 1: effect of monolayer surface pressure and electrostatic surface potentials on activity.
Biochemistry. 1992 Dec 29;31(51):12748-53
PMID: 1334430
-
Monomolecular layers in the study of biomembranes.
Subcell Biochem. 1994;23:83-120
PMID: 7855881
-
Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain.
Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10472-6
PMID: 7479822
-
The pleckstrin homology domain of phospholipase C-delta 1 binds with high affinity to phosphatidylinositol 4,5-bisphosphate in bilayer membranes.
Biochemistry. 1995 Dec 12;34(49):16228-34
PMID: 8519781
-
Structure of the high affinity complex of inositol trisphosphate with a phospholipase C pleckstrin homology domain.
Cell. 1995 Dec 15;83(6):1037-46
PMID: 8521504
-
Lateral pressure in membranes.
Biochim Biophys Acta. 1996 Oct 29;1286(3):183-223
PMID: 8982283
-
The pleckstrin homology domain of oxysterol-binding protein recognises a determinant specific to Golgi membranes.
Curr Biol. 1998 Jun 18;8(13):729-39
PMID: 9651677
-
Lipid polymorphism and protein-lipid interactions.
Biochim Biophys Acta. 1998 Nov 10;1376(3):353-68
PMID: 9804988
-
Characterization of the surfaces generated by liposome binding to the modified dextran matrix of a surface plasmon resonance sensor chip.
Anal Biochem. 2000 Apr 10;280(1):29-35
PMID: 10805517
-
How accurately can we image inositol lipids in living cells?
Trends Pharmacol Sci. 2000 Jul;21(7):238-41
PMID: 10871889
-
Signal-dependent membrane targeting by pleckstrin homology (PH) domains.
Biochem J. 2000 Aug 15;350 Pt 1:1-18
PMID: 10926821
-
Dynamin is membrane-active: lipid insertion is induced by phosphoinositides and phosphatidic acid.
Biochemistry. 2000 Oct 10;39(40):12485-93
PMID: 11015230
-
Greasing membrane fusion and fission machineries.
Traffic. 2000 Aug;1(8):605-13
PMID: 11208148
-
Structural mechanism of endosome docking by the FYVE domain.
Science. 2001 Mar 2;291(5509):1793-6
PMID: 11230696
-
Cellular functions of phosphatidylinositol 3-phosphate and FYVE domain proteins.
Biochem J. 2001 Apr 15;355(Pt 2):249-58
PMID: 11284710
-
Phox domain interaction with PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes.
Nat Cell Biol. 2001 Jul;3(7):613-8
PMID: 11433291
-
Regulation of CTP: phosphocholine cytidylyltransferase activity by the physical properties of lipid membranes: an important role for stored curvature strain energy.
Biochemistry. 2001 Sep 4;40(35):10522-31
PMID: 11523994
-
Effect of nonbilayer lipids on membrane binding and insertion of the catalytic domain of leader peptidase.
Biochemistry. 2001 Aug 14;40(32):9677-84
PMID: 11583168
-
All phox homology (PX) domains from Saccharomyces cerevisiae specifically recognize phosphatidylinositol 3-phosphate.
J Biol Chem. 2001 Nov 23;276(47):44179-84
PMID: 11557775
-
Phosphatidylinositol 3-phosphate induces the membrane penetration of the FYVE domains of Vps27p and Hrs.
J Biol Chem. 2002 Jul 19;277(29):26379-88
PMID: 12006563
-
Inositol lipid binding and membrane localization of isolated pleckstrin homology (PH) domains. Studies on the PH domains of phospholipase C delta 1 and p130.
J Biol Chem. 2002 Jul 26;277(30):27412-22
PMID: 12019260
-
Specificity and promiscuity in phosphoinositide binding by pleckstrin homology domains.
J Biol Chem. 1998 Nov 13;273(46):30497-508
PMID: 9804818
-
Phosphatidylinositol-4,5-bisphosphate is required for endocytic coated vesicle formation.
Curr Biol. 1998 Dec 17-31;8(25):1399-402
PMID: 9889104
-
Lipid composition and the lateral pressure profile in bilayers.
Biophys J. 1999 May;76(5):2625-39
PMID: 10233077
-
Spatiotemporal dynamics of inositol 1,4,5-trisphosphate that underlies complex Ca2+ mobilization patterns.
Science. 1999 May 28;284(5419):1527-30
PMID: 10348740
-
Phosphoinositide recognition domains.
Traffic. 2003 Apr;4(4):201-13
PMID: 12694559