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Infect Immun, June 1998, p. 2648-2654, Vol. 66, No. 6
Laboratory of Microbial Structure and
Function, Rocky Mountain Laboratories, National Institute of
Allergy and Infectious Diseases, National Institutes of Health,
Hamilton, Montana 59840
Received 5 December 1997/Returned for modification 13 February
1998/Accepted 24 March 1998
Borrelia burgdorferi, the causative agent of Lyme
disease, can contain multiple genes encoding different members
of the Erp lipoprotein family. Some arthropod-borne bacteria increase
the synthesis of proteins required for transmission or mammalian
infection when cultures are shifted from cool, ambient air temperature
to a warmer, blood temperature. We found that all of the
erp genes known to be encoded by infectious isolate B31
were differentially expressed in culture after a change in temperature,
with greater amounts of message being produced by bacteria shifted from
23 to 35°C than in those maintained at 23°C. Mice infected with B31 by tick bite produced antibodies that recognized each of the Erp proteins within 4 weeks of infection, suggesting that the Erp proteins
are produced by the bacteria during the early stages of mammalian
infection and may play roles in transmission from ticks to mammals.
Several of the B31 Erp proteins were also recognized by antibodies from
patients with Lyme disease and may prove to be useful antigens for
diagnostic testing or as components of a protective vaccine.
Borrelia burgdorferi, the
causative agent of Lyme disease, is spread to humans and other mammals
through the bites of infected Ixodes ticks (8).
In unfed ticks, the bacteria are primarily restricted to the midgut,
and as ticks feed, bacteria migrate from the midgut to the salivary
glands and are transmitted into the bite wound with the saliva (5,
19, 28, 30, 50). This mode of transmission undoubtedly requires
that B. burgdorferi recognize when the host tick is
feeding on a warm-blooded animal and then synthesize proteins required
for transmission and the subsequent establishment of infection in the
mammalian host. We are seeking to identify the proteins that are
important in B. burgdorferi transmission and,
ultimately, the factors that regulate their synthesis.
Many bacteria utilize environmental temperature as a signal to
determine their location, synthesizing vector-specific proteins at the
cooler temperatures experienced within an arthropod and mammal-specific
proteins at warmer, blood temperatures (6, 20, 26, 38, 39).
Differences in temperature may also change bacterial growth rates,
which in turn may provide internal signals affecting the production of
vector- or mammal-specific proteins. We have previously reported that
B. burgdorferi increases the synthesis of certain
proteins during tick feeding or after a shift in culture temperature
from 23 to 35°C (34, 42, 45). This temperature change also
results in a marked increase in bacterial growth rate (approximately
three to four times greater in bacteria shifted from 23 to 35°C than
in those maintained at 23°C) (42), and B. burgdorferi in infected ticks also undergoes a dramatic increase
in growth rate during tick feeding (14, 28).
The B. burgdorferi proteins that we reported as being
differentially synthesized as a result of temperature shift were
recognized by sera from infected animals (34, 42),
indicating that they are normally synthesized by the bacteria during
mammalian infection. At least one of these proteins, OspC, is not
synthesized by B. burgdorferi within the midgut of
unfed ticks (16, 34), whereas bacteria within the midgut and
salivary glands of ticks that have engorged with blood produce OspC
(12, 15, 34), suggesting that this protein is involved with
bacterial transmission or the early stages of mammalian infection.
We also found that the OspE and OspF proteins of B. burgdorferi N40 (23) were differentially synthesized
after a shift in culture temperature from 23 to 35°C (42).
Analyses of B. burgdorferi B31 indicated that this
isolate can carry many members of a family of genes that are homologous
to, and apparently allelic with, the N40 ospEF locus, which
we have designated erp (OspEF-related proteins) (11,
43). We previously characterized the four erp loci
present in a noninfectious B31 culture that has been passage repeatedly
in laboratory culture medium and have found that each erp
locus is carried on one of four homologous 32-kb circular plasmids
(cp32-1 through cp32-4) (11, 43). However, infectious, low-passage-number B31 bacteria may contain at least seven 32-kb circular plasmids (cp32-1 through cp32-7), each containing an erp locus (11). Infectious B31 can also carry a
related linear plasmid (lp56) (11, 48, 49) that was not
previously known to contain an erp locus. Since this large
number of different genes and proteins could allow for a wide range of
expression patterns, characterizing all of the erp genes and
their proteins within a particular isolate is an essential step toward
understanding the roles that these proteins may play in B. burgdorferi transmission and the establishment of Lyme disease
infections. Due to the extensive sequence similarities of the cp32
plasmids, they could not be confidently assembled by the B. burgdorferi B31 genome sequencing project of The Institute for
Genomic Research (17), and their complete sequences have not
yet been published. Homologs of the B31 Erp proteins have been
identified in other isolates of B. burgdorferi,
although no more than three loci have been described from any isolate
other than B31 (1, 23, 25, 44, 46). Immune responses
directed against Erp homologs have also been described, but again,
these analyses are incomplete, as only one or two proteins from any
isolate have been examined (13, 27, 46). In this report we
describe all of the erp genes known to be carried by an
infectious culture of B31 and show that all of the erp genes
tested can be expressed by cultured bacteria by changing the
temperature from 23 to 35°C. We also found that tick-infected laboratory animals produced antibodies that recognized all of the known
B31 Erp proteins, as did many human Lyme disease patients.
Bacteria.
B. burgdorferi B31 was originally
isolated from an infected Ixodes scapularis tick collected
on Shelter Island, New York (8). These bacteria have been
maintained in the laboratory via an infectious cycle between I. scapularis ticks and mice (34). Clone B31-4a was
derived from a single colony of infectious B31 plated on solid Barbour-Stoener-Kelly (BSK) medium (22, 31) and is also
infectious in laboratory mice (11).
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Borrelia burgdorferi Erp Proteins Are Immunogenic
in Mammals Infected by Tick Bite, and Their Synthesis Is
Inducible in Cultured Bacteria
ABSTRACT
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
Cloning and sequence analysis of erp genes. Plasmid DNAs from B31-4a were purified with a Qiagen (Chatsworth, Calif.) midi-purification kit from a 100-ml culture grown at 35°C. The erpAB2 and erpX loci were PCR amplified by using oligonucleotides specific to the orf3 gene found on cp32-1 and lp56, respectively (11, 40, 49) and a conserved DNA sequence that is located approximately 1.5 kb 3' of every erp locus (2, 11, 41) (Table 1). For PCR performed with an Expand Long Template PCR kit (Boehringer Mannheim, Indianapolis, Ind.), reaction conditions consisted of 94°C for 30 s, 50°C for 30 s, and 68°C for 8 min, followed by 20 cycles of the same conditions but with successive elongation steps increasing by 20 s each cycle (41).
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Analysis of mRNA.
Total RNA was extracted from B. burgdorferi B31-4a grown at 23°C or shifted to 35°C, using an
Ultraspec RNA isolation system (Biotecx, Houston, Tex.) according to
the manufacturer's instructions. The RNA was denatured with glyoxal
and dimethyl sulfoxide, separated by agarose gel electrophoresis in 10 mM sodium phosphate buffer (pH 7.0) (32), and transferred to
nylon membranes (Micron Separations, Westborough, Mass.). Probes
specific for the B31 erp, bapA, and flaB (flagellin) genes were generated by PCR from
recombinant plasmids carrying the appropriate loci, using the
oligonucleotides listed in Table 1, as previously described
(43). DNA fragments were radiolabeled with
[
-32P]dATP (Du Pont, Boston, Mass.) by random priming
(Life Technologies, Gaithersburg, Md.). Filters were hybridized with
each radiolabeled probe at 55°C in 1% (wt/vol) bovine serum
albumin-7% (wt/vol) sodium dodecyl sulfate (SDS)-0.5 M sodium
phosphate (pH 7.0)-1 mM EDTA and washed at 55°C in 0.2× SSC (1×
SSC is 0.15 M NaCl and 0.015 M sodium citrate)-0.1% (wt/vol) SDS as
previously described (7).
Protein purification and analysis. B. burgdorferi cultures were pelleted by centrifugation, washed twice with phosphate-buffered saline, resuspended in sample buffer (32), and lysed by boiling for 5 min.
DNA fragments encoding erpA, erpB2, erpC, erpD, erpG, erpK, erpL, erpM, and erpX were individually cloned into pProEX-1 (Life Technologies), so that each gene was in the correct reading frame to encode a fusion protein with the plasmid-encoded polyhistidine polypeptide. Recombinant plasmids were transformed into Escherichia coli DH5 (Life
Technologies). A single colony from each transformation was grown at
37°C to early log phase in 100 ml of LB broth (24), induced with 100 µg of isopropyl thiogalactoside per ml, and grown for an additional 2 h before harvesting by centrifugation. The bacteria were lysed by sonication, and the fusion proteins were purified by using His-Bind Resin column chromatography kits (Novagen, Madison, Wis.) as recommended by the manufacturer.
Proteins were separated by SDS-polyacrylamide gel electrophoresis
(21) and visualized by staining with Coomassie brilliant blue. Alternatively, proteins were transferred to nitrocellulose membranes (Life Technologies) and immunoblotted as previously described
(45), using horseradish peroxidase-linked protein A
(Amersham, Arlington Heights, Ill.) and SuperSignal chemiluminescent substrate (Pierce, Rockford, Ill.).
Antisera. Uninfected larval I. scapularis ticks, hatched and reared at our facility, were fed on white-footed mice (Peromyscus leucopus) that had previously been infected with B. burgdorferi B31. After molting to the nymphal stage, ticks were placed on uninfected white-footed mice and allowed to feed to repletion. Approximately 15 to 25 ticks were fed on each mouse. Sera were collected 4 weeks (two mice) or 8 weeks (three mice) after tick attachment. Infection was determined by immunoreactivity to the B. burgdorferi BmpA (P39) protein, an antigen diagnostic of active infection (35, 37). Sera were also collected from two mice that were not infected with B. burgdorferi.
Sera from three of the mice infected for 8 weeks were pooled and preadsorbed with individual recombinant B31 Erp proteins to remove specific antibodies in subsequent immunoblot studies. Sera were diluted 1:500 in TBS (Tris-buffered saline)-Tween (20 mM Tris [pH 7.5], 150 mM NaCl, 0.05% [vol/vol] Tween 20) (45) and incubated at 37°C for 2 h with approximately 10 µg of each recombinant B31 Erp protein. Sera from 10 Lyme disease patients with unknown stages of infection from Southampton, Long Island, N.Y. (37), were used in immunoblotting assays to determine reactivity to recombinant B31 Erp proteins. Additionally, sera from five noninfected humans from Montana (where Lyme disease is not endemic) were also used in these immunoblotting experiments. All human sera were diluted 1:200 in TBS-Tween for immunoblotting.Nucleotide sequence accession numbers. The complete sequences of the B31 erpAB2, erpIJ, erpLM, and erpX loci have been deposited in GenBank and given accession no. U78764, U72996, U72998, and AF020657, respectively. The previously described B31 erpAB1, erpCD, erpG, erpH, and erpK loci have the GenBank accession no. U44912, U44914, U42598, U44913, and U72997, respectively (11, 43).
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RESULTS |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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erp gene complement of an infectious B. burgdorferi B31 culture. To aid in our elucidation of Erp protein expression and function, we cloned and sequenced the erp loci carried on the known cp32 plasmid family members in an infectious culture of isolate B31. The infectious B. burgdorferi clone B31-4a carries lp56 and all of the known cp32 plasmids except cp32-2 (11). The B31 Erp proteins were found to vary significantly in sequence, with aligned pairs sharing between 100 and 17% amino acid residues (40). Since all of these plasmids are homologous throughout most of their lengths (11, 29, 41, 43, 49), we believe that all members of the erp gene family are actually alleles of one another. However, for the sake of clarity in discussing each gene and its protein, we have chosen to retain the designations of these genes as erpA, erpB, etc. (Table 2).
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Transcriptional regulation of the erp genes. The regions of DNA located immediately 5' of all the B31 erp loci, which presumably include the promoters and any cis regulatory sequences, are nearly identical to that found 5' of the N40 ospEF locus (11, 23, 41, 43), suggesting that all of these loci may be regulated similarly. The N40 OspE and OspF proteins can be differentially synthesized in culture by shifting the growth temperature from 23 to 35°C, as can a B31 protein that is antigenically similar to the N40 OspE protein (42). We therefore examined the expression of the B31-4a erp loci to determine whether they are also similarly regulated in culture.
Northern blot analyses with probes specific for each erp gene indicated that significantly greater levels of the erp transcripts were present in bacteria that were shifted to 35°C relative to those maintained at 23°C (Fig. 1A). We also examined the expression of the bapA gene located 3' of erpG on cp32-3 and found that it, too, was expressed at higher levels in the bacteria shifted to 35°C (Fig. 1A). Rehybridizations of the same RNA blots with a probe specific for the constitutively expressed flaB (flagellin) gene (7) indicated that there were comparable amounts of RNA in all samples (Fig. 1B). The slight variation seen on some flaB-probed filters is insufficient to account for the differences seen when the same filter was hybridized with erp-specific probes (compare Fig. 1A with Fig. 1B). These results lead us to predict that similar expression patterns will be observed for other homologous loci, such as the B31 erpCD and the erp homologs found in other B. burgdorferi isolates.
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Recognition of Erp proteins by animals infected with B31. Proteins produced by B. burgdorferi during transmission from tick to mammal might be antigenic and provoke an early immune response. Such is the case with the B. burgdorferi OspC protein (18). Since the ospC gene exhibits an in vitro pattern of temperature-inducible expression similar to that of the erp genes (34, 45), we examined whether laboratory animals infected by tick bite with isolate B31 also produced antibodies that recognized the Erp proteins.
Recombinant Erp proteins were purified, separated by SDS-polyacrylamide gel electrophoresis, and transferred to nitrocellulose membranes. All of the recombinant Erp proteins migrated with apparent molecular masses that were greater than those predicted from their gene sequences (Table 2). The filters were then immunoblotted with sera from each of five mice that had been infected with B31 by tick bite. We observed that every mouse produced antibodies that reacted with all of the recombinant Erp proteins, except ErpD, within 4 weeks of tick feeding (example shown in Fig. 2). Immunoblot signals were stronger from the ErpA/I and ErpB2/J recombinant proteins (Fig. 2), suggesting that B31 may produce more of these two proteins than the other Erp proteins. As noted above, very few of the bacteria in the infectious B31 culture contain cp32-2 (which encodes ErpD), and the lack of ErpD-specific antibodies correlates with this observation. Sera from uninfected mice did not contain antibodies that recognized any Erp protein (data not shown). These data are consistent with production of the Erp proteins by B. burgdorferi during early stages of mammalian infection. We cannot at this time rule out antibody cross-reactivity in the preceding experiment. For example, most of the bacteria in the infectious B31 culture also lack the erpC gene (encoded on cp32-2), yet sera from infected mice recognized the recombinant ErpC protein (Fig. 2), probably due to cross-reactive antibodies elicited by ErpA/I. These two proteins share extensive sequence identity (>83% identical amino acids) (43), and antibodies that recognize one protein may recognize the other, since antibodies raised against a recombinant N40 OspE protein (27) recognized both the recombinant ErpA/I and ErpC proteins (data not shown).
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Differential synthesis of Erp antigens. We have previously reported that raising the culture temperature from 23 to 35°C resulted in the increased production of several antigenic B31 proteins (42). Knowing that expression of the erp genes can be temperature induced and that their proteins are antigenic, we performed experiments to determine whether any of the previously detected temperature-induced B31 antigens were Erp proteins. Due to the limited amount of serum available from a single mouse, sera from three of the infected mice described above were pooled for use in these experiments. The pooled sera were preadsorbed with each recombinant Erp protein and used in immunoblot analyses with a B31 lysate that had been grown at 23°C and shifted to 35°C. The absence of a signal with an Erp preadsorbed serum would indicate that a particular immunoblot band corresponded with that Erp protein.
These experiments indicated that at least two of the major B31 antigens detectable on immunoblots are Erp proteins. Preadsorption of the sera with recombinant ErpA/I protein inhibited binding to a protein with an approximate molecular mass of 19 kDa (Fig. 3), indicating that this differentially expressed antigen was ErpA/I. Binding to ErpA/I was not blocked by preincubation with recombinant ErpC, which shares 83% identical amino acids with ErpA/I (43), indicating that the infected animals also produced antibodies against epitopes unique to ErpA/I. Preadsorption with recombinant ErpB2/J blocked antibody binding to an approximately 60-kDa differentially expressed protein, indicating that this antigen is ErpB2/J. The ErpB2/J protein is predicted to have a molecular mass of 43.6 kDa but, as noted above, the recombinant ErpB2/J protein also migrated with a larger apparent molecular mass in polyacrylamide gel electrophoresis (Fig. 2).
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Recognition of B31 Erp proteins by human Lyme disease patient sera. We next analyzed sera from 10 humans with Lyme disease to determine whether they produced antibodies that recognized the B31 Erp proteins. All 10 patients contained antibodies that recognized the B. burgdorferi BmpA (P39) protein, a characteristic marker of B. burgdorferi infection (35, 37) (data not shown). All of the sera contained antibodies that bound both ErpA/I and ErpC (Table 3). Eight of the patients contained antibodies that recognized ErpB2, seven recognized ErpM, and six recognized ErpL. The remaining Erp proteins were bound by antibodies found in half or fewer of the patients. Sera from humans without Lyme disease and residing in an area where Lyme disease is not endemic lacked antibodies that recognized any of the recombinant B31 Erp proteins (data not shown). These data suggest that production of antigens similar to ErpA/I and ErpC may be common in Lyme disease spirochetes, while fewer bacteria produce antigens similar to the other B31 Erp proteins.
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DISCUSSION |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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We have found that B. burgdorferi B31 contains a large repertoire of erp genes and proteins. Expression from the B31 erp loci tested increased in response to a culture temperature shift that mimicked the environmental change within the feeding tick. Additionally, animals infected by tick bite produced antibodies that recognized the Erp proteins encoded by infectious B31. These data are consistent with production of the Erp proteins during the transmission of B. burgdorferi from ticks to mammals and suggest that they may play roles in transmission or the establishment of mammalian infection. Further studies will determine the pattern of Erp protein synthesis within unfed and fed ticks and in infected mammals.
It has been proposed that each of the numerous erp genes may be expressed at different times during mammalian infection (13, 25, 43), perhaps as a method of avoiding immune clearance similar to the presumed function of Vmp protein variation in the relapsing fever agent, Borrelia hermsii (4). Our data suggest that all of the B31 Erp proteins examined are synthesized at approximately the same time during infection, as they were recognized by antisera from tick-infected mice within the first 4 weeks of infection. It may be argued that only a subset of the erp genes were expressed during the infection times studied, and we actually detected antibodies that cross-reacted with the other Erp proteins. Yet such cross-reactivity could negate any value in sequentially producing the Erp proteins, since protective antibodies that recognize the later-appearing proteins might already be present. The identity of the B31 erpAB2 and erpIJ genes also argues against the theory of sequential expression of the erp loci. Additionally, the conserved 5' noncoding regions of these regulons (1, 11, 23, 25, 41, 43, 44, 46) indicate that the same regulatory factors probably interact with all of their promoters, suggesting that expression of these loci would not be individually controlled.
The in vitro expression of the B31 erp genes that we have observed stands in contrast with reports that Erp homologs of other B. burgdorferi isolates were not expressed in cultured bacteria (1, 13, 44, 46). The promoter regions of all reported erp homologs are nearly identical, which, as noted above, indicates that they are all probably regulated by the same cis and trans factors. The apparently contradictory in vitro expression patterns may be a consequence of the culture conditions used in different experiments, since the other reports studied protein synthesis in bacteria grown continuously at 35°C but not in cultures shifted from 23 to 35°C. It is important, however, that regulated expression of the B. burgdorferi erp genes can be observed in the laboratory, as the bacterial factors responsible might now be detected and studied in detail.
Not all of the Erp proteins are essential for mammalian infection, as bacteria lacking cp32-2 (which encodes ErpC and ErpD) are apparently infectious and transmitted between ticks and mammals. Most, if not all, of the Erp proteins are dispensable for growth of B. burgdorferi in culture, since a high-passage-number clone of B31 contains only cp32-1, cp32-3, and cp32-4, with a mutated erpB gene (11, 43). The truncated erpB1 allele found in the high-passage-number bacteria (43) also demonstrates that these bacteria can acquire small mutations during cultivation in addition to the previously described loss of plasmids (3, 9, 10, 33, 36, 47), any of which may contribute to the concurrent loss of infectivity.
The ErpA/I and ErpB2/J proteins elicited a strong immune response in animals infected with B31. The ErpA/I and ErpC proteins were also recognized as antigens by sera from 10 of 10 Lyme disease patients from Long Island, while 8 patients' sera also recognized the ErpB2/J protein. These data suggest that structural features of at least some of the B31 Erp proteins may be conserved among different B. burgdorferi bacteria and may be involved in essential functions. Epitope conservation also suggests that some B31 Erp proteins could serve as useful Lyme disease diagnostic antigens or components of a protective vaccine. Analysis of sera from Lyme disease patients from other geographic locations will indicate whether the production of antigens similar to the B31 Erp proteins is common in other infectious B. burgdorferi bacteria.
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ACKNOWLEDGMENTS |
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We thank Martine Bos, Alan MacDonald, and Erol Fikrig for providing sera, Kit Tilly, Joseph Hinnebusch, Stephen Porcella, and Abdallah Elias for constructive comments on the manuscript, Gary Hettrick and Robert Evans for artwork, and Kelly Matteson and Carole Smaus for secretarial assistance.
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FOOTNOTES |
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* Corresponding author. Present address: Department of Microbiology and Immunology, MS 415 UKMC, University of Kentucky College of Medicine, Lexington, KY 40536. Phone: (606) 323-8967. Fax: (606) 257-8994. E-mail: lkspic00{at}pop.uky.edu.
Editor: J. G. Cannon
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REFERENCES |
|---|
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
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| 1. | Akins, D. R., S. F. Porcella, T. G. Popova, D. Shevchenko, S. I. Baker, M. Li, M. V. Norgard, and J. D. Radolf. 1995. Evidence for in vivo but not in vitro expression of a Borrelia burgdorferi outer surface protein F (OspF) homologue. Mol. Microbiol. 18:507-520[Medline]. |
| 2. | Amouriaux, P., M. Assous, D. Margarita, G. Baranton, and I. Saint Girons. 1993. Polymerase chain reaction with the 30-kb circular plasmid of Borrelia burgdorferi B31 as a target for detection of the Lyme borreliosis agents in cerebrospinal fluid. Res. Microbiol. 144:211-219[Medline]. |
| 3. |
Barbour, A. G.
1988.
Plasmid analysis of Borrelia burgdorferi, the Lyme disease agent.
J. Clin. Microbiol.
26:475-478 |
| 4. |
Barbour, A. G.,
S. L. Tessier, and H. G. Stoenner.
1982.
Variable major proteins of Borrelia hermsii.
J. Exp. Med.
156:1312-1324 |
| 5. | Benach, J. L., J. L. Coleman, R. A. Skinner, and E. M. Bosler. 1987. Adult Ixodes dammini on rabbits: a hypothesis for the development and transmission of Borrelia burgdorferi. J. Infect. Dis. 155:1300-1306[Medline]. |
| 6. |
Bölin, I.,
D. A. Portnoy, and H. Wolf-Watz.
1985.
Expression of the temperature-inducible outer membrane proteins of yersiniae.
Infect. Immun.
48:234-240 |
| 7. |
Bono, J. L.,
K. Tilly,
B. Stevenson,
D. Hogan, and P. Rosa.
1998.
Oligopeptide permease in Borrelia burgdorferi: putative peptide-binding components encoded by both chromosomal and plasmid loci.
Microbiology
144:1033-1044 |
| 8. |
Burgdorfer, W.,
A. G. Barbour,
S. F. Hayes,
J. L. Benach,
E. Grunwaldt, and J. P. Davis.
1982.
Lyme disease a tick-borne spirochetosis?
Science
216:1317-1319 |
| 9. | Busch, U., G. Will, C. Hizo-Teufel, B. Wilske, and V. Preac-Mursic. 1997. Long term in vitro cultivation of Borrelia burgdorferi sensu lato strains: influence on plasmid patterns, genome stability and expression of proteins. Res. Microbiol. 148:109-118[Medline]. |
| 10. | Carroll, J. A., and F. C. Gherardini. 1996. Membrane protein variations associated with in vitro passage of Borrelia burgdorferi. Infect. Immun. 64:392-398[Abstract]. |
| 11. |
Casjens, S.,
R. van Vugt,
K. Tilly,
P. A. Rosa, and B. Stevenson.
1997.
Homology throughout the multiple 32-kilobase circular plasmids present in Lyme disease spirochetes.
J. Bacteriol.
179:217-227 |
| 12. | Coleman, J. L., J. A. Gebbia, J. Piesman, J. L. Degen, T. H. Bugge, and J. L. Benach. 1997. Plasminogen is required for efficient dissemination of B. burgdorferi in ticks and for enhancement of spirochetemia in mice. Cell 89:1111-1119[Medline]. |
| 13. | Das, S., S. W. Barthold, S. Stocker Giles, R. R. Montgomery, S. R. Telford, and E. Fikrig. 1997. Temporal pattern of Borrelia burgdorferi p21 expression in ticks and the mammalian host. J. Clin. Invest. 99:987-995[Medline]. |
| 14. | de Silva, A. M., and E. Fikrig. 1995. Growth and migration of Borrelia burgdorferi in Ixodes ticks during blood feeding. Am. J. Trop. Med. Hyg. 53:397-404. |
| 15. |
de Silva, A. M.,
S. R. Telford III,
L. R. Brunet,
S. W. Barthold, and E. Fikrig.
1996.
Borrelia burgdorferi OspA is an arthropod-specific transmission-blocking Lyme disease vaccine.
J. Exp. Med.
183:271-275 |
| 16. | Fingerle, V., U. Hauser, G. Liegl, B. Petko, V. Preac-Mursic, and B. Wilske. 1995. Expression of outer surface proteins A and C of Borrelia burgdorferi in Ixodes ricinus. J. Clin. Microbiol. 33:1867-1869[Abstract]. |
| 17. | Fraser, C. M., S. Casjens, W. M. Huang, G. G. Sutton, R. Clayton, R. Lathigra, O. White, K. A. Ketchum, R. Dodson, E. K. Hickey, M. Gwinn, B. Dougherty, J.-F. Tomb, R. D. Fleischmann, D. Richardson, J. Peterson, A. R. Kerlavage, J. Quackenbush, S. Salzberg, M. Hanson, R. van Vugt, N. Palmer, M. D. Adams, J. Gocayne, J. Weidmann, T. Utterback, L. Watthey, L. McDonald, P. Artiach, C. Bowman, S. Garland, C. Fujii, M. D. Cotton, K. Horst, K. Roberts, B. Hatch, H. O. Smith, and J. C. Venter. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586[Medline]. |
| 18. | Fuchs, R., S. Jauris, F. Lottspeich, V. Preac-Mursic, B. Wilske, and E. Soutschek. 1992. Molecular analysis and expression of a Borrelia burgdorferi gene encoding a 22kDa protein (pC) in Escherichia coli. Mol. Microbiol. 6:503-509[Medline]. |
| 19. | Gern, L., Z. Zhu, and A. Aeschlimann. 1990. Development of Borrelia burgdorferi in Ixodes ricinus females during blood feeding. Ann. Parasitol. Hum. Comp. 65:89-93. |
| 20. | Hinnebusch, B. J., R. D. Perry, and T. G. Schwan. 1996. Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas. Science 273:367-370[Abstract]. |
| 21. |
King, G. J., and J. Swanson.
1978.
Studies on gonococcus infection. XV. Identification of surface proteins of Neisseria gonorrhoeae correlated with leukocyte association.
Infect. Immun.
21:575-584 |
| 22. |
Kurtti, T. J.,
U. G. Munderloh,
R. C. Johnson, and G. G. Ahlstrand.
1987.
Colony formation and morphology in Borrelia burgdorferi.
J. Clin. Microbiol.
25:2054-2058 |
| 23. |
Lam, T. T.,
T.-P. K. Nguyen,
R. R. Montgomery,
F. S. Kantor,
E. Fikrig, and R. A. Flavell.
1994.
Outer surface proteins E and F of Borrelia burgdorferi, the agent of Lyme disease.
Infect. Immun.
62:290-298 |
| 24. | Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. In Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y. |
| 25. |
Marconi, R. T.,
S. Y. Sung,
C. A. Norton Hughes, and J. A. Carlyon.
1996.
Molecular and evolutionary analyses of a variable series of genes in Borrelia burgdorferi that are related to ospE and ospF, constitute a gene family, and share a common upstream homology box.
J. Bacteriol.
178:5615-5626 |
| 26. |
Miller, J. F.,
J. J. Mekalanos, and S. Falkow.
1989.
Coordinate regulation and sensory transduction in the control of bacterial virulence.
Science
243:916-922 |
| 27. |
Nguyen, T.-P. K.,
T. T. Lam,
S. W. Barthold,
S. R. Telford III,
R. A. Flavell, and E. Fikrig.
1994.
Partial destruction of Borrelia burgdorferi within ticks that engorged on OspE- or OspF-immunized mice.
Infect. Immun.
62:2079-2084 |
| 28. | Piesman, J., J. R. Oliver, and R. J. Sinsky. 1990. Growth kinetics of the Lyme disease spirochete (Borrelia burgdorferi) in vector ticks (Ixodes dammini). Am. J. Trop. Med. Hyg. 42:352-357. |
| 29. |
Porcella, S. F.,
T. G. Popova,
D. R. Akins,
M. Li,
J. D. Radolf, and M. V. Norgard.
1996.
Borrelia burgdorferi supercoiled plasmids encode multicopy tandem open reading frames and a lipoprotein gene family.
J. Bacteriol.
178:3293-3307 |
| 30. | Ribeiro, J. M. C., T. N. Mather, J. Piesman, and A. Spielman. 1987. Dissemination and salivary delivery of Lyme disease spirochetes in vector ticks (Acari: Ixodidae). J. Med. Entomol. 24:201-205[Medline]. |
| 31. |
Rosa, P.,
D. S. Samuels,
D. Hogan,
B. Stevenson,
S. Casjens, and K. Tilly.
1996.
Directed insertion of a selectable marker into a circular plasmid of Borrelia burgdorferi.
J. Bacteriol.
178:5946-5953 |
| 32. | Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. In Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y. |
| 33. |
Schwan, T. G.,
W. Burgdorfer, and C. F. Garon.
1988.
Changes in infectivity and plasmid profile of the Lyme disease spirochete, Borrelia burgdorferi, as a result of in vitro cultivation.
Infect. Immun.
56:1831-1836 |
| 34. |
Schwan, T. G.,
J. Piesman,
W. T. Golde,
M. C. Dolan, and P. A. Rosa.
1995.
Induction of an outer surface protein on Borrelia burgdorferi during tick feeding.
Proc. Natl. Acad. Sci. USA
92:2909-2913 |
| 35. |
Simpson, W. J.,
W. Burgdorfer,
M. E. Schrumpf,
R. H. Karstens, and T. G. Schwan.
1991.
Antibody to a 39-kilodalton Borrelia burgdorferi antigen (P39) as a marker for infection in experimentally and naturally inoculated animals.
J. Clin. Microbiol.
29:236-243 |
| 36. | Simpson, W. J., C. F. Garon, and T. G. Schwan. 1990. Analysis of supercoiled circular plasmids in infectious and non-infectious Borrelia burgdorferi. Microb. Pathog. 8:109-118[Medline]. |
| 37. |
Simpson, W. J.,
M. E. Schrumpf, and T. G. Schwan.
1990.
Reactivity of human Lyme borreliosis sera with a 39-kilodalton antigen specific to Borrelia burgdorferi.
J. Clin. Microbiol.
28:1329-1337 |
| 38. | Spencer, R. R., and R. R. Parker. 1923. Rocky mountain spotted fever: infectivity of fasting and recently fed ticks. Public Health Rep. 38:333-339. |
| 39. | Spencer, R. R., and R. R. Parker. 1924. Rocky mountain spotted fever: experimental studies on tick virus. Public Health Rep. 39:3027-3040. |
| 40. | Stevenson, B., S. Casjens, and P. Rosa. Evidence of past recombination events among the genes encoding the Erp antigens of Borrelia burgdorferi. Microbiology, in press. |
| 41. |
Stevenson, B.,
S. Casjens,
R. van Vugt,
S. F. Porcella,
K. Tilly,
J. L. Bono, and P. Rosa.
1997.
Characterization of cp18, a naturally truncated member of the cp32 family of Borrelia burgdorferi plasmids.
J. Bacteriol.
179:4285-4291 |
| 42. | Stevenson, B., T. G. Schwan, and P. A. Rosa. 1995. Temperature-related differential expression of antigens in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 63:4535-4539[Abstract]. |
| 43. |
Stevenson, B.,
K. Tilly, and P. A. Rosa.
1996.
A family of genes located on four separate 32-kilobase circular plasmids in Borrelia burgdorferi B31.
J. Bacteriol.
178:3508-3516 |
| 44. |
Suk, K.,
S. Das,
W. Sun,
B. Jwang,
S. W. Barthold,
R. A. Flavell, and E. Fikrig.
1995.
Borrelia burgdorferi genes selectively expressed in the infected host.
Proc. Natl. Acad. Sci. USA
92:4269-4273 |
| 45. | Tilly, K., S. Casjens, B. Stevenson, J. L. Bono, D. S. Samuels, D. Hogan, and P. Rosa. 1997. The Borrelia burgdorferi circular plasmid cp26: conservation of plasmid structure and targeted inactivation of the ospC gene. Mol. Microbiol. 25:361-373[Medline]. |
| 46. | Wallich, R., C. Brenner, M. D. Kramer, and M. M. Simon. 1995. Molecular cloning and immunological characterization of a novel linear-plasmid-encoded gene, pG, of Borrelia burgdorferi expressed only in vivo. Infect. Immun. 63:3327-3335[Abstract]. |
| 47. | Xu, Y., C. Kodner, L. Coleman, and R. C. Johnson. 1996. Correlation of plasmids with infectivity of Borrelia burgdorferi sensu stricto type strain B31. Infect. Immun. 64:3870-3876[Abstract]. |
| 48. | Zückert, W. R., E. Filipuzzi-Jenny, J. Meister-Turner, M. Stålhammar-Carlemalm, and J. Meyer. 1994. Repeated DNA sequences on circular and linear plasmids of Borrelia burgdorferi sensu lato, p. 253-260. In J. S. Axford, and D. H. E. Rees (ed.), Lyme borreliosis. Plenum Press, New York, N.Y. |
| 49. |
Zückert, W. R., and J. Meyer.
1996.
Circular and linear plasmids of Lyme disease spirochetes have extensive homology: characterization of a repeated DNA element.
J. Bacteriol.
178:2287-2298 |
| 50. | Zung, J. L., S. Lewengrub, M. A. Rudzinska, A. Spielman, S. R. Telford, and J. Piesman. 1989. Fine structural evidence for the penetration of the Lyme disease spirochete Borrelia burgdorferi through the gut and salivary tissues of Ixodes dammini. Can. J. Zool. 67:1737-1748. |
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[Abstract] [Full Text] -
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[Abstract] [Full Text] -
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[Abstract] [Full Text] -
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[Abstract] [Full Text] -
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68: 4169-4173
[Abstract] [Full Text] -
Haake, D. A.
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146: 1491-1504
[Full Text] -
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[Abstract] [Full Text] -
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[Abstract] [Full Text] -
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[Abstract] [Full Text] -
Indest, K. J., Philipp, M. T.
(2000). DNA-Binding Proteins Possibly Involved in Regulation of the Post-Logarithmic-Phase Expression of Lipoprotein P35 in Borrelia burgdorferi. J. Bacteriol.
182: 522-525
[Abstract] [Full Text] -
Yang, X., Popova, T. G., Hagman, K. E., Wikel, S. K., Schoeler, G. B., Caimano, M. J., Radolf, J. D., Norgard, M. V.
(1999). Identification, Characterization, and Expression of Three New Members of the Borrelia burgdorferi Mlp (2.9) Lipoprotein Gene Family. Infect. Immun.
67: 6008-6018
[Abstract] [Full Text] -
Skare, J. T., Foley, D. M., Hernandez, S. R., Moore, D. C., Blanco, D. R., Miller, J. N., Lovett, M. A.
(1999). Cloning and Molecular Characterization of Plasmid-Encoded Antigens of Borrelia burgdorferi. Infect. Immun.
67: 4407-4417
[Abstract] [Full Text] -
Zuckert, W. R., Meyer, J., Barbour, A. G.
(1999). Comparative Analysis and Immunological Characterization of the Borrelia Bdr Protein Family. Infect. Immun.
67: 3257-3266
[Abstract] [Full Text] -
Obonyo, M., Munderloh, U. G., Fingerle, V., Wilske, B., Kurtti, T. J.
(1999). Borrelia burgdorferi in Tick Cell Culture Modulates Expression of Outer Surface Proteins A and C in Response to Temperature. J. Clin. Microbiol.
37: 2137-2141
[Abstract] [Full Text] -
El Hage, N., Lieto, L. D., Stevenson, B.
(1999). Stability of erp Loci during Borrelia burgdorferi Infection: Recombination Is Not Required for Chronic Infection of Immunocompetent Mice. Infect. Immun.
67: 3146-3150
[Abstract] [Full Text] -
Stevenson, B., Bono, J. L., Elias, A., Tilly, K., Rosa, P.
(1998). Transformation of the Lyme Disease Spirochete Borrelia burgdorferi with Heterologous DNA. J. Bacteriol.
180: 4850-4855
[Abstract] [Full Text]
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