Borrelia host adaptation Regulator (BadR) regulates rpoS to modulate host adaptation and virulence factors in Borrelia burgdorferi

Molecular Microbiology

Volumn 88, Issue 1, 2013, Pages 105-124

  Miller, Christine L ^a   Karna, S L Rajasekhar ^a   Seshu, J ^a  

^a UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BORRELIA HOST ADAPTATION REGULATOR PROTEIN; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RPOS; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ADAPTATION; ADAPTIVE BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BORRELIA BURGDORFERI; CONTROLLED STUDY; DNA BINDING; DOWN REGULATION; FEMALE; GENE EXPRESSION; HOST PATHOGEN INTERACTION; IMMUNOBLOTTING; IN VITRO STUDY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION REGULATION; UPREGULATION;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; BORRELIA BURGDORFERI; DOWN-REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHENOTYPE; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; SIGMA FACTOR; SPECIES SPECIFICITY; TICKS; UP-REGULATION; VIRULENCE FACTORS; XYLOSE;

BORRELIA; BORRELIA BURGDORFERI; IXODIDA; MUS; PYRONIA TITHONUS; SPIROCHAETES; VERTEBRATA;

EID: 84875626787     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12171     Document Type: Article

References (65)

1. Barbour, A.G., Burgdorfer, W., Grunwaldt, E., and Steere, A.C. (1983) Antibodies of patients with Lyme disease to components of the Ixodes dammini spirochete. J Clin Invest 72: 504-515.
2. Benson, M.J., Gawronski, J.D., Eveleigh, D.E., and Benson, D.R. (2004) Intracellular symbionts and other bacteria associated with deer ticks (Ixodes scapularis) from Nantucket and Wellfleet, Cape Cod, Massachusetts. Appl Environ Microbiol 70: 616-620.
3. Berg, T., Schild, S., and Reidl, J. (2007) Regulation of the chitobiose-phosphotransferase system in Vibrio cholerae. Arch Microbiol 187: 433-439.
4. Bugrysheva, J.V., Bryksin, A.V., Godfrey, H.P., and Cabello, F.C. (2005) Borrelia burgdorferi rel is responsible for generation of guanosine-3′-diphosphate-5′-triphosphate and growth control. Infect Immun 73: 4972-4981.
5. Caimano, M.J., Iyer, R., Eggers, C.H., Gonzalez, C., Morton, E.A., Gilbert, M.A., etal. (2007) Analysis of the RpoS regulon in Borrelia burgdorferi in response to mammalian host signals provides insight into RpoS function during the enzootic cycle. Mol Microbiol 65: 1193-1217.
6. Caimano, M.J., Kenedy, M.R., Kairu, T., Desrosiers, D.C., Harman, M., Dunham-Ems, S., etal. (2011) The hybrid histidine kinase Hk1 is part of a two-component system that is essential for survival of Borrelia burgdorferi in feeding Ixodes scapularis ticks. Infect Immun 79: 3117-3130.
7. CDC (2012) Summary of notifiable diseases - United States, 2010. MMWR Morb Mortal Wkly Rep 59: 1-111.
8. Dunham-Ems, S.M., Caimano, M.J., Eggers, C.H., and Radolf, J.D. (2012) Borrelia burgdorferi requires the alternative sigma factor RpoS for dissemination within the vector during tick-to-mammal transmission. PLoS Pathog 8: e1002532.
9. Edgar, R., Domrachev, M., and Lash, A.E. (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210.
10. Elias, A.F., Schmutzhard, J., Stewart, P.E., Schwan, T.G., and Rosa, P. (2002a) Population dynamics of a heterogeneous Borrelia burgdorferi B31 strain in an experimental mouse-tick infectious cycle. Wien Klin Wochenschr 114: 557-561.
11. Elias, A.F., Stewart, P.E., Grimm, D., Caimano, M.J., Eggers, C.H., Tilly, K., etal. (2002b) Clonal polymorphism of Borrelia burgdorferi strain B31 MI: implications for mutagenesis in an infectious strain background. Infect Immun 70: 2139-2150.
12. Esteve-Gassent, M.D., Elliott, N.L., and Seshu, J. (2009) sodA is essential for virulence of Borrelia burgdorferi in the murine model of Lyme disease. Mol Microbiol 71: 594-612.
13. Fikrig, E., and Narasimhan, S. (2006) Borrelia burgdorferi - traveling incognito? Microbes Infect 8: 1390-1399.
14. 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.
15. Grimm, D., Tilly, K., Byram, R., Stewart, P.E., Krum, J.G., Bueschel, D.M., etal. (2004) Outer-surface protein C of the Lyme disease spirochete: a protein induced in ticks for infection of mammals. Proc Natl Acad Sci USA 101: 3142-3147.
16. Hosono, K., Kakuda, H., and Ichihara, S. (1995) Decreasing accumulation of acetate in a rich medium by Escherichia coli on introduction of genes on a multicopy plasmid. Biosci Biotechnol Biochem 59: 256-261.
17. Hubner, A., Yang, X., Nolen, D.M., Popova, T.G., Cabello, F.C., and Norgard, M.V. (2001) Expression of Borrelia burgdorferi OspC and DbpA is controlled by a RpoN-RpoS regulatory pathway. Proc Natl Acad Sci USA 98: 12724-12729.
18. Hyde, J.A., Seshu, J., and Skare, J.T. (2006) Transcriptional profiling of Borrelia burgdorferi containing a unique bosR allele identifies a putative oxidative stress regulon. Microbiology 152: 2599-2609.
19. Ingram-Smith, C., Gorrell, A., Lawrence, S.H., Iyer, P., Smith, K., and Ferry, J.G. (2005) Characterization of the acetate binding pocket in the Methanosarcina thermophila acetate kinase. J Bacteriol 187: 2386-2394.
20. Jutras, B.L., Bowman, A., Brissette, C.A., Adams, C.A., Verma, A., Chenail, A.M., etal. (2012) EbfC (YbaB) is a new type of bacterial nucleoid-associated protein, and a global regulator of gene expression in the Lyme disease spirochete. J Bacteriol 194: 3395-3406.
21. Karna, S.L., Sanjuan, E., Esteve-Gassent, M.D., Miller, C.L., Maruskova, M., and Seshu, J. (2011) CsrA modulates levels of lipoproteins and key regulators of gene expression critical for pathogenic mechanisms of Borrelia burgdorferi. Infect Immun 79: 732-744.
22. 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.
23. Kimata, K., Inada, T., Tagami, H., and Aiba, H. (1998) A global repressor (Mlc) is involved in glucose induction of the ptsG gene encoding major glucose transporter in Escherichia coli. Mol Microbiol 29: 1509-1519.
24. von Lackum, K., and Stevenson, B. (2005) Carbohydrate utilization by the Lyme borreliosis spirochete, Borrelia burgdorferi. FEMS Microbiol Lett 243: 173-179.
25. Lybecker, M.C., and Samuels, D.S. (2007) Temperature-induced regulation of RpoS by a small RNA in Borrelia burgdorferi. Mol Microbiol 64: 1075-1089.
26. Ouyang, Z., Deka, R.K., and Norgard, M.V. (2011) BosR (BB0647) controls the RpoN-RpoS regulatory pathway and virulence expression in Borrelia burgdorferi by a novel DNA-binding mechanism. PLoS Pathog 7: e1001272.
27. Ouyang, Z., Narasimhan, S., Neelakanta, G., Kumar, M., Pal, U., Fikrig, E., etal. (2012) Activation of the RpoN-RpoS regulatory pathway during the enzootic life cycle of Borrelia burgdorferi. BMC Microbiol 12: 44.
28. Pal, U., Yang, X., Chen, M., Bockenstedt, L.K., Anderson, J.F., Flavell, R.A., etal. (2004) OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J Clin Invest 113: 220-230.
29. Pappas, C.J., Iyer, R., Petzke, M.M., Caimano, M.J., Radolf, J.D., and Schwartz, I. (2011) Borrelia burgdorferi requires glycerol for maximum fitness during the tick phase of the enzootic cycle. PLoS Pathog 7: e1002102.
30. Pennetier, C., Dominguez-Ramirez, L., and Plumbridge, J. (2008) Different regions of Mlc and NagC, homologous transcriptional repressors controlling expression of the glucose and N-acetylglucosamine phosphotransferase systems in Escherichia coli, are required for inducer signal recognition. Mol Microbiol 67: 364-377.
31. Plumbridge, J. (1995) Co-ordinated regulation of amino sugar biosynthesis and degradation: the NagC repressor acts as both an activator and a repressor for the transcription of the glmUS operon and requires two separated NagC binding sites. EMBO J 14: 3958-3965.
32. Plumbridge, J. (1996) How to achieve constitutive expression of a gene within an inducible operon: the example of the nagC gene of Escherichia coli. J Bacteriol 178: 2629-2636.
33. Plumbridge, J. (2001) Regulation of PTS gene expression by the homologous transcriptional regulators, Mlc and NagC, in Escherichia coli (or how two similar repressors can behave differently). J Mol Microbiol Biotechnol 3: 371-380.
34. Plumbridge, J. (2002) Regulation of gene expression in the PTS in Escherichia coli: the role and interactions of Mlc. Curr Opin Microbiol 5: 187-193.
35. Plumbridge, J., and Pellegrini, O. (2004) Expression of the chitobiose operon of Escherichia coli is regulated by three transcription factors: NagC, ChbR and CAP. Mol Microbiol 52: 437-449.
36. Plumbridge, J.A. (1991) Repression and induction of the nag regulon of Escherichia coli K-12: the roles of nagC and nagA in maintenance of the uninduced state. Mol Microbiol 5: 2053-2062.
37. Poncet, S., Milohanic, E., Maze, A., Nait Abdallah, J., Ake, F., Larribe, M., etal. (2009) Correlations between carbon metabolism and virulence in bacteria. Contrib Microbiol 16: 88-102.
38. Postma, P.W., Lengeler, J.W., and Jacobson, G.R. (1993) Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57: 543-594.
39. 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.
40. Raju, B.V., Esteve-Gassent, M.D., Karna, S.L., Miller, C.L., Van Laar, T.A., and Seshu, J. (2011) Oligopeptide permease A5 modulates vertebrate host-specific adaptation of Borrelia burgdorferi. Infect Immun 79: 3407-3420.
41. Rhodes, R.G., Coy, W., and Nelson, D.R. (2009) Chitobiose utilization in Borrelia burgdorferi is dually regulated by RpoD and RpoS. BMC Microbiol 9: 108.
42. Rhodes, R.G., Atoyan, J.A., and Nelson, D.R. (2010) The chitobiose transporter, chbC, is required for chitin utilization in Borrelia burgdorferi. BMC Microbiol 10: 21.
43. Rogers, E.A., Terekhova, D., Zhang, H.M., Hovis, K.M., Schwartz, I., and Marconi, R.T. (2009) Rrp1, a cyclic-di-GMP-producing response regulator, is an important regulator of Borrelia burgdorferi core cellular functions. Mol Microbiol 71: 1551-1573.
44. Samuels, D.S. (1995) Electrotransformation of the spirochete Borrelia burgdorferi. Methods Mol Biol 47: 253-259.
45. Samuels, D.S. (2011) Gene regulation in Borrelia burgdorferi. Annu Rev Microbiol 65: 479-499.
46. Sanjuan, E., Esteve-Gassent, M.D., Maruskova, M., and Seshu, J. (2009) Overexpression of CsrA (BB0184) alters the morphology and antigen profiles of Borrelia burgdorferi. Infect Immun 77: 5149-5162.
47. Schiefner, A., Gerber, K., Seitz, S., Welte, W., Diederichs, K., and Boos, W. (2005) The crystal structure of Mlc, a global regulator of sugar metabolism in Escherichia coli. J Biol Chem 280: 29073-29079.
48. Schneider, C.A., Rasband, W.S., and Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
49. Shin, D., Lim, S., Seok, Y.J., and Ryu, S. (2001) Heat shock RNA polymerase (E sigma(32)) is involved in the transcription of mlc and crucial for induction of the Mlc regulon by glucose in Escherichia coli. J Biol Chem 276: 25871-25875.
50. Smyth, G.K. (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
51. Sohanpal, B.K., Friar, S., Roobol, J., Plumbridge, J.A., and Blomfield, I.C. (2007) Multiple co-regulatory elements and IHF are necessary for the control of fimB expression in response to sialic acid and N-acetylglucosamine in Escherichia coli K-12. Mol Microbiol 63: 1223-1236.
52. Steere, A.C. (2006) Lyme borreliosis in 2005, 30 years after initial observations in Lyme Connecticut. Wien Klin Wochenschr 118: 625-633.
53. Stevenson, B., Zuckert, W.R., and Akins, D.R. (2000) Repetition, conservation, and variation: the multiple cp32 plasmids of Borrelia species. J Mol Microbiol Biotechnol 2: 411-422.
54. Strother, K.O., Broadwater, A., and De Silva, A. (2005) Plasmid requirements for infection of ticks by Borrelia burgdorferi. Vector Borne Zoonotic Dis 5: 237-245.
55. Sultan, S.Z., Pitzer, J.E., Miller, M.R., and Motaleb, M.A. (2010) Analysis of a Borrelia burgdorferi phosphodiesterase demonstrates a role for cyclic-di-guanosine monophosphate in motility and virulence. Mol Microbiol 77: 128-142.
56. Sze, C.W., and Li, C. (2011) Inactivation of bb0184, which encodes carbon storage regulator A, represses the infectivity of Borrelia burgdorferi. Infect Immun 79: 1270-1279.
57. Sze, C.W., Morado, D.R., Liu, J., Charon, N.W., Xu, H., and Li, C. (2011) Carbon storage regulator A (CsrA(Bb)) is a repressor of Borrelia burgdorferi flagellin protein FlaB. Mol Microbiol 82: 851-864.
58. Tanaka, Y., Kimata, K., and Aiba, H. (2000) A novel regulatory role of glucose transporter of Escherichia coli: membrane sequestration of a global repressor Mlc. EMBO J 19: 5344-5352.
59. Tilly, K., Elias, A.F., Errett, J., Fischer, E., Iyer, R., Schwartz, I., etal. (2001) Genetics and regulation of chitobiose utilization in Borrelia burgdorferi. J Bacteriol 183: 5544-5553.
60. Tilly, K., Grimm, D., Bueschel, D.M., Krum, J.G., and Rosa, P. (2004) Infectious cycle analysis of a Borrelia burgdorferi mutant defective in transport of chitobiose, a tick cuticle component. Vector Borne Zoonotic Dis 4: 159-168.
61. Titgemeyer, F., Reizer, J., Reizer, A., and Saier, M.H., Jr (1994) Evolutionary relationships between sugar kinases and transcriptional repressors in bacteria. Microbiology 140 (Part 9): 2349-2354.
62. Tokarz, R., Anderton, J.M., Katona, L.I., and Benach, J.L. (2004) Combined effects of blood and temperature shift on Borrelia burgdorferi gene expression as determined by whole genome DNA array. Infect Immun 72: 5419-5432.
63. Van Laar, T.A., Lin, Y.H., Miller, C.L., Karna, S.L., Chambers, J.P., and Seshu, J. (2012) Effect of levels of acetate on the mevalonate pathway of Borrelia burgdorferi. PLoS ONE 7: e38171.
64. Xu, Y., Bruno, J.F., and Luft, B.J. (2008) Profiling the humoral immune response to Borrelia burgdorferi infection with protein microarrays. Microb Pathog 45: 403-407.
65. Yang, X.F., Alani, S.M., and Norgard, M.V. (2003) The response regulator Rrp2 is essential for the expression of major membrane lipoproteins in Borrelia burgdorferi. Proc Natl Acad Sci USA 100: 11001-11006.