Understanding lipid rafts and other related membrane domains.

Abstract

Evidence in support of the classical lipid raft hypothesis has remained elusive. Data suggests that transmembrane proteins and the actin-containing cortical cytoskeleton can organize lipids into short-lived nanoscale assemblies that can be assembled into larger domains under certain conditions. This supports an evolving view in which interactions between lipids, cholesterol, and proteins create and maintain lateral heterogeneity in the cell membrane.

Full text

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Understanding lipid rafts and other related membrane domains
Aaron K Neumann1, Michelle S Itano1and Ken Jacobson1,2*
Addresses:1Department of Cell and Developmental Biology, University of North Carolina, CB# 7090, Chapel Hill, NC 27599-7090, USA;
2Lineberger Comprehensive Cancer Center, University of North Carolina, CB# 7295, Chapel Hill, NC 27599-7295, USA
*Corresponding author: Ken Jacobson (frap@med.unc.edu)
F1000 Biology Reports 2010, 2:31 (doi:10.3410/B2-31)
The electronic version of this article is the complete one and can be found at: http://f1000.com/reports/biology/content/2/31
Abstract
Evidence in support of the classical lipid raft hypothesis has remained elusive. Data suggests that
transmembrane proteins and the actin-containing cortical cytoskeleton can organize lipids into short-
lived nanoscale assemblies that can be assembled into larger domains under certain conditions. This
supports an evolving view in which interactions between lipids, cholesterol, and proteins create and
maintain lateral heterogeneity in the cell membrane.
Introduction and context
Differential lipid composition between the apical and
basolateral membrane domains of epithelial cell
plasma membranes [1,2] made it clear that membrane
lipids are not laterally distributed in a homogeneous
fashion. The lipid raft hypothesis was developed to
explain lateral separation of bilayer lipids, and this idea
quickly found applications in viral budding, endocy-
tosis, and signal transduction (reviewed in [3]). In
model membranes, lipids can separate into microsco-
pically resolvable raft-like domains [4]. Plasma mem-
brane surrogates formed by chemical membrane
blebbing or cell swelling procedures also show phase
behaviour [5-8]. Similar domains are not evident upon
direct observation of unperturbed plasma membranes
in living cells, but the non-equilibrium nature of cell
membranes, including endocytosis, exocytosis, and
other motile processes, may prevent overt phase
separation. Likewise, quantitative analysis of lipid-
anchored protein and lipid diffusion in cell membranes
by fluorescence recovery after photobleaching (FRAP),
Förster resonance energy transfer (FRET), and fluores-
cence correlation spectroscopy (FCS) [9-11] indicated
that rafts in the plasma membrane of resting cells must
be very small or ephemeral (or both), forcing an
evolution of the lipid raft hypothesis. These tiny clusters
do not represent lipid phase separations but are
probably short-range ordering imposed upon lipids by
transmembrane proteins and cortical actin structures.
Thus, the current challenge for the field is to understand
the interplay between protein and lipid that converts
the exceedingly small, unstable clusters of components
into larger, more stable membrane microdomains
required for function [3,12].
Major recent advances
The recent development of sensitive quantitative micro-
scopy methods has advanced our knowledge of lipid
dynamics in resting cells. The diffusion of raft lipids (e.g.,
sphingomyelin) and non-raft lipids (e.g., phosphatidy-
lethanolamine) was measured by an elegant FCS techni-
que within regions as small as 30 nm in diameter using
stimulation emission depletion fluorescence microscopy.
The results indicate that raft lipids, but not non-raft lipids,
are indeed preferentially trapped, albeit for short dis-
tances (<20 nm) and for short periods (10-20 ms) [13].
HomoFRET measurements, combining FRAP, emission
anisotropy, and theoretical model fitting to test models of
lateral organization in the membrane, were used deter-
mine the degree of clustering of glycosylphosphatidylino-
sitol (GPI)-anchored proteins in the plasma membrane
[14,15].TheformationofGPI-anchoredproteinnanoclus-
ters (of ~4 molecules or even less) [14] is an active process
involving both actin and myosin, and these nanoclusters
are nonrandomly distributed into larger domains of
<450 nm [15]. Additionally, high-speed single-particle
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tracking (50 kHz) revealed that GPI-anchored proteins,
along with other membrane proteins, undergo rapid hop
diffusion between 40 nm actin-regulated compartments,
witha compartment dwell timeof1-3msonaverage [16].
However, when GPI-anchored proteins were deliberately
cross-linkedbygold orquantum dot particles, theyunder-
went transient confinement or ‘STALL’ (stimulation-
induced temporary arrest of lateral diffusion) from a
cholesterol-dependent nanodomain in a Src family kinase
mediated manner [17-19]. A recent study identified a
transmembrane protein (carboxyl-terminal Src kinase
[Csk]-binding protein) involved in the linkage between
the particle-cross-linked GPI-anchored protein, Thy1, and
the cytoskeleton (Figure 1) [20].
Larger microdomains involve raft lipids and specific
membrane proteins. The lipid envelope of influenza and
HIV virions, but not those of the vesicular stomatitis
virus (VSV) or Semliki Forest virus (SFV), is enriched in
raft-like lipids, leading to the notion that these viruses
bud from lipid microdomains in the plasma membrane
[21-25]. By contrast, the lipidomes of VSV and SFV are
very similar to each other and to that of the plasma
membrane suggesting that these viruses do not select or
generate lipid raft domains for budding [25].
The protein and lipid environment of the budding
domains of hemagglutinin (HA) and HIV has been the
source of several recent papers examining the process of
viral budding using quantitative live-cell imaging tech-
niques. Influenza buds from HA clusters (ranging up to
micrometers in diameter) [26] regulated by HA trans-
membrane region length and palmitoylation [27].
Recent fluorescence lifetime imaging microscopy
(FLIM)-FRET experiments in living cells indicate that
HA colocalizes with lipid microdomain markers, further
supporting the role of lipid-protein interactions in
influenza virus budding [28,29]. Proton magic angle
spinning nuclear magnetic resonance was used to detect
a minor fraction (~10-15%) of liquid-ordered mem-
brane phospholipids in HA virions and virion lipid
extracts at 37°C. While lipid ordering increased at lower
temperatures, it was not required for virion fusion with
target membranes [30].
Progressive recruitment of cytoplasmic HIV-1 Gag to the
membrane, via post-translational acyl lipid modification
and PIP2/basic residue interactions, forms membrane
domains that culminate in virion budding [31-33].
While the HIV-1 lipid envelope composition indicates
enrichment in lipids and proteins associated with ‘rafts’
[21], paradoxically, one report has failed to observe an
enrichment of enhanced green fluorescent protein
(EGFP)-GPI at Gag domains in living cells [32],
suggesting that the local lipid microenvironment may
not exactly parallel the classic raft lipid composition.
Recent work has implicated the tetraspanin family of
proteins in Gag domain formation and function.
Tetraspanins, a widely expressed and highly conserved
class of transmembrane proteins (reviewed in [34]),
form tetraspanin-enriched microdomains (TEMs)
through lateral tetraspanin-tetraspanin interactions and
binding to non-tetraspanin membrane proteins. HIV-1
Gag is targeted to TEMs and virus buds from these
domains [35,36]. Tetraspanins can be palmitoylated [37]
and the lipid environment within TEMs contains
cholesterol, but GPI-anchored proteins and caveolin
are not enriched in TEMs (reviewed in [38]). Recently,
cholesterol and tetraspanin palmitoylation were
Figure 1. EBP50-ERM assembly is the common adaptor complex
for linking cholesterol-dependent Thy-1 clusters to the membrane
apposed cytoskeleton
The glycosylphosphatidylinositol(GPI)-anchored protein Thy-1 engages mem-
brane lipids and proteins for transmembrane signaling. Thy-1 crosslinking by
streptavidin-coated quantum dots aggregates GPI lipid tails in the outer
leaflet of the plasma membrane in a cholesterol-dependent manner.
Carboxyl-terminal Src kinase (Csk)-binding protein (CBP), a transmem-
brane protein, is recruited to or captured by Thy-1 clusters along with Src-
family kinase substrates (KS). CBP or KS (or both) are phosphorylated by
Src-family kinases (SFK), enabling CBP to bind to actin filaments via an
EBP50-ERM (ezrin/radixin/moesin-binding phosphoprotein 50-ezrin/radixin/
moesin) adaptor linkage resulting in a transient anchorage. When either
CBP or the adaptors are dephosphorylated by an unspecified protein
tyrosine phosphatase (PTP) the anchorage is terminated. Image adapted
from [20]; Chen et al., J Cell Sci 2009.
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implicated in the confined diffusion and co-diffusion (of
two tetraspanin molecules) of the tetraspanin CD9 [39].
Tetraspanins appear to induce order in the plasma
membrane by virtue of protein clustering, but they likely
also stabilize lipid microenvironments in the plasma
membrane allowing for lateral organization of HIV-1
Gag and virion budding.
Some lectin-based membrane domains form in the
absence of post-translational lipid modifications or
known lipid binding activity. Dendritic cell-specific
intracellular adhesion molecule-3-grabbing non-integrin
(DC-SIGN), a tetrameric C-type lectin with affinity for
high-mannose glycans, forms microdomains on the
plasma membrane [40-42] that serve as high-avidity
binding sites for numerous pathogens. A previous report
suggested that DC-SIGN interacts with lipid rafts [40], but
this was based on detergent insolubility and cholera toxin
colocalization assays, which generally do not faithfully
report on intrinsic membrane lateral heterogeneity. Also,
DC-SIGNdomainsdonot dependoncholesterol(unpub-
lished data). Surprisingly, DC-SIGN domains do not
recover following photobleaching[42].This resultimplies
that DC-SIGN within domains does not exchange with
the surrounding membrane. The source of this stability
remains a mystery, and its cause may not reside in the
membrane-apposed cytoskeleton but in extracellular
cross-linking factors such as galectins (reviewed in [43]).
DC-SIGN membrane domains that are multiplexed with
another C-type lectin, CD206 (unpublished data), appear
to mediate the formation of fungipods, novel cellular
protrusive structures involved in fungal recognition by
dendritic cells (Figure 2) [44]. Thus, the lateral hetero-
geneity in membranes provided by rafts and other
microdomains continues to provide surprising functional
consequences.
Future directions
A variety of membrane domain forming systems have a
wide gamut of lipid and protein constituents and possess
a correspondingly broad range of functions. Recent
advances have shown that preferential lipid trapping or
confinement in the resting plasma membrane occurs
only on very small spatiotemporal scales. Critical
attention must be paid when determining if and when
such confinement becomes biologically meaningful for
processes such as endocytosis and signal transduction.
While lipid ordering can be stabilized by oligomeriza-
tion of membrane-associated proteins (i.e., GM1 cross-
linking, influenza HA clustering), the lipids in these
domains may still exchange between domain and
surrounding membranes, making even these stabilized
raft-like domains dynamic environments. At what point
does a membrane domain become stable enough to be
biologically relevant? What is the range of protein and
lipid turnover rates seen in membrane domains and are
Figure 2. C-type lectin domains and fungipod formation
C-type lectins (CLRs) form a type of plasma membrane domain that is not dependent on cholesterol. (A) Plasma membrane domains containing mixtures
(yellow) of dendritic cell-specific intracellular adhesion molecule-3-grabbing non-integrin (DC-SIGN) (green) and CD206 (red) are observed on a monocyte-
derived dendritic cell (DC) by immunofluorescence. DC-SIGN domains are known sites of binding and entry for a range of pathogens including HIV-1.
(B) Yeast cell wall material is sensed by these CLR membrane domains, triggering a unique protrusive response, the fungipod. The image shows an example
of a DC fungipod formed via CD206 ligation by a fixed Saccharomyces cerevisiae particle (zymosan), visualized by scanning electron microscopy (9500×).
Figure 2B was reproduced from [44], Neumann & Jacobson, PLoS Pathog 2010.
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there different turnover rates for each constituent? It is
likely that a spectrum of membrane microdomains exists
with different compositions and physical characteristics
suited to their diverse purposes. The lipid species and
their ordering within raft-like complexes appear to be key
factors in determining intradomain cohesiveness and
resultant domain size and lifetime.
Abbreviations
DC-SIGN, dendritic cell-specific intracellular adhesion
molecule-3-grabbing non-integrin; FCS, fluorescence
correlation spectroscopy; FRAP, fluorescence recovery
after photobleaching; FRET, Förster resonance energy
transfer; GPI, glycosylphosphatidylinositol; HA, hemag-
glutinin; PIP2, phosphatidylinositol 4,5-bisphosphate;
SFV, Semliki Forest virus; TEM, tetraspanin-enriched
microdomain; VSV, vesicular stomatitis virus.
Competing interests
The authors declare that they have no competing
interests.
Acknowledgments
This work was supported by National Institutes of Health
Grant GM 41402 and the Cell Migration Consortium
Grant GM 064346.
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