Outer-surface Protein C of the Lyme Disease Spirochete: a Protein Induced in Ticks for Infection of Mammals

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2004 Feb 19

PMID 14970347

Citations 251

Authors

Dorothee Grimm

Kit Tilly

Rebecca Byram

Philip E Stewart

Jonathan G Krum

Dawn M Bueschel

Tom G Schwan

Paul F Policastro

Abdallah F Elias

Patricia A Rosa

Affiliations

Soon will be listed here.

Abstract

Environmentally responsive synthesis of surface proteins represents a hallmark of the infectious cycle of the Lyme disease agent, Borrelia burgdorferi. Here we created and analyzed a B. burgdorferi mutant lacking outer-surface protein C (OspC), an abundant Osp that spirochetes normally synthesize in the tick vector during the blood meal and down-regulate after transmission to the mammal. We demonstrate that B. burgdorferi strictly requires OspC to infect mice but not to localize or migrate appropriately in the tick. The induction of a spirochetal virulence factor preceding the time and host in which it is required demonstrates a developmental sequence for transmission of this arthropod-borne pathogen.

Citing Articles

contributes to the virulence of in a murine model of Lyme disease.

Waldron C, George S, Thompson C, Liao Y, Ouyang Z Infect Immun. 2024; 93(1):e0045924.

PMID: 39679711 PMC: 11784157. DOI: 10.1128/iai.00459-24.

Borrelia PeptideAtlas: A proteome resource of common Borrelia burgdorferi isolates for Lyme research.

Reddy P, Sun Z, Wippel H, Baxter D, Swearingen K, Shteynberg D Sci Data. 2024; 11(1):1313.

PMID: 39622905 PMC: 11612207. DOI: 10.1038/s41597-024-04047-9.

Hitchhiker's Guide to .

Bourgeois J, Hu L J Bacteriol. 2024; 206(9):e0011624.

PMID: 39140751 PMC: 11411949. DOI: 10.1128/jb.00116-24.

The plasmid-encoded members of paralogous gene family 52 are dispensable to the enzootic cycle of .

Groshong A, Gibbons N, Moore B, Bellamy W, Blevins J Infect Immun. 2024; 92(10):e0021424.

PMID: 39120148 PMC: 11475691. DOI: 10.1128/iai.00214-24.

Suppression of host humoral immunity by varies over the course of infection.

Williams M, Zhang Y, Pulse M, Berg R, Allen M Infect Immun. 2024; 92(4):e0001824.

PMID: 38514468 PMC: 11003232. DOI: 10.1128/iai.00018-24.

References

Piesman J . Standard system for infecting ticks (Acari: Ixodidae) with the Lyme disease spirochete, Borrelia burgdorferi. J Med Entomol. 1993; 30(1):199-203. DOI: 10.1093/jmedent/30.1.199. View

Wooten R, Ma Y, Yoder R, Brown J, Weis J, Zachary J . Toll-like receptor 2 is required for innate, but not acquired, host defense to Borrelia burgdorferi. J Immunol. 2001; 168(1):348-55. DOI: 10.4049/jimmunol.168.1.348. View

MARGOLIS N, Hogan D, Cieplak Jr W, Schwan T, Rosa P . Homology between Borrelia burgdorferi OspC and members of the family of Borrelia hermsii variable major proteins. Gene. 1994; 143(1):105-10. DOI: 10.1016/0378-1119(94)90613-0. View

Carter C, Bergstrom S, Norris S, Barbour A . A family of surface-exposed proteins of 20 kilodaltons in the genus Borrelia. Infect Immun. 1994; 62(7):2792-9. PMC: 302883. DOI: 10.1128/iai.62.7.2792-2799.1994. View

Simpson W, Cieplak W, Schrumpf M, Barbour A, Schwan T . Nucleotide sequence and analysis of the gene in Borrelia burgdorferi encoding the immunogenic P39 antigen. FEMS Microbiol Lett. 1994; 119(3):381-7. DOI: 10.1111/j.1574-6968.1994.tb06917.x. View

MARGOLIS N, Hogan D, Tilly K, Rosa P . Plasmid location of Borrelia purine biosynthesis gene homologs. J Bacteriol. 1994; 176(21):6427-32. PMC: 196994. DOI: 10.1128/jb.176.21.6427-6432.1994. View

Schwan T, Piesman J, Golde W, Dolan M, Rosa P . Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc Natl Acad Sci U S A. 1995; 92(7):2909-13. PMC: 42328. DOI: 10.1073/pnas.92.7.2909. View

Montgomery R, Malawista S, Feen K, Bockenstedt L . Direct demonstration of antigenic substitution of Borrelia burgdorferi ex vivo: exploration of the paradox of the early immune response to outer surface proteins A and C in Lyme disease. J Exp Med. 1996; 183(1):261-9. PMC: 2192432. DOI: 10.1084/jem.183.1.261. View

de Silva A, Telford 3rd S, Brunet L, Barthold S, Fikrig E . Borrelia burgdorferi OspA is an arthropod-specific transmission-blocking Lyme disease vaccine. J Exp Med. 1996; 183(1):271-5. PMC: 2192397. DOI: 10.1084/jem.183.1.271. View

10.

Tilly K, Casjens S, Stevenson B, Bono J, Samuels D, Hogan D . The Borrelia burgdorferi circular plasmid cp26: conservation of plasmid structure and targeted inactivation of the ospC gene. Mol Microbiol. 1997; 25(2):361-73. DOI: 10.1046/j.1365-2958.1997.4711838.x. View

11.

Fraser C, Casjens S, Huang W, Sutton G, Clayton R, Lathigra R . Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature. 1997; 390(6660):580-6. DOI: 10.1038/37551. View

12.

Bono J, Tilly K, Stevenson B, Hogan D, Rosa P . Oligopeptide permease in Borrelia burgdorferi: putative peptide-binding components encoded by both chromosomal and plasmid loci. Microbiology (Reading). 1998; 144 ( Pt 4):1033-1044. DOI: 10.1099/00221287-144-4-1033. View

13.

Schwan T, Hinnebusch B . Bloodstream- versus tick-associated variants of a relapsing fever bacterium. Science. 1998; 280(5371):1938-40. DOI: 10.1126/science.280.5371.1938. View

14.

de Silva A, Zeidner N, Zhang Y, Dolan M, Piesman J, Fikrig E . Influence of outer surface protein A antibody on Borrelia burgdorferi within feeding ticks. Infect Immun. 1998; 67(1):30-5. PMC: 96273. DOI: 10.1128/IAI.67.1.30-35.1999. View

15.

Carroll J, Garon C, Schwan T . Effects of environmental pH on membrane proteins in Borrelia burgdorferi. Infect Immun. 1999; 67(7):3181-7. PMC: 116493. DOI: 10.1128/IAI.67.7.3181-3187.1999. View

16.

Mbow M, Gilmore Jr R, Titus R . An OspC-specific monoclonal antibody passively protects mice from tick-transmitted infection by Borrelia burgdorferi B31. Infect Immun. 1999; 67(10):5470-2. PMC: 96906. DOI: 10.1128/IAI.67.10.5470-5472.1999. View

17.

Gilmore Jr R, Piesman J . Inhibition of Borrelia burgdorferi migration from the midgut to the salivary glands following feeding by ticks on OspC-immunized mice. Infect Immun. 1999; 68(1):411-4. PMC: 97152. DOI: 10.1128/IAI.68.1.411-414.2000. View

18.

Schwan T, Piesman J . Temporal changes in outer surface proteins A and C of the lyme disease-associated spirochete, Borrelia burgdorferi, during the chain of infection in ticks and mice. J Clin Microbiol. 2000; 38(1):382-8. PMC: 88728. DOI: 10.1128/JCM.38.1.382-388.2000. View

19.

Kobryn K, Chaconas G . ResT, a telomere resolvase encoded by the Lyme disease spirochete. Mol Cell. 2002; 9(1):195-201. DOI: 10.1016/s1097-2765(01)00433-6. View

20.

Revel A, Talaat A, Norgard M . DNA microarray analysis of differential gene expression in Borrelia burgdorferi, the Lyme disease spirochete. Proc Natl Acad Sci U S A. 2002; 99(3):1562-7. PMC: 122230. DOI: 10.1073/pnas.032667699. View