lipid metabolism and dynamics during phagocytosis

Lipid metabolism and dynamics during phagocytosisTony Yeung1,2, Barish Ozdamar1, Paul Paroutis1 andSergio Grinstein1,2

Phagocytosis, the engulfment of particles, mediates the

elimination of invading pathogens as well as the clearance of

apoptotic cells. Ingested particles reside within a vacuole or

phagosome, where they are eventually destroyed and

digested. The phagosomal lumen acquires microbicidal and

digestive properties through interaction with various

components of the endocytic pathway, a process known as

maturation. Lipids are known to have numerous roles in

phagosome formation and maturation; recent developments in

the design of lipid-specific probes and in high-resolution

imaging have revealed that lipids, notably phosphoinositides,

are involved in signaling, actin assembly and the recruitment of

molecular motors to sites of ingestion. In addition,

phosphoinositides and other lipids also regulate multiple

membrane budding, fission and fusion events required for

maturation.

Addresses1 Division of Cell Biology, The Hospital for Sick Children,

555 University Avenue, Toronto, M5G 1X8, Canada2 Institute of Medical Sciences, University of Toronto, Toronto,

M5S 1A8, Canada

T Yeung and B Ozdamar contributed equally to this work.

Corresponding author: Grinstein, Sergio ([email protected])

Current Opinion in Cell Biology 2006, 18:429–437

This review comes from a themed issue on

Membranes and organelles

Edited by Pietro de Camilli and Antonella de Matteis

Available online 14th June 2006

0955-0674/$ – see front matter

# 2006 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.ceb.2006.06.006

IntroductionPhagocytosis, the uptake of particles �0.5 mm in dia-

meter, is a central event in innate immunity and in tissue

remodeling. Professional phagocytes, mainly neutrophils

and macrophages, internalize invading microorganisms to

resolve infection and can also engulf apoptotic bodies,

contributing to the clearance of senescent or damaged

cells. Phagocytosis is triggered by surface receptors that

become cross-linked upon binding to cognate molecules

on the surface of the particles, which act as a large

multivalent ligand. Engagement of such receptors, typi-

fied by Fc and complement receptors, initiates a complex

signaling cascade that induces extensive actin and mem-

brane remodeling, driving the extension of pseudopods

and culminating with particle engulfment. Immediately

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after sealing, the phagosome undergoes multiple rounds

of fission and fusion with other organelles, a carefully

choreographed sequence of events collectively known as

‘maturation’ [1,2]. It is becoming increasingly apparent

that lipid-mediated signaling is intimately involved in

both phagosome formation and maturation. This review

will highlight recent advances in our understanding of

lipid metabolism and redistribution during phagocytosis.

Phagosome formationAs is the case for most mammalian cells, the plasma

membrane of phagocytes is rich in cholesterol and sphin-

golipids. Microdomains enriched in these lipids, often

called rafts, have been proposed to play a crucial role in

phagocytosis of IgG-coated particles, which is mediated

by Fcg receptors [3,4]. This class of phagocytic receptors

has been studied in most detail and will be used as a

paradigm hereafter. Fcg-receptors become activated

upon tyrosine phosphorylation of their immunoreceptor

tyrosine-based activation motif (ITAM), a process cata-

lyzed by Src-family kinases. Src-family kinases such as

Lyn, which are acylated by multiple saturated chains,

partition preferentially to cholesterol-rich microdomains

and this association is thought to be required for their

clustering and activation in the vicinity of cross-linked

receptors [5,6]. This notion is based on experiments

where depletion of cellular cholesterol using statins or

b-methyl-cyclodextrin impaired Fc receptor-mediated

signaling and phagocytosis [3,7,8]. However, statins also

affect the prenylation of Rho-family GTPases that are

essential for pseudopod extension, and depletion of cho-

lesterol interferes with processes that are not mediated by

rafts [9]. Moreover, other investigators failed to detect

inhibition of phagocytosis following cholesterol depletion

[10]. It is therefore premature to conclude that cholesterol

and sphingolipid-rich microdomains are involved in pha-

gosome formation.

The role of other lipids in phagosome formation is better

defined. Phosphoinositides have been studied in most

detail by biochemical methods and, more recently, by

fluorescence imaging using genetically encoded biosen-

sors. Chimeric constructs consisting of fluorescent pro-

teins fused to pleckstrin homology (PH) domains that

recognize the headgroups of phosphatidylinositol-4,5-

bisphosphate (PI(4,5)P2) or phosphatidylinositol-3,4,5-tri-sphosphate (PI(3,4,5)P3) have been used to monitor the

dynamics of these lipids in intact cells during particle

ingestion [11,12]. Both of these lipids undergo acute,

exquisitely localized changes during phagosome forma-

tion. PI(4,5)P2,which is constitutively present in the


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430 Membranes and organelles

plasma membrane, becomes transiently and modestly

accumulated in pseudopods of forming phagosomes,

but disappears rapidly thereafter, being undetectable in

the membrane of sealed phagosomes (Figure 1a–c). Sti-

mulation of type I phosphatidylinositol-phosphate-5-

kinase (PIP5KI) is likely to be responsible for the tran-

sient accumulation of PI(4,5)P2. PIP5KI is present at the

phagosomal cup [11,13], where it may be activated by

Arf6 or Rho-family GTPases and/or by lipid mediators

like phosphatidic acid that are generated during particle

ingestion [14,15]. The causes of the subsequent disap-

pearance of PI(4,5)P2 are likely to be more complex. It is

clear that a fraction of the inositide is hydrolyzed by a

phospholipase C, most likely PLCg in Fcg-mediated

phagocytosis [11]. This is suggested by the accompanying

increase in cytosolic [Ca2+], attributed to inositol 3,4,5-

trisphosphate, and by the generation of diacylglycerol at

the cup, which coincides spatially and temporally with the

disappearance of the phosphoinositide (Figure 1d). In

addition, it is conceivable, though not yet demonstrated,

that PI(4,5)P2 may be degraded at sites of phagocytosis by

phosphoinositide 4- and/or 5-phosphatases like those

recently shown to be active during endocytosis [16].

Disappearance of PI(4,5)P2 from nascent phagosomes is

not, however, due solely to its hydrolysis. A fraction of the

phosphoinositide is converted to PI(3,4,5)P3 by class I

phosphatidylinositol 3-kinase (PI3K), which is recruited

and activated by Syk or by adaptor proteins like Gab2

[12,17–19]. Chimeras containing the PH domain of Akt

that preferentially bind 30-polyphosphoinositides

undergo a remarkable accumulation at sites of phagosome

formation and remain briefly associated with nascent

phagosomes (Figure 1f–g) [12,20]. As in the case of

diacylglycerol, the distribution of PI(3,4,5)P3 is confined

to the forming phagosome. It is remarkable how the lipid

species generated de novo during phagocytosis, a rela-

tively slow process lasting minutes, fail to diffuse past the

boundary of the cup. It is tempting to speculate that a

diffusional barrier is formed at the edge of advancing

pseudopods, but other mechanisms should not be

excluded. Localized generation at the base of the cup

and a combination of diffusion and hydrolysis at the edge

of the forming phagosome could equally explain the

observations. Active endocytosis near the tip of the pseu-

dopods could similarly limit the redistribution of the

lipids to the unengaged plasma membrane. Lastly, bind-

ing of lipids to immobile complexes within the cup may

restrict their lateral mobility, a notion indirectly sup-

ported by evidence obtained by measuring the behavior

of lipid-anchored fluorescent proteins after photobleach-

ing (Yeung et al., unpublished).

The accumulation of PI(3,4,5)P3 is not only highly loca-

lized, but is also very brief and hence difficult to capture

by means other than imaging. There is good evidence that

the 5-phosphatase SHIP contributes to PI(3,4,5)P3


hydrolysis: SHIP isoforms are recruited to sites of pha-

gocytosis, ostensibly by association of their SH2 domain

with phosphotyrosines [21,22], and their overexpression

curtails PI(3,4,5)P3 accumulation and phagocytic effi-

ciency [22,23]. Overexpression of the 30-phosphatase

PTEN can similarly depress phagocytosis, but whether

this enzyme is normally present and active at sites of

ingestion is less clear.

The fate of other phospholipids during phagocytosis

remains largely unexplored. Phosphatidylinositol 4-phos-

phate (PI(4)P) not only serves as a substrate for the

synthesis of PI(4,5)P2 by PIP5KI [13], but may also recruit

this kinase to the plasma membrane via its inositide-

specific activation loop [24]. Recently, the PH domain of

Osh2p (the yeast homologue of the oxysterol-binding

protein) has been developed as a probe for PI(4)P [25].

Preliminary experiments using PH-Osh2p chimeras sug-

gest that PI(4)P is metabolized during phagocytosis

(Yeung et al., unpublished). This result is consistent with

its role as a substrate for the stimulated biosynthesis of

PI(4,5)P2 and may also help to explain the dissociation of

PIP5KI from the phagosome following its internalization

[11,13].

What are the functional consequences of localized phos-

phoinositide metabolism during phagocytosis? That ino-

sitides are crucial for successful phagocytosis is best

illustrated by the effects of PI3K inhibitors like wort-

mannin, which can abrogate particle internalization

[26,27]. The picture, however, is complicated by the

size-dependence of the inhibitory effect: wortmannin

obliterates phagocytosis of large particles (e.g. >5 mm),

while particles the size of most bacteria (�1 mm) are

barely affected [26]. This suggests that not all phagocy-

tosis is the same and that generalizations should be

avoided. Nevertheless, it is clear that plasmalemmal

polyphosphoinositides play multiple, complementary

roles in orchestrating phagocytosis, signaling its initiation

and contributing to the cytoskeletal and membrane remo-

deling (Figure 2). The formation of PI(3,4,5)P3 stimulates

the hydrolysis of PI(4,5)P2 by promoting the recruitment,

phosphorylation and activation of PLCg [28]. In addition,

the headgroup of PI(3,4,5)P3 is likely to contribute to the

association of exchange factors that activate Rho-family

GTPases within the phagocytic cup, though this event is

not an absolute requirement to trigger actin polymeriza-

tion, which persists when PI3K is inhibited [1,26]. Dyna-

min II is also recruited to the phagocytic cup along with

amphiphysin II in a PI3K-dependent manner. Their

precise mode of action is unclear, but interference with

either dynamin II or amphiphysin II function was shown

to inhibit phagocytosis [29,30].

In addition to their role in signaling, phosphoinositides are

central to the cytoskeletal rearrangements that underlie

engulfment. PI(4,5)P2 can promote actin polymerization


Lipid metabolism and dynamics during phagocytosis Grinstein et al. 431

Figure 1

Lipid metabolism during phagosome formation. (a) Time course illustrating the changes in the relative abundance of PIP, PI(4,5)P2, PI(3,4,5)P3,

and diacylglycerol (DAG) during phagocytosis. The dashed line indicates preliminary results using the PH domain of Osh2p to probe for the

distribution of PI(4)P. The curves are idealized profiles, not directly derived from experimental data; their height is intended to reflect relative

changes and is not indicative of absolute concentrations. Distribution of (b,c) PI(4,5)P2, (d,e) DAG and (f,g) PI(3,4,5)P3 during (b,d,f) and shortly

(�2–4 min) after (c,e,g) phagosome formation. The lipids were monitored using GFP-tagged chimeras of PH-PLCd, C1-PKCd and PH-AKT,

respectively. Inset in (b) shows the accumulation of PH-PLCd at the phagocytic cup at very early stages of phagocytosis. Asterisks indicate

phagocytic particles.

www.sciencedirect.com Current Opinion in Cell Biology 2006, 18:429–437


Figure 2

Functional consequences of lipid metabolism during phagosome formation. Schematic representation of a forming phagosome induced by

activation of Fcg receptors. PI(4,5)P2 (shown in blue) plays an important role in phagocytosis by mediating actin remodeling through its interaction

with cytoskeletal proteins including the capping protein profilin, WASP family proteins and actin-severing proteins like gelsolin (not shown).

PI(3,4,5)P3 (shown in pink) promotes localized membrane remodeling by recruiting amphiphysin, dynamin and myosin X to the phagocytic cup.

It may also contribute to the activation of Rac1 by recruiting the guanine nucleotide exchange factor Vav, although PI3K-independent activation

of Rac1 has been reported.

in at least three ways: first, by inducing Arp2/3 activation by

WASP; second, by removing capping proteins like profilin

from the ends of actin filaments; and third, by stimulating

gelsolin to sever filaments, thereby generating fast-grow-

ing barbed ends. PI(3,4,5)P3 also contributes directly to the

mechanical events leading to particle intake by recruiting

WAVE [31] and myosin X to forming phagosomes [32]. Of

note, the dissociation of the cytoskeleton from the sealed

phagosome, which is believed to be required for matura-

tion to proceed, coincides with the disappearance of

PI(4,5)P2 from the phagosomal membrane, suggesting that

the inositide plays a role in the termination of actin

assembly. In support of this concept, Scott et al. found


that preventing the loss of PI(4,5)P2 by impairing PLC

caused retention of phagosomal actin [33�]. Conversely,

these authors also found that when inositide hydrolysis

proceeded normally, actin dissociated from the phago-

somes even when constitutively active Rac1 remained

associated with their membrane.

Phosphoinositides, particularly PI(3,4,5)P3, are seemingly

also involved in the membrane remodeling that enables

phagocytic cells to retain near-normal surface area while

engulfing large and/or multiple particles. Fusion of endo-

membranes at sites of phagocytosis is now believed to

mediate the conservation of surface area and to



simultaneously initiate the maturation sequence. Such

fusion seemingly involves products of PI3K, as it is

inhibited by wortmannin [26]. The specific lipids

involved and their precise mode of action remain to be

defined.

Phagosome maturationThe membrane of the phagosome is originally derived

from the plasmalemma and its soluble contents are a

sampling of the extracellular space. The lumen of the

nascent phagosome is therefore a rather benign environ-

ment, incapable of eliminating invading microorganisms

or of disposing apoptotic bodies. These capabilities are

acquired subsequently, as a result of maturation. In many

respects, phagosomal maturation recapitulates progres-

sion from endocytic vesicles to lysosomes. Early phago-

somes acquire Rab5 and EEA1, quintessential markers of

early endosomes. Phagosomes next adopt late endosomal

features. This transition is accompanied by divestment of

Rab5 and acquisition of Rab7 and by the appearance of

specific markers such as LAMP1 and the mannose-6-

phosphate receptor [34]. Ultimately, phagosomes merge

with lysosomes, acquiring cathepsins and other hydro-

lases. Throughout this sequence, the phagosomal lumen

becomes progressively more acidic.

Aside from a general assessment of the total lipid com-

position at specific stages in the maturation process,

Figure 3

Lipid metabolism during phagosome maturation. (a) Time course illustrating

and LBPA during phagosome formation and maturation. The dashed lines in

occur based on the parallel behavior of the endocytic pathway. The height

indicative of absolute concentrations. (b–d) Distribution of PI(3)P accumulat

tandem FYVE domains from EEA1 attached to GFP. Time zero is defined as


comparatively little was known about the specific role

of lipids in phagosomal maturation. Only the major lipid

species had been determined by end-point determina-

tions, yielding little dynamic information. This situation

changed recently with the generation of antibodies and

fluorescent probes able to detect minor lipid species

(Figure 3a). One such lipid, phosphatidylinositol 3-phos-

phate (PI(3)P), which is characteristic of early endosomes,

was detected in phagosomes using constructs consisting

of FYVE or PX domains fused to a fluorescent protein

[35]. PI(3)P is clearly apparent on the membrane of

phagosomes within 1–2 min of sealing and persists for

�10 min, disappearing subsequently (Figure 3). Two

lines of evidence point to hVps34, a class III PI(3)K,

being the enzyme that catalyzes the transient production

of PI(3)P: the kinase was detected on isolated phagosomal

membranes by immunoblotting [36] and, more compel-

lingly, antibodies directed to hVps34 prevented the accu-

mulation of PI(3)P [12]. It is not clear what reaction

removes PI(3)P from phagosomes, but hydrolysis by 30-phosphatases of the myotubularin family and/or conver-

sion to phosphatidylinositol-3,5-bisphosphate (PI(3,5)P2)

(Figure 4a) by PIKfyve, a 5-kinase, are likely alternatives

[37–39].

The importance of PI(3)P on phagosomes is highlighted

by the fact that wortmannin and LY294002, which inhibit

class III as well as class I PI3K, arrest maturation at an

the changes in the relative abundance of PI(4,5)P2, PI(3)P, PI(3,5)P2

dicate hypothetical concentration changes that are proposed to

of the curves is intended to reflect relative changes and is not

ion during phagosome maturation. PI(3)P was monitored using two

after the sealing of the phagosome.



Figure 4

Lipid remodeling during endosome progression. (a) The structure of PI(3)P, PI(3,5)P2 and LBPA. Phosphate groups shown as red circles.

(b) Lipid regulators of endosomal maturation and their effectors. Top inset: PI(3)P generated by hVps34 in early endosomes anchors Hrs that

associates with the ESCRT complex, which promotes inward budding and multivesicular body (MVB) formation. PI(3)P can be converted to

PI(3,5)P2 by PIKfyve. Bottom inset: LBPA binds to Alix and favors membrane curvature. LBPA is abundant in internal vesicles of MVBs.

early stage [40]. The effects of PI(3)P are, in all like-

lihood, mediated by its ability to recruit ligands like

EEA1 and Hrs (Figure 4b). EEA1 bridges and may

contribute to the fusion of membranes bearing Rab5

and Rab4, while Hrs brings to the membrane the oligo-

meric ESCRT complex, which drives the inward mem-

brane budding that generates multivesicular bodies

(MVBs) (Figure 4b) [41]. There is convincing evidence

implicating both EEA1 and Hrs in phagosome matura-

tion: microinjection of inhibitory antibodies, transfection

of dominant-negative constructs or delivery of siRNA can

impair the acquisition of lysosomal markers by maturing


phagosomes [36,42]. Other PI(3)P-binding proteins, such

as sorting nexins, are also recruited to phagosomes in a

PI(3)P-dependent manner, but their function has not

been clarified.

Other lipids are also likely to be actively involved in

phagosome maturation. As mentioned above, PI(3,5)P2 is

likely to be formed by PIKfyve (Figure 4a). Because its

yeast homologue, Fab1p, is an important regulator of

vacuolar sorting, PIKfyve is likely to contribute to phago-

some maturation. However, the existence of PI(3,5)P2 on

phagosomes and its functional involvement remain to be



established. By contrast, there is convincing evidence that

another important lipid mediator accumulates in phago-

somes. Lysobisphosphatidic acid (LBPA) (also known as

bismonoacylphosphatidic acid), which is generated by

degradation of phosphatidylglycerol and cardiolipin

[43], is normally abundant in the internal membranes

of MVBs and late endosomes [44] (Figure 4). It has also

been identified in maturing endosomes, though it is

unclear whether it is formed in situ or is imported by

fusion with late endosomes. LBPA has a unique cone-

shaped structure that may induce membrane curvature,

facilitating the budding that generates MVBs [45] (Figure

4b). Recently, Gruenberg and colleagues demonstrated

that the addition of LBPA to pure lipid liposomes causes

them to adopt an MVB-like multivesicular morphology,

but only if the pH is acidic, as is the case in the phago-

somal lumen [46�]. However, LBPA is unlikely to be

solely responsible for budding. Indeed, Gruenberg’s team

identified ALIX, an E class Vps protein, as a regulator of

MVB formation. ALIX is an LBPA-binding protein and

its depletion by means of siRNA reduces the number of

acidic compartments in the cells [46�]. The presence of

ALIX in phagosomes has not been reported and much

remains to be learned about its possible role and that of

LBPA in maturation.

The internal vesicles of MVBs also contain significant

amounts of cholesterol. Typically implicated in the stabi-

lization of microdomains at the plasma membrane, cho-

lesterol is also found in the endocytic pathway. Nearly 80%

of the cholesterol content in the endocytic pathway is

confined to the recycling compartments of the early and

late endosomes [47]. Intriguingly, cholesterol is nearly

absent from lysosomal membranes. Insights into to the

role of cholesterol in endomembrane traffic have been

gleaned from studies in cells derived from Niemann-Pick

type C (NPC) patients. NPC is an inherited cholesterol-

storage disorder that typically results in a marked accu-

mulation of cholesterol in late endosomal structures [48].

Defects in the cholesterol-binding proteins NPC1 and

NPC2 account for nearly all cases of NPC. Most interest-

ingly, the NPC phenotype is also associated with defects in

traffic between late endosomes and lysosomes [49]. Under

normal conditions, the progressive decrease in cholesterol

levels along the endocytic pathway is accompanied by an

increase in the levels of ceramide [50]. Ceramide, pro-

duced from the catabolism of sphingomyelin [51], is also

capable of stabilizing lipid microdomains [52] and thus

may function in an analogous manner to cholesterol.

Though the precise contribution of the cholesterol-to-

ceramide switch during endocytic progression has not

yet been adequately explored, it is tempting to speculate

that the ratio of these two lipids may function as a vital cue

in the late-endosome-to-lysosome transition.

Despite its importance in endocytic traffic, remarkably

little is known about cholesterol in phagosomes.


Evidence of its presence is sketchy and precise quantita-

tion of cholesterol concentration at the individual stages

of the maturation sequence is lacking. Cholesterol has

been invoked in regulating the fate of PI(3)P in phago-

somes, their ability to bind flotillin and even in their

microbicidal competence. However, most of this informa-

tion is preliminary and much remains to be done.

ConclusionsWhile formerly regarded as a solvent matrix for membrane

proteins or as an insulator separating cellular compart-

ments, it is now strikingly clear that lipids play an active

and very dynamic role in virtually all aspects of cell func-

tion, with phagocytosis being no exception. Lipids are

critical in transducing phagocytic signals, in remodeling

the actin cytoskeleton and in attracting molecular motors

during phagosome formation. In phagosome maturation,

lipids dictate membrane fusion and fission. Importantly,

lipid metabolism is also a critical event in host–pathogen

interactions. This is best illustrated by Salmonella, which

co-opts the host cell phosphoinositide metabolism during

invasion. The bacterium injects effectors that induce loca-

lized hydrolysis of PI(4,5)P2 to gain entrance into the cell

[53], and promote the formation of PI(3)P to establish a

favorable replicative niche [54�]. Conversely, Mycobacter-ium promotes the exclusion of PI(3)P from the phagosomal

membrane in order to arrest phagosomal maturation, pre-

venting fusion with potentially microbicidal lysosomes

[55�]. We predict that lipids will be similarly found to

control other aspects of the microbicidal response, such as

the generation of reactive oxygen intermediates. More

sophisticated lipid detection methods and the develop-

ment of additional biosensors for in situ determination will

be needed to propel this field forward.

AcknowledgmentsWork in the authors’ laboratory is supported by the Heart and StrokeFoundation of Canada and the Canadian Institutes for Health Research.T. Y is supported by a CIHR MD/PhD studentship. B. O. is supported bya ResTraComp fellowship from the Hospital for Sick Children. S.G. is thecurrent holder of the Pitblado Chair in Cell Biology.

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Scott CC, Dobson W, Botelho RJ, Coady-Osberg N,Chavrier P, Knecht DA, Heath C, Stahl P, Grinstein S:Phosphatidylinositol-4,5-bisphosphate hydrolysis directsactin remodeling during phagocytosis. J Cell Biol 2005,169:139-149.

This study explores the mechanisms leading to actin disassembly duringphagocytosis and suggests that PI(4,5)P2 hydrolysis rather than Rac1inactivation is mainly responsible for actin depolymerization during com-pletion of phagocytosis.

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This study reports the ability of the unique lipid LBPA to induce theformation of multivesicular structures in a pH-dependent manner.

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52. Xu X, Bittman R, Duportail G, Heissler D, Vilcheze C,London E: Effect of the structure of natural sterols andsphingolipids on the formation of ordered sphingolipid/steroldomains (rafts). Comparison of cholesterol to plant, fungal,and disease-associated sterols and comparison ofsphingomyelin, cerebrosides, and ceramide. J Biol Chem 2001,276:33540-33546.

53. Terebiznik MR, Vieira OV, Marcus SL, Slade A, Yip CM,Trimble WS, Meyer T, Finlay BB, Grinstein S: Elimination ofhost cell PtdIns(4,5)P(2) by bacterial SigD promotesmembrane fission during invasion by Salmonella.Nat Cell Biol 2002, 4:766-773.

54.�

Hernandez LD, Hueffer K, Wenk MR, Galan JE: Salmonellamodulates vesicular traffic by altering phosphoinositidemetabolism. Science 2004, 304:1805-1807.

Reports the ability of the bacterial phosphatase SopB to catalyze thegeneration of PI(3)P, which modulated membrane traffic.

55.�

Vergne I, Chua J, Lee HH, Lucas M, Belisle J, Deretic V:Mechanism of phagolysosome biogenesis block by viableMycobacterium tuberculosis. Proc Natl Acad Sci USA 2005,102:4033-4038.

A mycobacterial phosphatase is found to reduce the phagosomal contentof PI(3)P, contributing to maturation arrest.


lipid metabolism and dynamics during phagocytosis

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