- Email: [email protected]
Lipids protein-lipid interactions on the surfaces of cell membranes
425
Lipids Protein-lipid
interactions
on the surfaces of cell membranes
Editorial overview John A Glomset Addresses Howard Hughes MedIcal Institute, Departments Biochemistry, and Regional Primate Research Washington, Seattle, WA 98195, USA; e-mail: [email protected]
of MedIcme and Center, University
Current
9:425-427
c
Opinion
Elsevler
in Structural
Science
Ltd ISSN
Abbreviations Gia y-carboxyglutamate interfacial btnding i-face
‘I’he three
1999,
0959-440X
surface
relate to the peripheral cells. ‘I‘hesc proteina arc’ the focus of an important. emerging field in structural biology It’s already clear that they are quite diverse and include cytoskeletal proteins [ I]. the coat proteins ofsecrctory :ind cndocytic \esiclcs [2]. protein kinases [.;I. (;‘I’l’-l)inding proteins [a] and rhc cnzymcs and lipid transport proteins that contribiitc to lipid-dependent ccl1 c\idcnce is xuimulatin~ signaling [Lb]. l;urthermore. that they bind to the lipids of cell n~cn~I~~ncs by diffcrcnt mechanisms. I:or exfmple, some of the proteins con&n pleckstrin ho~nology domains that bintl phosI’t”)inositid~~ [ 71, others contain CL domains that binci mcmbmne lipiclx in thu presence of (:a’+ [Xl. others contain positi\,cl! char,& regions chat bind to ncgati\,ely chargctl phosphoglycerides [9] and others contain covalently attached f:ltt) ac) I ,group\ or prenyl groups th3t anchor them to mcmbranca [l,lO]. Ikynd this, adjdccnt mcmhrdnc lipids that tlo not bind proteins directly ma)’ nioilulatc the protein-lipid interactions [ 11 1. the binciing of proteins to membrane surfaces ma) promcw ftlrther changes in the structure and fLlncti(Jn of the proteins [12] and groups of protcins that bind to the wnc membrane surface ina!interact with each other to cffcct complex mcmbr;Inc response\ (e.g. [ 131). membrane
reviews
Biology
of
proteins
in this section of
mammalian
In \.ic\\- of this complexity SC\ eraI key questions have to considered for each protein-lipid interaction. What region of the protein is involved in membrane binding and what specific amino acids in the region form the intcrfaciul binciing sllrface (i-face)? kl:hich membrane lipids interact with the amino acids and what types of intermolecular contacts arc in\ olved? I>oes the targetinK of the protein to a membrane deptznd solely on these lipici\ or tloes it also depend on 311 interactjon n-it11 ;i niombrane protein? IIoes protein-lipid binding h:ivc additional structural cffccts on the protein or on ddj;tcent membrane lipids and proteins? Ho\{ drc the pl-ntein’s lx
interactions with membrane lipids and proteins regulated? ‘1 i) answer questions like these for even a single, peripheral membrane protein u~~uld be a major task, so the challenge for the field ;1s a whole is clear. ‘l’hr rc\iew by Cklb, (:ho and Wilton (pp 328-332) summarizes initial attempts to address this challenge for secreted members of the phospholipase A, cnzync sllpcrfamily. In particular, the authors focus on the i-faces of these enzymes, which are of special interest because of the corrcl~tion between different amino acid compositions and differcnccs in the cnzynes ability to interact with mocJcI lipid surfaces. l;or example, the i-fact of ;I sccrctcd phospholipasc 11, from the pancreas contains several basic amino acids that interact elcctrostaticall\~ \vith model lipid surfaces that contain negatively charged p~~r~sl~llo~lyccrides. Similar interactions may bc of functiondl importance i,v S+CYI. hccause the enzyme norm;llly catalyzes the hydrolysis of ingcstecl phosphogl!,cerid~s that arc present in mixed micclles and emulsions that also contain conjugated bile acid\. other phospholipvse A, cnLymes secreted b); mammali:m cells are thought to bind to cell plasma mcmbrancs during inflamniatoq responses.
426
Lipids
‘I’he three groups of proteins that are discussed in the re\.iew by Nelsestuen and Ostrowski (pp 433437) alSo show (:a’+-dependent binding to lipid surfaces, but by different mechanisms and with a considerably higher (:a?+ stoichiometrv. The pentraxins are extracellular proteins that, like some CJfthe secreted phospholipase .A? enzymes, responses are thought to contribute to inflammatory (73~2.51. (:a-‘+ ions bind to the fjvc subunits of‘ each pentrasin molecule and this can promote protein-lipid interactions with negatively charged model membranes [Zh-D]. Nelsestuen and Ostrowski make the point that pentraxins that have positively charged, (:a?+-containing i-faces bind to these membranes, whercas corresponding pentraxins that have negatively charged i-faces do not. ‘I-his obscr\,ation may bc of biological relevance becatlse
attachment of the coagulation factors to lipid surfaces. Nelsestuen and Ostrowski suggest that these attachments may depend on yet-to-be characterized, site-specific mechanisms involving one or more phosphoglyceride head ,qroups, rather than on nonspecific electrostatic or hydrophobic interactions.
‘I’hc studies reviewed by (;rlb, (Iho and LVilton, and by Nelsestuen and Ostrowski provide evidence that the i-faces of peripheral membrane proteins arc heterogeneous and contain a great deal of detailed, structurally important information. ‘l’he full significance of this information ma) not become clear until the corresponding membrane lipid interfaces that contribute to protein-lipid interactions arc better understood. ‘I’he lipid bilqers of mammalian cell the OlltCr SUrfxcS (Jf d~mi~~?d CCllS tiild xtivated pl:ltcktS membranes are also heterogeneous and structurally comare thought to contain relatively high amounts of pho+ plex; however. most investigations of the lipids that phatidylscrine. On chc other hand, human plasma interact with peripheral membrane proteins have been Cl-reacti\yc prowin, a pelltrasin that dots not show (:a’*done using rclativcly simple lipid systems that have a limtlcpendent binding to negati\.ely charged model ited porcntial for providing detailed structural information. membranes, reportedly show\ (IaL+-dependent bindinK ‘I’herefore. work with more informati\,c lipid systems is both to model membranes that cctntain high amounts of needed. ‘I’he review by Hrockman (pp 4.38-43.3) provides I~sophosphatid~lcholine [.?0,.31] and to cells that 113~~~ an indication of the t)pe of information that will be been damaged 1,). treutmcnt 11ith snake \cnom phospholirequired. It shows how careful eupcrimentation with lipid p;~sc A, [.31..32]. ‘I’hc basis for these effects remains to bc monolayers can be used t0 obtain imporunt insights about dutermined, but hum3n (:-rcacti\rc protcin is kn0w.n to the molecular role of lipids in protein-lipid interactions. contain ;I (:a’+-dependent binding site for the polar head x:roltp of phosphatitiylcholinc [ZH,?)] and it has been specReferences trlated that this binding site may bc invA.ed [25(.
In contrast to pcntraxins, annexins show (:a’+-dependent binding to the cytosolic surfaces of cell membranes I.3.3). ( L-I h ions bind to rhe i-face of each annexin [?A] and I\jelsestucn and Ostrowaki argue that this may promote protcin-lipid interactions through a combination of electrostatic and hydrophobic mechanisms. [ndced. crl;stsllographic studies with phosphoglyccridc analogs ha\c suggested that some of the bound (:a’+ ions may bind directly to the ox)gens of phospholipid head groups ].3S]. In addition, (:a?+ binding to anncxin V causes a buried tryptophan residue (‘IiylXS) to become csposed on the surface of the i-face (.3h..ii] and the replacement of this tryptophan with an alaninc residue has hecn shown to dccrcase the affinity of annexin \T for model membranes [.1X]. Interestingly, studies of mutated forms of anncxin I ha1.c prov-ided evidence that individual domains of anncxins, though structurall!. homologous. may haw distinct functions in lipid-vesicle binding and aggregation [.iU], If similar studies of other anncsinc stlpport this possibilit!; str~rctlirc/functioii studies invol\,ing mutations in rhe domains that promote protein-lipid interactions most effccti\~elv might be \w); informati\.c. ~‘itamin-k;-dependent plasma proteins bind to the extracellular surfaces of cells in response to injury and contribute to the control of blood clotting reactions [#)]. ‘l‘hc?; contain Gla (y-carhos~glutanl~lte) residues at their N termini that bind (:a?+ and promote the functional
1.
lsenberg membrane
G, Nlggll lipids.
V: Interaction Int Rev Cyfol
2.
Kobayashl T, Gu F, Gruenberg J: Lipids, lipid protein interactions in endocytic membrane 1998, 9:517-526.
3.
Mellor H. Parker PJ: The extended Bmchem J 1998, 332:281-292.
4.
Glomset JA, Farnsworth CC: Role of protein modification reactions in programming interactions between ras-related GTPases and cell membranes. Annu Rev Cell Viol 1994, lo:1 81-205.
5.
Leslie J Biol
6.
Cockcroft in signal 432.
S: Phosphatidylinositol transduction and
7.
Rebecchl fold with 27:503-528.
MJ, Scarlata S: Pleckstrin diverse functions. Annu
8.
RIZO J, Sudhof TC: CZ-domains, universal Ca2+-binding domain. 15882.
9.
Murray D, Ben-Tal N, Honig B, McLaughltn S: Electrostatic interaction of myristoylated proteins with membranes: physics, complicated biology. Cell 1997, 80:929-938.
C: Properties Chem 1997,
of cytoskeletal 1998, 178:73-l
protein
proteins 25.
domains traffic. kinase
transfer traffic.
and lipidCell Dev Bioi C superfamily.
and regulation of cytosolic 27:16709-l 6712. vesicle
phospholipase
proteins: Bioessays
homology Rev Siophys
with
A,.
a requirement 1998, 20:423-
domains: Bomol
a common Sfrucf 1998,
structure and function of a J Bioi Chem 1998, 273:15879-
palmitoylation 9:146-l 54.
IO
Mumby SM: Reversible opin Ceil B/O/ 1997,
11.
Thomas WE, Glomset JA: Multiple factors a soluble, Ca2+-independent diacylglycerol phosphoglyceride vesicles. Biochemistry
influence the binding of kinase to unilamellar 1999, 38:331 O-331 9.
12.
Newton AC: Regulation 1997, 9:161-167.
C. Curr
13.
Frank SR, Hatfield JC. Casanova JE: Remodeling cytoskeleton is coordinately regulated by protein the ADP-ribosylation factor nucleotide exchange MO/ Biol 1998, 9:3133-3146.
of protein
of signaling
simple
kinase
proteins.
Curr
Opin
Cell
of the
actin
kinase factor
Biol
C and ARNO.
Editorial
14.
Han SK, Kim KP, Koduri R, Bittova L, Munoz NM, Leff AR, Wilton DC, Gelb MH, Cho W: Roles of Trp in high membrane binding and proinflammatory activity of human group V phospholipase. J Biol Chem 1999,274:11881-l 1888.
15.
Scott D, Sigler phospholipases
16.
Yu BZ, Rogers J, Nlcol GR, Theopold KH, Seshadri K, Vishweshwara S, Jain MK: Catalytic significance of the specificity of divalent cations as K, and k,, cofactors for secreted phospholipase A2. Brochemistry 1998, 37:12576-l 2587.
PB: Structure and catalytic mechanism A,. Adv Protein Chem 1994, 45:53-88.
28.
Shrive AK, Cheetham GMT, Holden D, Myles DA, Turnell WG, Volanakls JE, Pepys MB, Blommer AC, Greenhough TJ: Three dimensional structure of human C-reactive protein. Nat Sbuct 1996, 3:346-354.
of secretory
N, White HE, Emsley J, Wood SP, Pepys MB, Blundell analyses of pentraxins: implications for protomer and ligand binding. Structure 1994, 2:1017-l 027.
29.
Thompson D, Pepys MB, Wood human C-reactive protein and Structure 1999, 7:169-l 77.
30.
Li VP, Mold C, DuClos TW: C-reactive protein binding 1994, 152:2995-3005.
18.
Penstc
31.
Volanakls artificial
32.
Narkates AJ, Volanakis artificial and natural 1982, 389:172-l 82.
33.
Gerke V, Moss SE: Annexins Biophys Acta 1997,1357:129-i
cytosolic 19.
20.
21.
22.
Pensic 0, Paterson HF, Mosedale Mapping the phosphoiipid-binding determinants of the C2 domain J Biol Chem 1999,274:14979-l
M, Williams RL: Crystal binding domain from Chem 1998, 3:1596-l 604.
G, Lara-Gonzalez S, Williams surface and translocation from cytosolic phospholipase 4987.
Nalefski EA, McDonagh T, Somers W, Seehra Independent folding and ligand specificity dependent lipid binding domain of cytosolic J Do/ Chem 1998, 273:1365-l 372.
J, Falkes JJ, Clark of the C2 calciumphospholipase
RL:
JE, Wirtz KWA: phosphatidylcholine
of
Subly-tic complement attack exposes sites on cell membranes. J lmmunol Interaction of C-reactive protein with bilayers. Nature 1979, 281 :I 55-157.
JE: C-reactive phospholipid
protein bilayers.
binding specificities: Ann N Y Acad Sci
JD:
membrane
dynamics.
Bochfm
54.
35.
Davletov B, Perisic 0, Willlams RL: Calcium-dependent membrane penetration is a hallmark of the C2 domain of cytosolic phospholipase A2 whereas the C2A domain of synaptotagmin binds membranes electrostatically. J Biol Chem 1998,273:19093-l 9096.
Swairjo MA, Concha bridging mechanism the membrane-binding 2:968-974.
36.
Bittova L, Sumandea M, Cho W: A structure-function study of the C2 domain of cytosolic phospholipase A,. J B/o/ Chem 1999, 274:9665-9672.
Concha annexin changes.
37.
Sopkova J, Renouard a new high-calcium 234:816-825.
38.
Campos B, MO YD, Mealy TR. LI CW, Swalrjo MA, Balch C, Head Retzinger G, Dedman JR, Seaton BA: Mutational and crystallographic analyses of interfacial residues in annex V suggest direct interactions with phospholipid membrane components. Biochemistry 1998, 37:8004-8010.
39.
Bitto E. Cho W: Roles of individual domains of annexin I in its vesicle binding and vesicle aggregation: a comprehensive mutagenesis study. Biochemistry 1998, 37:10231-l 0237.
40.
Zwaal blood
A,.
Gewurz H, Zhang pentraxins. Curr
of the
24.
Gabay C, Kushner I: Acute-phase proteins responses to inflammation. N E/,g/ J Med
25.
Hack CE, Wolbink GJ, Schalkwljk C, Speijer H, Hermens WT, van den Bosch H: A role for secretory phospholipase A, and C-reactive protein in the removal of injured cells. Immunol Today 1997. 18:111-115.
and other systemic 1999, 340:448-454.
Emsley JW, White HE, O’Hara BP, Snnivasan OG, Tickel IJ. Blundell TL. Pepys MB, Wood SP: Structure of pentameric human serum amyloid P component. Nature 1994, 367338.345.
BA, Dedman
and
Seaton
and function 7:54-64.
B/o/
SP: The physiological structure its complex with phosphocholine.
34.
XH, Lmt TF: Structure Opin Immunol 1995,
TL:
A,
23.
26.
427
Srimvasan Comparative assembly
Sutton RB, Davletov BA, Berghuis AM, Sudhof TC, Sprang SR: Structure of the first Cz domain of synaptotagmin I: a novel Ca*+/phospholipid-binding fold. Cell 1995,80:929-938. 0, Fong S, Lynch DE, Bycroft of a calcium-phospholipid phospholipase A,. J Brol
Glomset
27.
17.
structure
overview
JR: Annexins.
Biometals
1998,
11:399-404.
NO, Kaetzel MA, Dedman JR, Seaton BA: Ca*+and phosphoiipid head group recognition in protein annexin V. Nat Struct 610l 1995,
NO, Head JF, Kaetzel V crystal structure: Science 1993,261
MA, Dedman Ca(2+)-induced :132 l-1 324.
M, Lewlt-Bentley form of annexin
JR, Seaton BA: conformational
Rat
A: The crystal structure V. J MO/ Bol 1993.
RFA, Comfurius P, Bevers EM: Lipid-protein coagulation. Biochim Siophys Acta 1996,
interactions 1376:433-453.
of
JF,
in
Lipids Protein-lipid
interactions
on the surfaces of cell membranes
Editorial overview John A Glomset Addresses Howard Hughes MedIcal Institute, Departments Biochemistry, and Regional Primate Research Washington, Seattle, WA 98195, USA; e-mail: [email protected]
of MedIcme and Center, University
Current
9:425-427
c
Opinion
Elsevler
in Structural
Science
Ltd ISSN
Abbreviations Gia y-carboxyglutamate interfacial btnding i-face
‘I’he three
1999,
0959-440X
surface
relate to the peripheral cells. ‘I‘hesc proteina arc’ the focus of an important. emerging field in structural biology It’s already clear that they are quite diverse and include cytoskeletal proteins [ I]. the coat proteins ofsecrctory :ind cndocytic \esiclcs [2]. protein kinases [.;I. (;‘I’l’-l)inding proteins [a] and rhc cnzymcs and lipid transport proteins that contribiitc to lipid-dependent ccl1 c\idcnce is xuimulatin~ signaling [Lb]. l;urthermore. that they bind to the lipids of cell n~cn~I~~ncs by diffcrcnt mechanisms. I:or exfmple, some of the proteins con&n pleckstrin ho~nology domains that bintl phosI’t”)inositid~~ [ 71, others contain CL domains that binci mcmbmne lipiclx in thu presence of (:a’+ [Xl. others contain positi\,cl! char,& regions chat bind to ncgati\,ely chargctl phosphoglycerides [9] and others contain covalently attached f:ltt) ac) I ,group\ or prenyl groups th3t anchor them to mcmbranca [l,lO]. Ikynd this, adjdccnt mcmhrdnc lipids that tlo not bind proteins directly ma)’ nioilulatc the protein-lipid interactions [ 11 1. the binciing of proteins to membrane surfaces ma) promcw ftlrther changes in the structure and fLlncti(Jn of the proteins [12] and groups of protcins that bind to the wnc membrane surface ina!interact with each other to cffcct complex mcmbr;Inc response\ (e.g. [ 131). membrane
reviews
Biology
of
proteins
in this section of
mammalian
In \.ic\\- of this complexity SC\ eraI key questions have to considered for each protein-lipid interaction. What region of the protein is involved in membrane binding and what specific amino acids in the region form the intcrfaciul binciing sllrface (i-face)? kl:hich membrane lipids interact with the amino acids and what types of intermolecular contacts arc in\ olved? I>oes the targetinK of the protein to a membrane deptznd solely on these lipici\ or tloes it also depend on 311 interactjon n-it11 ;i niombrane protein? IIoes protein-lipid binding h:ivc additional structural cffccts on the protein or on ddj;tcent membrane lipids and proteins? Ho\{ drc the pl-ntein’s lx
interactions with membrane lipids and proteins regulated? ‘1 i) answer questions like these for even a single, peripheral membrane protein u~~uld be a major task, so the challenge for the field ;1s a whole is clear. ‘l’hr rc\iew by Cklb, (:ho and Wilton (pp 328-332) summarizes initial attempts to address this challenge for secreted members of the phospholipase A, cnzync sllpcrfamily. In particular, the authors focus on the i-faces of these enzymes, which are of special interest because of the corrcl~tion between different amino acid compositions and differcnccs in the cnzynes ability to interact with mocJcI lipid surfaces. l;or example, the i-fact of ;I sccrctcd phospholipasc 11, from the pancreas contains several basic amino acids that interact elcctrostaticall\~ \vith model lipid surfaces that contain negatively charged p~~r~sl~llo~lyccrides. Similar interactions may bc of functiondl importance i,v S+CYI. hccause the enzyme norm;llly catalyzes the hydrolysis of ingcstecl phosphogl!,cerid~s that arc present in mixed micclles and emulsions that also contain conjugated bile acid\. other phospholipvse A, cnLymes secreted b); mammali:m cells are thought to bind to cell plasma mcmbrancs during inflamniatoq responses.
426
Lipids
‘I’he three groups of proteins that are discussed in the re\.iew by Nelsestuen and Ostrowski (pp 433437) alSo show (:a’+-dependent binding to lipid surfaces, but by different mechanisms and with a considerably higher (:a?+ stoichiometrv. The pentraxins are extracellular proteins that, like some CJfthe secreted phospholipase .A? enzymes, responses are thought to contribute to inflammatory (73~2.51. (:a-‘+ ions bind to the fjvc subunits of‘ each pentrasin molecule and this can promote protein-lipid interactions with negatively charged model membranes [Zh-D]. Nelsestuen and Ostrowski make the point that pentraxins that have positively charged, (:a?+-containing i-faces bind to these membranes, whercas corresponding pentraxins that have negatively charged i-faces do not. ‘I-his obscr\,ation may bc of biological relevance becatlse
attachment of the coagulation factors to lipid surfaces. Nelsestuen and Ostrowski suggest that these attachments may depend on yet-to-be characterized, site-specific mechanisms involving one or more phosphoglyceride head ,qroups, rather than on nonspecific electrostatic or hydrophobic interactions.
‘I’hc studies reviewed by (;rlb, (Iho and LVilton, and by Nelsestuen and Ostrowski provide evidence that the i-faces of peripheral membrane proteins arc heterogeneous and contain a great deal of detailed, structurally important information. ‘l’he full significance of this information ma) not become clear until the corresponding membrane lipid interfaces that contribute to protein-lipid interactions arc better understood. ‘I’he lipid bilqers of mammalian cell the OlltCr SUrfxcS (Jf d~mi~~?d CCllS tiild xtivated pl:ltcktS membranes are also heterogeneous and structurally comare thought to contain relatively high amounts of pho+ plex; however. most investigations of the lipids that phatidylscrine. On chc other hand, human plasma interact with peripheral membrane proteins have been Cl-reacti\yc prowin, a pelltrasin that dots not show (:a’*done using rclativcly simple lipid systems that have a limtlcpendent binding to negati\.ely charged model ited porcntial for providing detailed structural information. membranes, reportedly show\ (IaL+-dependent bindinK ‘I’herefore. work with more informati\,c lipid systems is both to model membranes that cctntain high amounts of needed. ‘I’he review by Hrockman (pp 4.38-43.3) provides I~sophosphatid~lcholine [.?0,.31] and to cells that 113~~~ an indication of the t)pe of information that will be been damaged 1,). treutmcnt 11ith snake \cnom phospholirequired. It shows how careful eupcrimentation with lipid p;~sc A, [.31..32]. ‘I’hc basis for these effects remains to bc monolayers can be used t0 obtain imporunt insights about dutermined, but hum3n (:-rcacti\rc protcin is kn0w.n to the molecular role of lipids in protein-lipid interactions. contain ;I (:a’+-dependent binding site for the polar head x:roltp of phosphatitiylcholinc [ZH,?)] and it has been specReferences trlated that this binding site may bc invA.ed [25(.
In contrast to pcntraxins, annexins show (:a’+-dependent binding to the cytosolic surfaces of cell membranes I.3.3). ( L-I h ions bind to rhe i-face of each annexin [?A] and I\jelsestucn and Ostrowaki argue that this may promote protcin-lipid interactions through a combination of electrostatic and hydrophobic mechanisms. [ndced. crl;stsllographic studies with phosphoglyccridc analogs ha\c suggested that some of the bound (:a’+ ions may bind directly to the ox)gens of phospholipid head groups ].3S]. In addition, (:a?+ binding to anncxin V causes a buried tryptophan residue (‘IiylXS) to become csposed on the surface of the i-face (.3h..ii] and the replacement of this tryptophan with an alaninc residue has hecn shown to dccrcase the affinity of annexin \T for model membranes [.1X]. Interestingly, studies of mutated forms of anncxin I ha1.c prov-ided evidence that individual domains of anncxins, though structurall!. homologous. may haw distinct functions in lipid-vesicle binding and aggregation [.iU], If similar studies of other anncsinc stlpport this possibilit!; str~rctlirc/functioii studies invol\,ing mutations in rhe domains that promote protein-lipid interactions most effccti\~elv might be \w); informati\.c. ~‘itamin-k;-dependent plasma proteins bind to the extracellular surfaces of cells in response to injury and contribute to the control of blood clotting reactions [#)]. ‘l‘hc?; contain Gla (y-carhos~glutanl~lte) residues at their N termini that bind (:a?+ and promote the functional
1.
lsenberg membrane
G, Nlggll lipids.
V: Interaction Int Rev Cyfol
2.
Kobayashl T, Gu F, Gruenberg J: Lipids, lipid protein interactions in endocytic membrane 1998, 9:517-526.
3.
Mellor H. Parker PJ: The extended Bmchem J 1998, 332:281-292.
4.
Glomset JA, Farnsworth CC: Role of protein modification reactions in programming interactions between ras-related GTPases and cell membranes. Annu Rev Cell Viol 1994, lo:1 81-205.
5.
Leslie J Biol
6.
Cockcroft in signal 432.
S: Phosphatidylinositol transduction and
7.
Rebecchl fold with 27:503-528.
MJ, Scarlata S: Pleckstrin diverse functions. Annu
8.
RIZO J, Sudhof TC: CZ-domains, universal Ca2+-binding domain. 15882.
9.
Murray D, Ben-Tal N, Honig B, McLaughltn S: Electrostatic interaction of myristoylated proteins with membranes: physics, complicated biology. Cell 1997, 80:929-938.
C: Properties Chem 1997,
of cytoskeletal 1998, 178:73-l
protein
proteins 25.
domains traffic. kinase
transfer traffic.
and lipidCell Dev Bioi C superfamily.
and regulation of cytosolic 27:16709-l 6712. vesicle
phospholipase
proteins: Bioessays
homology Rev Siophys
with
A,.
a requirement 1998, 20:423-
domains: Bomol
a common Sfrucf 1998,
structure and function of a J Bioi Chem 1998, 273:15879-
palmitoylation 9:146-l 54.
IO
Mumby SM: Reversible opin Ceil B/O/ 1997,
11.
Thomas WE, Glomset JA: Multiple factors a soluble, Ca2+-independent diacylglycerol phosphoglyceride vesicles. Biochemistry
influence the binding of kinase to unilamellar 1999, 38:331 O-331 9.
12.
Newton AC: Regulation 1997, 9:161-167.
C. Curr
13.
Frank SR, Hatfield JC. Casanova JE: Remodeling cytoskeleton is coordinately regulated by protein the ADP-ribosylation factor nucleotide exchange MO/ Biol 1998, 9:3133-3146.
of protein
of signaling
simple
kinase
proteins.
Curr
Opin
Cell
of the
actin
kinase factor
Biol
C and ARNO.
Editorial
14.
Han SK, Kim KP, Koduri R, Bittova L, Munoz NM, Leff AR, Wilton DC, Gelb MH, Cho W: Roles of Trp in high membrane binding and proinflammatory activity of human group V phospholipase. J Biol Chem 1999,274:11881-l 1888.
15.
Scott D, Sigler phospholipases
16.
Yu BZ, Rogers J, Nlcol GR, Theopold KH, Seshadri K, Vishweshwara S, Jain MK: Catalytic significance of the specificity of divalent cations as K, and k,, cofactors for secreted phospholipase A2. Brochemistry 1998, 37:12576-l 2587.
PB: Structure and catalytic mechanism A,. Adv Protein Chem 1994, 45:53-88.
28.
Shrive AK, Cheetham GMT, Holden D, Myles DA, Turnell WG, Volanakls JE, Pepys MB, Blommer AC, Greenhough TJ: Three dimensional structure of human C-reactive protein. Nat Sbuct 1996, 3:346-354.
of secretory
N, White HE, Emsley J, Wood SP, Pepys MB, Blundell analyses of pentraxins: implications for protomer and ligand binding. Structure 1994, 2:1017-l 027.
29.
Thompson D, Pepys MB, Wood human C-reactive protein and Structure 1999, 7:169-l 77.
30.
Li VP, Mold C, DuClos TW: C-reactive protein binding 1994, 152:2995-3005.
18.
Penstc
31.
Volanakls artificial
32.
Narkates AJ, Volanakis artificial and natural 1982, 389:172-l 82.
33.
Gerke V, Moss SE: Annexins Biophys Acta 1997,1357:129-i
cytosolic 19.
20.
21.
22.
Pensic 0, Paterson HF, Mosedale Mapping the phosphoiipid-binding determinants of the C2 domain J Biol Chem 1999,274:14979-l
M, Williams RL: Crystal binding domain from Chem 1998, 3:1596-l 604.
G, Lara-Gonzalez S, Williams surface and translocation from cytosolic phospholipase 4987.
Nalefski EA, McDonagh T, Somers W, Seehra Independent folding and ligand specificity dependent lipid binding domain of cytosolic J Do/ Chem 1998, 273:1365-l 372.
J, Falkes JJ, Clark of the C2 calciumphospholipase
RL:
JE, Wirtz KWA: phosphatidylcholine
of
Subly-tic complement attack exposes sites on cell membranes. J lmmunol Interaction of C-reactive protein with bilayers. Nature 1979, 281 :I 55-157.
JE: C-reactive phospholipid
protein bilayers.
binding specificities: Ann N Y Acad Sci
JD:
membrane
dynamics.
Bochfm
54.
35.
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