Contributions of environmental signals and conserved residues to the functions of carbon storage regulator a of borrelia burgdorferi

Infection and Immunity

Volumn 81, Issue 8, 2013, Pages 2972-2985

  Rajasekhar Karna, S L ^a   Prabhu, Rajesh G ^a   Lin, Ying Han ^a   Miller, Christine L ^a   Seshu, J ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID DERIVATIVE; ACETYL COENZYME A; ALANINE; AMINO ACID; BACTERIAL PROTEIN; CARBON STORAGE REGULATOR A PROTEIN; MUTANT PROTEIN; PHOSPHATE ACETYLTRANSFERASE; SIGMA FACTOR RPON; SIGMA FACTOR RPOS; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BINDING SITE; BORRELIA BURGDORFERI; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; GEL MOBILITY SHIFT ASSAY; GENE DELETION; GENE SEQUENCE; GENETIC REGULATION; GENETIC TRANSCRIPTION; IMMUNE RESPONSE; MUTANT; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; REGULON; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; VERTEBRATE;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; BLOTTING, WESTERN; BORRELIA BURGDORFERI; CONSERVED SEQUENCE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PARASITE INTERACTIONS; MOLECULAR SEQUENCE DATA; REAL-TIME POLYMERASE CHAIN REACTION; TICKS;

EID: 84880695572     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00494-13     Document Type: Article

References (62)

1. Barbour AG. 1989. The molecular biology of Borrelia. Rev. Infect. Dis. 11(Suppl)6:S1470-S1474.
2. Samuels DS. 2011. Gene regulation in Borrelia burgdorferi. Annu. Rev. Microbiol. 65:479-499.
3. Radolf JD, Caimano MJ, Stevenson B, Hu LT. 2012. Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes. Nat. Rev. Microbiol. 10:87-99.
4. Miller CL, Karna SL, Seshu J. 2013. Borrelia host adaptation Regulator (BadR) regulates rpoS to modulate host adaptation and virulence factors in Borrelia burgdorferi. Mol. Microbiol. 88:105-124.
5. Babb K, El-Hage N, Miller JC, Carroll JA, Stevenson B. 2001. Distinct regulatory pathways control expression of Borrelia burgdorferi infection-associated OspC and Erp surface proteins. Infect. Immun. 69:4146-4153.
6. Brooks CS, Hefty PS, JolliffSE, Akins DR. 2003. Global analysis of Borrelia burgdorferi genes regulated by mammalian host-specific signals. Infect. Immun. 71:3371-3383.
7. Crowley JT, Toledo AM, LaRocca TJ, Coleman JL, London E, Benach JL. 2013. Lipid exchange between Borrelia burgdorferi and host cells. PLoS Pathog. 9:e1003109. doi: 10.1371/journal.ppat.1003109.
8. Caimano MJ, Eggers CH, Gonzalez CA, Radolf JD. 2005. Alternate sigma factor RpoSisrequired for the invivo-specific repression ofBorrelia burgdorferi plasmid lp54-borne ospA and lp6.6 genes. J. Bacteriol. 187: 7845-7852.
9. Caimano MJ, Eggers CH, Hazlett KR, Radolf JD. 2004. RpoS is not central to the general stress response in Borrelia burgdorferi but does control expression of one or more essential virulence determinants. Infect. Immun. 72:6433-6445.
10. Caimano MJ, Iyer R, Eggers CH, Gonzalez C, Morton EA, Gilbert MA, Schwartz I, Radolf JD. 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.
11. Caimano MJ, Kenedy MR, Kairu T, Desrosiers DC, Harman M, Dunham-Ems S, Akins DR, Pal U, Radolf JD. 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.
12. Tokarz R, Anderton JM, Katona LI, Benach JL. 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.
13. Ojaimi C, Brooks C, Casjens S, Rosa P, Elias A, Barbour A, Jasinskas A, Benach J, Katona L, Radolf J, Caimano M, Skare J, Swingle K, Akins D, Schwartz I. 2003. Profiling of temperature-induced changes in Borrelia burgdorferigene expression byusing whole genome arrays. Infect. Immun. 71:1689-1705.
14. Burtnick MN, Downey JS, Brett PJ, Boylan JA, Frye JG, Hoover TR, Gherardini FC. 2007. Insights into the complex regulation of rpoS in Borrelia burgdorferi. Mol. Microbiol. 65:277-293.
15. Lybecker MC, Abel CA, Feig AL, Samuels DS. 2010. Identification and function of the RNA chaperone Hfq in the Lyme disease spirochete Bor-relia burgdorferi. Mol. Microbiol. 78:622-635.
16. Lybecker MC, Samuels DS. 2007. Temperature-induced regulation of RpoS by a small RNA in Borrelia burgdorferi. Mol. Microbiol. 64:1075-1089.
17. Sultan SZ, Pitzer JE, Miller MR, Motaleb MA. 2010. Analysis of a Borrelia burgdorferi phosphodiesterase demonstrates a role for cyclic-di-guanosine monophosphate in motility and virulence. Mol. Microbiol. 77: 128-142.
18. He M, Oman T, Xu H, Blevins J, Norgard MV, Yang XF. 2008. Abrogation of ospAB constitutively activates the Rrp2-RpoN-RpoS pathway (sigmaN-sigmaS cascade) in Borrelia burgdorferi. Mol. Microbiol. 70: 1453-1464.
19. Pappas CJ, Iyer R, Petzke MM, Caimano MJ, Radolf JD, Schwartz I. 2011. Borrelia burgdorferi requires glycerol for maximum fitness during the tick phase of the enzootic cycle. PLoS Pathog. 7:e1002102. doi: 10.1371/journal.ppat.1002102.
20. Hübner A, Yang X, Nolen DM, Popova TG, Cabello FC, Norgard MV. 2001. Expression of Borrelia burgdorferiOspC and DbpA iscontrolled bya RpoN-RpoS regulatory pathway. Proc. Natl. Acad. Sci. U. S. A. 98:12724-12729.
21. Yang XF, Alani SM, Norgard MV. 2003. The response regulator Rrp2 is essential for the expression of major membrane lipoproteins in Borrelia burgdorferi. Proc. Natl. Acad. Sci. U. S. A. 100:11001-11006.
22. Boardman BK, He M, Ouyang Z, Xu H, Pang X, Yang XF. 2008. Essential role of the response regulator Rrp2 in the infectious cycle of Borrelia burgdorferi. Infect. Immun. 76:3844-3853.
23. Xu H, Caimano MJ, Lin T, He M, Radolf JD, Norris SJ, Gheradini F, Wolfe AJ, Yang XF. 2010. Role of acetyl-phosphate in activation of the Rrp2-RpoN-RpoS pathway in Borrelia burgdorferi. PLoS Pathog. 6:e1001104. doi :10.1371/journal.ppat.1001104.
24. Hyde JA, Shaw DK, Smith Iii R, Trzeciakowski JP, Skare JT. 2009. The BosR regulatory protein of Borrelia burgdorferi interfaces with the RpoS regulatory pathway and modulates both the oxidative stress response and pathogenic properties of the Lyme disease spirochete. Mol. Microbiol. 74:1344-1355.
25. Ouyang Z, Deka RK, Norgard MV. 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. doi :10.1371/journal.ppat.1001272.
26. Sze CW, Li C. 2011. Inactivation of bb0184, which encodes carbon storage regulator A, represses the infectivity of Borrelia burgdorferi. Infect. Im-mun. 79:1270-1279.
27. Van Laar TA, Lin YH, Miller CL, Karna SL, Chambers JP, Seshu J. 2012. Effect of levels of acetate on the mevalonate pathway of Borrelia burgdor-feri. PLoS One 7:e38171. doi: 10.1371/journal.pone.0038171.
28. Sanjuan E, Esteve-Gassent MD, Maruskova M, Seshu J. 2009. Overex-pression of CsrA (BB0184) alters the morphology and antigen profiles of Borrelia burgdorferi. Infect. Immun. 77:5149-5162.
29. Karna SL, Sanjuan E, Esteve-Gassent MD, Miller CL, Maruskova M, Seshu J. 2011. CsrA modulates levels of lipoproteins and key regulators of gene expression critical for pathogenic mechanisms of Borrelia burgdor-feri. Infect. Immun. 79:732-744.
30. Romeo T. 1998. Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol. Microbiol. 29:1321-1330.
31. Romeo T, Vakulskas CA, Babitzke P. 2013. Post-transcriptional regulation on a global scale: form and function of Csr/Rsm systems. Environ. Microbiol. 15:313-324.
32. Edwards AN, Patterson-Fortin LM, Vakulskas CA, Mercante JW, Pot-rykus K, Vinella D, Camacho MI, Fields JA, Thompson SA, Georgellis D, Cashel M, Babitzke P, Romeo T. 2011. Circuitry linking the Csr and stringent response global regulatory systems. Mol. Microbiol. 80:1561-1580.
33. Raju BV, Esteve-Gassent MD, Karna SL, Miller CL, Van Laar TA, Seshu J. 2011. Oligopeptide permease A5 modulates vertebrate host-specific adaptation of Borrelia burgdorferi. Infect. Immun. 79:3407-3420.
34. Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R, Lathigra R, White O, Ketchum KA, Dodson R, Hickey EK, Gwinn M, Dougherty B, Tomb JF, Fleischmann RD, Richardson D, Peterson J, Kerlavage AR, Quackenbush J, Salzberg S, Hanson M, van Vugt R, Palmer N, Adams MD, Gocayne J, Weidman J, Utterback T, Watthey L, McDonald L, Artiach P, Bowman C, Garland S, Fuji C, Cotton MD, Horst K, Roberts K, Hatch B, Smith HO, Venter JC. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
35. Mercante J, Edwards AN, Dubey AK, Babitzke P, Romeo T. 2009. Molecular geometry of CsrA (RsmA) binding to RNA and its implications for regulated expression. J. Mol. Biol. 392:511-528.
36. Mercante J, Suzuki K, Cheng X, Babitzke P, Romeo T. 2006. Comprehensive alanine-scanning mutagenesis of Escherichia coli CsrA defines two subdomains of critical functional importance. J. Biol. Chem. 281:31832-31842.
37. Ge Y, Old IG, Girons IS, Charon NW. 1997. The flgK motility operon of Borrelia burgdorferi is initiated by a sigma 70-like promoter. Microbiology 143(Pt 5):1681-1690.
38. Yakhnin H, Pandit P, Petty TJ, Baker CS, Romeo T, Babitzke P. 2007. CsrA of Bacillus subtilis regulates translation initiation of the gene encoding the flagellin protein (hag) by blocking ribosome binding. Mol. Micro-biol. 64:1605-1620.
39. Mukherjee S, Babitzke P, Kearns DB. 2013. FliW and FliS function independently to control cytoplasmic flagellin levels in Bacillus subtilis. J. Bacteriol. 195:297-306.
40. Mukherjee S, Yakhnin H, Kysela D, Sokoloski J, Babitzke P, Kearns DB. 2011. CsrA-FliW interaction governs flagellin homeostasis and a checkpoint on flagellar morphogenesis in Bacillus subtilis. Mol. Microbiol. 82: 447-461.
41. Sze CW, Morado DR, Liu J, Charon NW, Xu H, Li C. 2011. Carbon storage regulator A (CsrA(Bb)) isa repressor of Borrelia burgdorferi flagel-lin protein FlaB. Mol. Microbiol. 82:851-864.
42. Elias AF, Stewart PE, Grimm D, Caimano MJ, Eggers CH, Tilly K, Bono JL, Akins DR, Radolf JD, Schwan TG, Rosa P. 2002. Clonal polymorphism of Borrelia burgdorferi strain B31 MI: implications for mutagenesis in an infectious strain background. Infect. Immun. 70:2139-2150.
43. Samuels DS. 1995. Electrotransformation of the spirochete Borrelia burg-dorferi. Methods. Mol. Biol. 47:253-259.
44. Maruskova M, Esteve-Gassent MD, Sexton VL, Seshu J. 2008. Role of the BBA64 locus of Borrelia burgdorferi in early stages of infectivity in a murine model of Lyme disease. Infect. Immun. 76:391-402.
45. Maruskova M, Seshu J. 2008. Deletion of BBA64, BBA65, and BBA66 loci does not alter the infectivity of Borrelia burgdorferi in the murine model of Lyme disease. Infect. Immun. 76:5274-5284.
46. Esteve-Gassent MD, Elliott NL, Seshu J. 2009. sodA is essential for virulence of Borrelia burgdorferi in the murine model of Lyme disease. Mol. Microbiol. 71:594-612.
47. Seshu J, Boylan JA, Hyde JA, Swingle KL, Gherardini FC, Skare JT. 2004. A conservative amino acid change alters the function of BosR, the redox regulator of Borrelia burgdorferi. Mol. Microbiol. 54:1352-1363.
48. Seshu J, Esteve-Gassent MD, Labandeira-Rey M, Kim JH, Trzecia-kowski JP, Hook M, Skare JT. 2006. Inactivation of the fibronectin-binding adhesin gene bbk32 significantly attenuates the infectivity potential of Borrelia burgdorferi. Mol. Microbiol. 59:1591-1601.
49. Seshu J, Boylan JA, Gherardini FC, Skare JT. 2004. Dissolved oxygen levels alter gene expression and antigen profiles in Borrelia burgdorferi. Infect. Immun. 72:1580-1586.
50. Yang X, Goldberg MS, Popova TG, Schoeler GB, Wikel SK, Hagman KE, Norgard MV. 2000. Interdependence of environmental factors influencing reciprocal patterns of gene expression in virulent Borrelia burgdor-feri. Mol. Microbiol. 37:1470-1479.
51. Labandeira-Rey M, Seshu J, Skare JT. 2003. The absence of linear plas-mid 25 or 28-1 of Borrelia burgdorferi dramatically alters the kinetics of experimental infection via distinct mechanisms. Infect. Immun. 71:4608-4613.
52. Steere AC, Coburn J, Glickstein L. 2004. The emergence of Lyme disease. J. Clin. Invest. 113:1093-1101.
53. Rosa PA, Tilly K, Stewart PE. 2005. The burgeoning molecular genetics of the Lyme disease spirochaete. Nat. Rev. Microbiol. 3:129-143.
54. Dresser AR, Hardy PO, Chaconas G. 2009. Investigation of the genes involved in antigenic switching at the vlsE locus in Borrelia burgdorferi: an essential role for the RuvAB branch migrase. PLoS Pathog. 5:e1000680. doi: 10.1371/journal.ppat.1000680.
55. Lin T, Gao L, Edmondson DG, Jacobs MB, Philipp MT, Norris SJ. 2009. Central role of the Holliday junction helicase RuvAB in vlsE recombination and infectivity of Borrelia burgdorferi. PLoS Pathog. 5:e1000679. doi: 10.1371/journal.ppat.1000679.
56. Ouyang Z, Deka RK, Norgard MV. 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. doi :10.1371/journal.ppat.1001272.
57. Jutras BL, Bowman A, Brissette CA, Adams CA, Verma A, Chenail AM, Stevenson B. 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.
58. Jutras BL, Verma A, Adams CA, Brissette CA, Burns LH, Whetstine CR, Bowman A, Chenail AM, Zuckert WR, Stevenson B. 2012. BpaB and EbfC DNA-binding proteins regulate production of the Lyme disease spirochete's infection-associated Erp surface proteins. J. Bacteriol. 194:778-786.
59. Wolfe AJ. 2005. The acetate switch. Microbiol. Mol. Biol. Rev. 69:12-50.
60. Kumari S, Beatty CM, Browning DF, Busby SJ, Simel EJ, Hovel-Miner G, Wolfe AJ. 2000. Regulation of acetyl coenzyme A synthetase in Esche-richia coli. J. Bacteriol. 182:4173-4179.
61. Ristow LC, Miller HE, Padmore LJ, Chettri R, Salzman N, Caimano MJ, Rosa PA, Coburn J. 2012. The beta(3)-integrin ligand of Borrelia burg-dorferi is critical for infection of mice but not ticks. Mol. Microbiol. 85: 1105-1118.
62. Vogel J. 2009. A rough guide to the non-coding RNA world of Salmonella. Mol. Microbiol. 71:1-11.