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Infection and Immunity, December 1998, p. 6017-6021, Vol. 66, No. 12
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Chlamydia trachomatis IncA Is Localized
to the Inclusion Membrane and Is Recognized by Antisera from
Infected Humans and Primates
John P.
Bannantine,1
Walter E.
Stamm,2
Robert J.
Suchland,2 and
Daniel
D.
Rockey1,*
Department of Microbiology, Oregon State
University, Corvallis, Oregon 97331-3804,1 and
Division of Allergy and Infectious Diseases, School of
Medicine, University of Washington, Seattle, Washington
98195-65232
Received 22 June 1998/Returned for modification 29 July
1998/Accepted 11 September 1998
 |
ABSTRACT |
Chlamydia psittaci produces a collection of proteins,
termed IncA, IncB, and IncC, that are localized to the chlamydial
inclusion membrane. In this report we demonstrate that IncA is also
produced by Chlamydia trachomatis. C. trachomatis IncA is
structurally similar to C. psittaci IncA and is also
localized to the inclusion membrane. Immunoblot analysis demonstrated
that sera from C. trachomatis-infected patients and from
experimentally infected monkeys both recognized C. trachomatis IncA.
| |
TEXT |
Chlamydiae depend heavily on their
host cells for energy and essential nutrients, including amino acids
and nucleoside triphosphates. Unlike species of the bacterial parasites
Shigella, Listeria, and Rickettsia,
which have direct access to the nutrient-rich environment of the host
cytoplasm (8, 20, 21), chlamydiae are sequestered in a
membrane-bound vacuole, termed an inclusion. Living within a vacuole
presents some unique challenges not faced by organisms in the
cytoplasm. One of these challenges includes the acquisition of
nutrients from the host cell. Heinzen and Hackstadt (6)
showed that the inclusion membrane is not passively permeable to
molecules as small as 520 Da by microinjection studies of fluorescent tracer molecules. Therefore, nutrient acquisition is likely mediated through transport mechanisms at the inclusion membrane.
Another key to chlamydial pathogenesis and survival is their ability to
avoid fusion with lysosomal compartments in order to persist and
replicate within the host cell. Several experiments have shown the
mature chlamydial inclusion to be nonfusogenic with markers from the
endosomal-lysosomal pathway. Electron microscopic analysis showed that
ferritin-labeled lysosomes do not fuse with the inclusion
(23). Neither fluid-phase markers nor markers of the early
or late endosomes are associated with the chlamydial inclusion (7,
15, 19). However, chlamydiae do sequester and modify host cell
lipids and apparently reside in an exocytic arm of the host vesicular
trafficking network (4, 5, 22). Modification of the vesicle
to intersect an exocytic pathway requires chlamydial protein synthesis,
which suggests that the chlamydiae synthesize proteins that determine
the vesicular interactions of the inclusion (16).
It is thought that both acquisition of nutrients and avoidance of
lysosomal fusion may be mediated by chlamydial proteins secreted into
the inclusion membrane. This led to the identification and
characterization of IncA, a Chlamydia psittaci protein that is present uniquely in infected cells, is localized to the inclusion membrane (12), is exposed to the host cell cytoplasm, and is phosphorylated by the host cell (13). Two additional
inclusion membrane proteins, termed IncB and IncC, were recently
identified in C. psittaci (1).
Despite considerable effort, incA, incB, and
incC were never detected in Chlamydia trachomatis
by conventional laboratory methods. The failure of these approaches led
to the concern that C. psittaci IncA, IncB, and IncC might
not directly model inclusion development in the human pathogenic
species of the chlamydiae. With the completion of the C. trachomatis genome project (17), incA has
been identified in this species. This report describes our
characterization of IncA from C. trachomatis.
Organisms.
C. trachomatis LGV-434, serovar L2, and
C. trachomatis serovar D were cultivated in HeLa 229 cells
as previously described (3). The trachoma biovar strains
(serovars A, B, Ba, and C), the genital strains (serovars D, D-, E, F,
G, H, I, Ia, J, and K), and the LGV biovar strains (serovars L1, L2,
L2a, and L3) were also cultivated in HeLa cells. Specific strains
studied included A/G-17/OT, B/TW-5/OT, Ba/Ap-2/OT, C/TW-3/OT,
D/UW-3/Cx, Da/TW-448/Cx, D-/MT 157/Cx, E/UW-5/Cx, F/UW-6/Cx,
G/UW-57/Cx, H/UW-4/Cx, I/UW-12/Ur, Ia/UW-202/NP, I-/MT 518/Cx,
J/UW-36/Cx, K/UW-31/Cx, L1/440/Bu, L2/434/Bu, L2a/UW-396/Bu, L3/404/Bu,
and C. psittaci GPIC.
Antiserum production.
A maltose-binding protein (MBP)-IncA
fusion protein was produced by using the pMAL-c2 vector system from New
England Biolabs as described previously (1). C. trachomatis serovar D incA was amplified with
5'-AGCCATAGGATCTGGTTTCAGCGA-3' and
5'-GCGCGGATCCTAGGAGCTTTTTGTAGAGGGTGA-3' and then
cloned into pMAL-c2.
MBP-IncA was used as antigen for the production of monospecific
antibody in New Zealand White rabbits (12). Antiserum
against C. trachomatis serovar L2 was produced in
cynomolgus monkeys (Macaca fascicularis). Monkeys were
anesthetized and infected urethrally with C. trachomatis
elementary bodies (EBs) three times over the course of 6 months.
Symptoms of infection were monitored over time. Antisera from infected
monkeys were tested for reactivity to chlamydiae by enzyme-linked
immunosorbent assay (reference 18 and unpublished
data) and immunoblotting. Human sera that demonstrated high titers of
antibody to C. trachomatis or Chlamydia pneumoniae by microimmunofluorescence assay were selected from stored serum specimens at the University of Washington. Negative control antisera were taken from patients who had no detectable reactivity by microimmunofluorescence against any of the C. trachomatis serovars listed above or C. pneumoniae
TWAR. Antilipopolysaccharide monoclonal antibody was produced as
described previously (2).
Immunoblotting and immunofluorescence microscopy.
Polyacrylamide gel electrophoresis and immunoblotting were performed as
previously described (11, 12). Chlamydiae grown in HeLa
cells on sterile glass coverslips were methanol fixed 30 h
postinfection and stained as previously described (12). Immunostained coverslips were visualized with the 63× objective of a
Zeiss microscope equipped with an epifluorescence condenser and an MC
63 C photomicrographic camera.
Sequence analysis of C. trachomatis incA.
All sequence
analysis was conducted by using methods described by Bannantine et al.
(1). C. trachomatis incA was identified by
limited homology in the C. trachomatis genome sequence
database (17). A BLAST search of the amino acid sequence
showed C. psittaci IncA to be the strongest match in the
database, but that match was weak, with an E value of only 2 × 10
5. The 30-kDa size of IncA from C. trachomatis is smaller than that of C. psittaci IncA,
and their identity and similarity were only 21 and 41%, respectively.
Weak homology at the nucleotide sequence level explained why C. trachomatis incA was not detected by Southern hybridization or PCR
amplification with probes and primers from the C. psittaci
genomic sequence. Although IncA sequence identity between C. trachomatis and C. psittaci is low, comparison of their
hydropathy plots shows similar large hydrophobic regions near the
N-terminal ends (Fig. 1). Such a long
hydrophobic region, with its unique bilobed shape, may be useful in
predicting other chlamydial proteins in the inclusion membrane since it
is also present in IncB and IncC (1). The location of the
hydrophobic domain is near the C-terminal end in IncB and IncC. To show
that this hydrophobic domain is not fortuitous, several open reading frames (ORFs) identified in the C. trachomatis genome
project have been screened by hydropathy plot analysis, and only tested ORFs that encode proteins with similar secondary structure are localized to the inclusion membrane (13a). Primers were
designed from the serovar D incA sequence, and they
amplified incA from serovar L2 as well as D. The sequence
from these two serovars is highly conserved: only 5 of 273 amino acids
are different. The same primers did not amplify a product with C. pneumoniae genomic DNA as a template.
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FIG. 1.
Comparison of IncA proteins from C. psittaci
and C. trachomatis by hydropathy plot analysis. A hydropathy
profile of each protein shows a unique bilobed hydrophobic domain in
the N-terminal half. Profiles were determined by the algorithm
developed by Kyte and Doolittle (9), with a window size of
seven amino acids. The vertical axis displays relative hydrophilicity,
with negative scores indicating relative hydrophobicity.
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|
The region surrounding
incA is not conserved between
C. trachomatis and
C. psittaci. In previous work,
we and others have
isolated four independent
C. psittaci
genomic clones that collectively
define a group of four physically
linked genes as shown in Fig.
2 (
12,
13a). The completion of the
C. trachomatis genome
sequence
has allowed a comparison of the arrangement of these genes in
C. psittaci and
C. trachomatis. Each of the
four ORFs is present
in the
C. trachomatis genome, but the
physical linkage has been
disrupted. In
C. psittaci,
incA is immediately upstream of an
ORF designated GPIC133
(Fig.
2), with an intergenic region of
157 bp (see orf2 in reference
12). ORF 133 is present in both
C. psittaci and
C. trachomatis and is relatively
conserved, with
58% identity between the deduced amino acid sequences.
The
incA coding sequence in
C. trachomatis
is downstream and separated
from ORF 133 (D133) by 12,678 bp, with
incA located at contig
2.3 in the genome and D133 located at
contig 2.5. Note the scale
difference between the two genomic segments
in Fig.
2.
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FIG. 2.
ORF map of the chromosomal region surrounding
incA in C. psittaci and C. trachomatis. ORFs 131, 132, 133, and incA are labeled.
Note the scale difference between the maps. ORF 133 is immediately
downstream of incA in C. psittaci, whereas it is
upstream and separated by at least 10 kb in C. trachomatis.
Base pairs are indicated above each map, and arrows indicate the
direction of transcription. The ORF designation is preserved from the
C. trachomatis serovar D genome database designations.
Pustell protein matrix analysis was used to confirm that GPIC131 and
GPIC132 correspond to D131 and D132, respectively.
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Immunoblot analysis of infected cells and purified
C. trachomatis EBs was performed with rabbit anti-MBP-IncA as a
probe.
A 27-kDa band was present only in the infected cells and not in
lysates of EBs or uninfected cells (data not
shown).
In order to determine if IncA was recognized by sera from convalescent
animals and humans, purified MBP-IncA fusion protein
was loaded onto a
preparative sodium dodecyl sulfate-polyacrylamide
gel and used to
examine reactivity with sera from patients and
monkeys infected with
C. trachomatis. The majority of the sera
from
chlamydia-infected patients (10 of 11) and all monkey
convalescent-phase
sera recognized the IncA protein (Fig.
3A) but not the MBP portion
of the fusion
(Fig.
3B). IncA was faintly recognized by sera from
one of the
C. pneumoniae-infected patients (Fig.
3A, lane 1).
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FIG. 3.
Preparative immunoblot analysis of a purified
MBP-C. trachomatis IncA fusion protein (A) and purified MBP
(B), each probed with antisera from chlamydia-infected patients and
monkeys. Lane A, anti-MBP; lane B, monkey convalescent-phase sera;
lanes 1 and 2, sera from C. pneumoniae-infected patients;
lanes 3 to 13, sera from C. trachomatis-infected patients;
lanes 14 and 15, negative control sera.
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|
Antisera against IncA and a monoclonal antibody against chlamydial
lipopolysaccharide were used to immunostain methanol-fixed
layers of
C. trachomatis-infected HeLa cells. Anti-IncA reacted
with
the membrane of the inclusion but not the chlamydial developmental
forms (Fig.
4A to C). Antigenic fibers
extending away from the
inclusion, which are similar in structure to
those found in
C. psittaci-infected cells (
12),
were also present in
C. trachomatis-infected
cells (Fig.
4B
to D). Their function and origins remain unknown.
Also evident in Fig.
4B and C are antigenic fibers that traverse
between otherwise
apparently separate cells. It is likely that
these are daughter cells
in which inclusions can either divide
with the dividing cell
(
10) or stay in one daughter cell and
leave the other
uninfected.
C. psittaci IncA can also be found
in fibers
that extend between pairs of infected cells (data not
shown). One major
difference between these two processes is that
in
C. psittaci (strain GPIC), each daughter cell usually remains
infected. In
C. trachomatis, however, uninfected progeny
cells
are common. Because IncA is also found in fibers that extend to
the uninfected daughter cells (Fig.
4B and C), the result is a
cell
lacking chlamydial developmental forms but containing chlamydial
antigen.
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FIG. 4.
Immunofluorescence microscopy with anti-IncA
demonstrating that IncA is localized to the inclusion membrane in
C. trachomatis-infected cells. Serovar L2-infected HeLa
cells were fixed in methanol 25 h postinfection and stained with
anti-major outer membrane protein (A) and/or anti-MBP-IncA (B to E).
Panels A to C represent a single image, with panel C photographed in a
different focal plane. Note the fibers extending between the two
inclusions in different cells as well as from one infected cell to an
apparently uninfected cell (uninfected cell at tip of arrow). Note also
the antigenic fibers extending from several inclusions in one focal
plane (D) and IncA in inclusions at different stages of maturation in
another focal plane (E). Bars in panels A and D represent 10 µm for
panels A to C and panels D and E, respectively.
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|
In addition to the LGV biovar strain (serovar L2) shown in Fig.
4,
several other
C. trachomatis serovars of clinical interest
were analyzed by immunofluorescence microscopy for staining with
anti-MBP-IncA (Table
1). Anti-MBP-IncA
labeled the inclusion
membranes of all serovars tested.
The inclusion membrane mediates all contact between the host cell and
chlamydiae; therefore, the acquisition of nutrients
and the
nonfusogenic nature of the chlamydial inclusion may be
elucidated by
studying chlamydial proteins that reside in the
inclusion membrane.
Because the routing of transport vesicles
throughout the cell is
mediated by proteins present on the transport
vesicle membrane
(
14), IncA as well as IncB and IncC are excellent
candidate
proteins for mediating inclusion trafficking within
infected cells. We
undertook these studies to define the presence
and intracellular
location of IncA in all of the major
C. trachomatis serovars
and to assess whether an antibody response to IncA was
present in
infected patients and primates. We speculate that
C. pneumoniae also produces Inc-like proteins and are initiating
an
investigation into this system. Finally, we continue to pursue
questions surrounding the role of the Inc proteins in the chlamydial
infection process as well as their role as possible protective
antigens
in the host response to chlamydial
infection.
Nucleotide sequence accession number.
The nucleotide sequence
of C. trachomatis LGV-434, serotype L2, incA has
been deposited in the GenBank database under accession no. AF067958.
| |
ACKNOWLEDGMENTS |
We gratefully acknowledge Richard Stephens and Claudia Fenner at
the University of California, Berkeley, for their efforts in the
completion of the C. trachomatis genome project. We thank Linda Cles of the University of Washington for providing the human serum samples. We also thank Harlan Caldwell and Michael Parnell for
assistance with the production of primate convalescent-phase sera.
A portion of this work was supported by Public Health Service (PHS)
grants AI-31448 and N01-AI-75329 to W.E.S. and PHS grant AI42869-01 to
D.D.R.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Oregon State
University, Department of Microbiology, 220 Nash Hall, Corvallis, OR
97331-3804. Phone: (541) 737-1848. Fax: (541) 737-0496. E-mail:
rockeyd{at}ucs.orst.edu.
Technical paper 11411 of the Oregon State University Extension and
Experiment Station.
Editor:
P. E. Orndorff
| |
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Infection and Immunity, December 1998, p. 6017-6021, Vol. 66, No. 12
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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