Proteolysis of BB0323 results in two polypeptides that impact physiologic and infectious phenotypes in Borrelia burgdorferi

Molecular Microbiology

Volumn 88, Issue 3, 2013, Pages 510-522

  Kariu, Toru ^a   Yang, Xiuli ^a   Marks, Carolyn B ^b,c   Zhang, Xinyue ^a   Pal, Utpal ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF RICHMOND   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BINDING PROTEIN; MEMBRANE PROTEIN; POLYPEPTIDE; SERINE PROTEINASE;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL SURVIVAL; BORRELIA BURGDORFERI; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE PRODUCT; GENETIC CONSERVATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION;

ANIMALS; BACTERIAL PROTEINS; BLOTTING, WESTERN; BORRELIA BURGDORFERI; CLONING, MOLECULAR; IMMUNOPRECIPITATION; MICE; MICE, INBRED C3H; MUTAGENESIS, SITE-DIRECTED; PEPTIDES; PHENOTYPE; POLYMERASE CHAIN REACTION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; RECOMBINANT PROTEINS;

BORRELIA BURGDORFERI; MAMMALIA; SPIROCHAETA;

EID: 84876742059     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12202     Document Type: Article

References (44)

1. Beck, G., Benach, J.L., and Habicht, G.S. (1990) Isolation, preliminary chemical characterization, and biological activity of Borrelia burgdorferi peptidoglycan. Biochem Biophys Res Commun 167: 89-95.
2. Bergström, S., and Zückert, W.R. (2010) Structure, function and biogenesis of the Borrelia cell envelope. In Borrelia, Molecular Biology, Host Interaction and Pathogenesis. Samuels, D.S., and Radolf, J.D. (eds). Norfolk: Caister Academic Press, pp. 139-166.
3. Bernadac, A., Gavioli, M., Lazzaroni, J.C., Raina, S., and Lloubes, R. (1998) Escherichia coli tol-pal mutants form outer membrane vesicles. J Bacteriol 180: 4872-4878.
4. Buist, G., Kok, J., Leenhouts, K.J., Dabrowska, M., Venema, G., and Haandrikman, A.J. (1995) Molecular cloning and nucleotide sequence of the gene encoding the major peptidoglycan hydrolase of Lactococcus lactis, a muramidase needed for cell separation. J Bacteriol 177: 1554-1563.
5. Buist, G., Steen, A., Kok, J., and Kuipers, O.P. (2008) LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol Microbiol 68: 838-847.
6. Cascales, E., Bernadac, A., Gavioli, M., Lazzaroni, J.C., and Lloubes, R. (2002) Pal lipoprotein of Escherichia coli plays a major role in outer membrane integrity. J Bacteriol 184: 754-759.
7. Casjens, S., Palmer, N., van Vugt, R., Huang, W.M., Stevenson, B., Rosa, P., etal. (2000) A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 35: 490-516.
8. Casjens, S.R., Mongodin, E.F., Qiu, W.G., Dunn, J.J., Luft, B.J., Fraser-Liggett, C.M., and Schutzer, S.E. (2011) Whole-genome sequences of two Borrelia afzelii and two Borrelia garinii Lyme disease agent isolates. J Bacteriol 193: 6995-6996.
9. Charon, N.W., Cockburn, A., Li, C., Liu, J., Miller, K.A., Miller, M.R., etal. (2012) The unique paradigm of spirochete motility and chemotaxis. Annu Rev Microbiol 66: 349-370.
10. Clausen, T., Southan, C., and Ehrmann, M. (2002) The HtrA family of proteases: implications for protein composition and cell fate. Mol Cell 10: 443-455.
11. Clausen, T., Kaiser, M., Huber, R., and Ehrmann, M. (2011) HTRA proteases: regulated proteolysis in protein quality control. Nat Rev Mol Cell Biol 12: 152-162.
12. Eckert, C., Lecerf, M., Dubost, L., Arthur, M., and Mesnage, S. (2006) Functional analysis of AtlA, the major N-acetylglucosaminidase of Enterococcus faecalis. J Bacteriol 188: 8513-8519.
13. Elias, A.F., Stewart, P.E., Grimm, D., Caimano, M.J., Eggers, C.H., Tilly, K., etal. (2002) Clonal polymorphism of Borrelia burgdorferi strain B31 MI: implications for mutagenesis in an infectious strain background. Infect Immun 70: 2139-2150.
14. Ferris, H.U., Furukawa, Y., Minamino, T., Kroetz, M.B., Kihara, M., Namba, K., and Macnab, R.M. (2005) FlhB regulates ordered export of flagellar components via autocleavage mechanism. J Biol Chem 280: 41236-41242.
15. Frank, K.L., Bundle, S.F., Kresge, M.E., Eggers, C.E., and Samuels, D.S. (2003) aadA confers streptomycin resistance in Borrelia burgdorferi. J Bacteriol 185: 6723-6727.
16. Fraser, C.M., Casjens, S., Huang, W.M., Sutton, G.G., Clayton, R., Lathigra, R., etal. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390: 580-586.
17. Gerding, M.A., Ogata, Y., Pecora, N.D., Niki, H., and de Boer, P.A. (2007) The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli. Mol Microbiol 63: 1008-1025.
18. Grimm, D., Eggers, C.H., Caimano, M.J., Tilly, K., Stewart, P.E., Elias, A.F., etal. (2004) Experimental assessment of the roles of linear plasmids lp25 and lp28-1 of Borrelia burgdorferi throughout the infectious cycle. Infect Immun 72: 5938-5946.
19. Kenedy, M.R., Lenhart, T.R., and Akins, D.R. (2012) The role of Borrelia burgdorferi outer surface proteins. FEMS Immunol Med Microbiol 66: 1-19.
20. Kumar, M., Kaur, S., Kariu, T., Yang, X., Bossis, I., Anderson, J.F., and Pal, U. (2011) Borrelia burgdorferi BBA52 is a potential target for transmission blocking Lyme disease vaccine. Vaccine 29: 9012-9019.
21. Kung, F., Anguita, J., and Pal, U. (2013) Borrelia burgdorferi and tick proteins supporting pathogen persistence in the vector. Future Microbiol 8: 41-56.
22. Lazzaroni, J.C., Germon, P., Ray, M.C., and Vianney, A. (1999) The Tol proteins of Escherichia coli and their involvement in the uptake of biomolecules and outer membrane stability. FEMS Microbiol Lett 177: 191-197.
23. Llamas, M.A., Ramos, J.L., and Rodriguez-Herva, J.J. (2000) Mutations in each of the tol genes of Pseudomonas putida reveal that they are critical for maintenance of outer membrane stability. J Bacteriol 182: 4764-4772.
24. Loosmore, S.M., Yang, Y.P., Oomen, R., Shortreed, J.M., Coleman, D.C., and Klein, M.H. (1998) The Haemophilus influenzae HtrA protein is a protective antigen. Infect Immun 66: 899-906.
25. Meltzer, M., Hasenbein, S., Mamant, N., Merdanovic, M., Poepsel, S., Hauske, P., etal. (2009) Structure, function and regulation of the conserved serine proteases DegP and DegS of Escherichia coli. Res Microbiol 160: 660-666.
26. Merdanovic, M., Clausen, T., Kaiser, M., Huber, R., and Ehrmann, M. (2011) Protein quality control in the bacterial periplasm. Annu Rev Microbiol 65: 149-168.
27. Motaleb, M.A., Corum, L., Bono, J.L., Elias, A.F., Rosa, P., Samuels, D.S., and Charon, N.W. (2000) Borrelia burgdorferi periplasmic flagella have both skeletal and motility functions. Proc Natl Acad Sci USA 97: 10899-10904.
28. Ostberg, Y., Carroll, J.A., Pinne, M., Krum, J.G., Rosa, P., and Bergstrom, S. (2004) Pleiotropic effects of inactivating a carboxyl-terminal protease, CtpA, in Borrelia burgdorferi. J Bacteriol 186: 2074-2084.
29. Pal, U., Li, X., Wang, T., Montgomery, R.R., Ramamoorthi, N., Desilva, A.M., etal. (2004) TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell 119: 457-468.
30. Paster, B.J., Dewhirst, F.E., Weisburg, W.G., Tordoff, L.A., Fraser, G.J., Hespell, R.B., etal. (1991) Phylogenetic analysis of the spirochetes. J Bacteriol 173: 6101-6109.
31. Piesman, J., and Eisen, L. (2008) Prevention of tick-borne diseases. Annu Rev Entomol 53: 323-343.
32. Promnares, K., Kumar, M., Shroder, D.Y., Zhang, X., Anderson, J.F., and Pal, U. (2009) Borrelia burgdorferi small lipoprotein Lp6.6 is a member of multiple protein complexes in the outer membrane and facilitates pathogen transmission from ticks to mice. Mol Microbiol 74: 112-125.
33. Radolf, J.D., Caimano, M.J., Stevenson, B., and Hu, L.T. (2012) Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes. Nat Rev Microbiol 10: 87-99.
34. Samuels, D.S. (2011) Gene regulation in Borrelia burgdorferi. Annu Rev Microbiol 65: 479-499.
35. Schleifer, K.H., and Kandler, O. (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36: 407-477.
36. Schutzer, S.E., Fraser-Liggett, C.M., Casjens, S.R., Qiu, W.G., Dunn, J.J., Mongodin, E.F., and Luft, B.J. (2011) Whole-genome sequences of thirteen isolates of Borrelia burgdorferi. J Bacteriol 193: 1018-1020.
37. Steere, A.C., Coburn, J., and Glickstein, L. (2004) The emergence of Lyme disease. J Clin Invest 113: 1093-1101.
38. Stewart, P.E., Hoff, J., Fischer, E., Krum, J.G., and Rosa, P.A. (2004) Genome-wide transposon mutagenesis of Borrelia burgdorferi for identification of phenotypic mutants. Appl Environ Microbiol 70: 5973-5979.
39. Wei, W., Dorjsuren, D., Lin, Y., Qin, W., Nomura, T., Hayashi, N., and Murakami, S. (2001) Direct interaction between the subunit RAP30 of transcription factor IIF (TFIIF) and RNA polymerase subunit 5, which contributes to the association between TFIIF and RNA polymerase II. J Biol Chem 276: 12266-12273.
40. Yang, X., Coleman, A.S., Anguita, J., and Pal, U. (2009) A chromosomally encoded virulence factor protects the Lyme disease pathogen against host-adaptive immunity. PLoS Pathog 5: e1000326.
41. Yang, X., Lenhart, T.R., Kariu, T., Anguita, J., Akins, D.R., and Pal, U. (2010) Characterization of unique regions of Borrelia burgdorferi surface-located membrane protein 1. Infect Immun 78: 4477-4487.
42. Yang, X., Promnares, K., Qin, J., He, M., Shroder, D.Y., Kariu, T., etal. (2011) Characterization of multiprotein complexes of the Borrelia burgdorferi outer membrane vesicles. J Proteome Res 10: 4556-4566.
43. Yeh, Y.C., Comolli, L.R., Downing, K.H., Shapiro, L., and McAdams, H.H. (2012) The Caulobacter Tol-Pal complex is essential for outer membrane integrity and the positioning of a polar localization factor. J Bacteriol 192: 4847-4858.
44. Zhang, X., Yang, X., Kumar, M., and Pal, U. (2009) BB0323 function is essential for Borrelia burgdorferi virulence and persistence through tick-rodent transmission cycle. J Infect Dis 200: 1318-1330.