Commentary
TLR signalling and phagosome maturation: an
alternative viewpoint
David G. Russell* and Robin M. Yates
Microbiology and Immunology, College of Veterinary
Medicine, Cornell University, Ithaca, NY 14853, USA.
In the February issue of Cellular Microbiology Blander
expounds on the role of Toll-like receptors (TLRs) in
intraphagosomal sensing and the modulation of the
nascent phagosome (Blander, 2007a). The review
extends the hypothesis of Medzhitov and Blander that the
innate sensing machinery is capable of triggering an
accelerated or ‘inducible’ maturation that results in a
more hostile intraphagosomal environment (Blander and
Medzhitov, 2004; 2006a). Attractive though this hypoth-
esis of TLR-mediated phagosomal autonomy may be it is
contradicted directly by data from our study that used
real-time, kinetic analysis of the rates of phagosome acidi-
fication and phagosome–lysosome fusion in the presence
and absence of stimulation by particle-associated TLR
agonists (Yates and Russell, 2005; Yates et al., 2005).
Given that these papers have been overlooked in recent
reviews (Blander, 2007a,b), we feel it important to inform
readers of the substantive data arguing that TLR stimula-
tion does not impact on phagosome maturation.
In our study we employed novel fluorometric assays
that facilitate real-time measurement of pH through ratio-
metric fluorescence and phagosome–lysosome fusion
through fluorescence resonance energy transfer to probe
the kinetics of phagosome maturation (Yates and Russell,
2005; Yates et al., 2005). Initial experiments examined the
rate of maturation of IgG bead- and mannosylated bead-
containing phagosomes in the presence or absence of
lipopolysaccharide (LPS) or Pam3Cys. The experiments
were performed on both wild-type and TLR2- and TLR4-
deficient macrophages. Although we could observe TLR-
mediated signalling in the presence of coupled TLR
agonist and TLR, detected by p38 phosphorylation and
a-IkB degradation, we could not observe differences in
the rate or extent of phagosome maturation.
In a recent review by Blander and Medzhitov the
authors argue that the use of Fc receptors or the mannose
receptor provides the ‘inducible’ signal without the need
for stimulation of TLRs (Blander and Medzhitov, 2006a).
Unfortunately the authors failed to acknowledge that in
our study we then went on to examine the phagocytic
processing of additional particles (Yates and Russell,
2005). We studied uptake of Staphylococcus aureus, one
of the particles also used by Blander and Medzhitov,
and employed phosphatidylserine-coated beads as a
surrogate for the apoptotic cells to reproduce the ‘non-
inflammatory’ uptake pathway invoked in their earlier pub-
lication (Blander and Medzhitov, 2004). We looked at the
kinetics of phagosome–lysosome fusion in phagosomes
containing Staphylococcus aureus with and without
absorbed LPS in both wild-type and TLR2-deficient
macrophages. Once again although TLR-dependent sig-
nalling was detected under appropriate conditions, no
differences in phagosome maturation was observed.
Furthermore, the rate of maturation of phosphatidylserine-
coated bead-containing phagosomes, mimicking apop-
totic cells, also revealed no alterations in the kinetics of
phagosome acidification despite addition of LPS or
Pam3Cys to the particle.
So why the discrepancy? One set of experiments in our
study may hold the key. When we compared the rates of
phagosome maturation in macrophages from MyD88-
deficient mice with those from parental strain controls we
found that MyD88-deficient macrophages demonstrated
diminished phagosome–lysosome fusion in the presence
and absence of TLR agonist (Yates and Russell, 2005).
Intriguingly however, LPS altered the kinetics and degree
of phagosome–lysosome fusion in both wild-type and
MyD88-deficient macrophages. This result has two impor-
tant implications. First, MyD88-deficient macrophages
have a phagosome maturation defect that is independent
of the absence of short-term TLR-dependent signalling.
Second, LPS has the capacity to modulate phagosome
maturation independently of the action of TLR stimulation
through MyD88.
How do we interpret the data from Blander and
Medzhitov in the context of our results? Analysis of the
publication reporting the TLR-dependent modulation of
Received 8 February, 2007; accepted 15 February, 2007. *For
correspondence. E-mail dgr8@cornell.edu; Tel. (+1) 607 2533401;
Fax (+1) 607 2534058.
Cellular Microbiology (2007) 9(4), 849–850 doi:10.1111/j.1462-5822.2007.00920.x
© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltd