HrpA, an RNA Helicase Involved in RNA Processing, Is Required for Mouse Infectivity and Tick Transmission of the Lyme Disease Spirochete

PLoS Pathogens

Volumn 9, Issue 12, 2013, Pages 1-16

  Salman Dilgimen, Aydan ^a   Hardy, Pierre Olivier ^a   Radolf, Justin D ^b   Caimano, Melissa J ^b   Chaconas, George ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HRPA PROTEIN; RNA HELICASE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; DISEASE TRANSMISSION; GENE EXPRESSION; LYME DISEASE; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NORTHERN BLOTTING; POINT MUTATION; PROTEIN EXPRESSION; RNA PROCESSING; SITE DIRECTED MUTAGENESIS; SPIROCHETE; TICK; ANIMAL; BORRELIA BURGDORFERI; C3H MOUSE; CELL CULTURE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IXODES; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; TRANSGENIC ORGANISM; VIRULENCE;

ANIMALS; BACTERIAL PROTEINS; BORRELIA BURGDORFERI; CELLS, CULTURED; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; IXODES; LYME DISEASE; MALE; MICE; MICE, INBRED C3H; ORGANISMS, GENETICALLY MODIFIED; RNA HELICASES; RNA PROCESSING, POST-TRANSCRIPTIONAL; VIRULENCE;

EID: 84892878516     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003841     Document Type: Article

References (75)

1. 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.
2. Stanek G, Wormser GP, Gray J, Strle F, (2012) Lyme borreliosis. Lancet 379: 461-473.
3. Skare JT, Carroll JA, X.F Y, Samuels DS, Akins DR (2010) Gene regulation, transcriptomics and proteomics. In: Samuels DS, Radolf JD, editors. Borrelia: Molecular Biology, Host Interaction and Pathogenesis. Norfolk, UK: Caister Academic Press. pp. 67-101.
4. Samuels DS, (2011) Gene Regulation in Borrelia burgdorferi. Annu Rev Microbiol.
5. Caimano MJ, Iyer R, Eggers CH, Gonzalez C, Morton EA, et al. (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. Fisher MA, Grimm D, Henion AK, Elias AF, Stewart PE, et al. (2005) Borrelia burgdorferi sigma54 is required for mammalian infection and vector transmission but not for tick colonization. Proc Natl Acad Sci U S A 102: 5162-5167.
7. Hubner A, Yang X, Nolen DM, Popova TG, Cabello FC, et al. (2001) Expression of Borrelia burgdorferi OspC and DbpA is controlled by a RpoN-RpoS regulatory pathway. Proc Natl Acad Sci U S A 98: 12724-12729.
8. 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.
9. Boardman BK, He M, Ouyang Z, Xu H, Pang X, et al. (2008) Essential role of the response regulator Rrp2 in the infectious cycle of Borrelia burgdorferi. Infect Immun 76: 3844-3853.
10. Blevins JS, Xu H, He M, Norgard MV, Reitzer L, et al. (2009) Rrp2, a sigma54-dependent transcriptional activator of Borrelia burgdorferi, activates rpoS in an enhancer-independent manner. J Bacteriol 191: 2902-2905.
11. Groshong AM, Gibbons NE, Yang XF, Blevins JS, (2012) Rrp2, a prokaryotic enhancer-like binding protein, is essential for viability of Borrelia burgdorferi. J Bacteriol 194: 3336-3342.
12. 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.
13. 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.
14. Guell M, Yus E, Lluch-Senar M, Serrano L, (2011) Bacterial transcriptomics: what is beyond the RNA horiz-ome? Nat Rev Microbiol 9: 658-669.
15. Gripenland J, Netterling S, Loh E, Tiensuu T, Toledo-Arana A, et al. (2010) RNAs: regulators of bacterial virulence. Nat Rev Microbiol 8: 857-866.
16. Papenfort K, Vogel J, (2010) Regulatory RNA in bacterial pathogens. Cell Host Microbe 8: 116-127.
17. Caron MP, Lafontaine DA, Masse E, (2010) Small RNA-mediated regulation at the level of transcript stability. RNA Biol 7: 140-144.
18. Frohlich KS, Vogel J, (2009) Activation of gene expression by small RNA. Curr Opin Microbiol 12: 674-682.
19. Lioliou E, Romilly C, Romby P, Fechter P, (2010) RNA-mediated regulation in bacteria: from natural to artificial systems. N Biotechnol 27: 222-235.
20. Lybecker MC, Samuels DS, (2007) Temperature-induced regulation of RpoS by a small RNA in Borrelia burgdorferi. Mol Microbiol 64: 1075-1089.
21. Lybecker MC, Abel CA, Feig AL, Samuels DS, (2010) Identification and function of the RNA chaperone Hfq in the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 78: 622-635.
22. Karna SL, Sanjuan E, Esteve-Gassent MD, Miller CL, Maruskova M, et al. (2011) CsrA modulates levels of lipoproteins and key regulators of gene expression critical for pathogenic mechanisms of Borrelia burgdorferi. Infect Immun 79: 732-744.
23. Sze CW, Li C, (2011) Inactivation of bb0184, which encodes carbon storage regulator A, represses the infectivity of Borrelia burgdorferi. Infect Immun 79: 1270-1279.
24. Hardwick SW, Luisi BF, (2012) Rarely at rest: RNA helicases and their busy contributions to RNA degradation, regulation and quality control. RNA Biol 10: 56-70.
25. Martin R, Straub AU, Doebele C, Bohnsack MT, (2012) DExD/H-box RNA helicases in ribosome biogenesis. RNA Biol 9.
26. Cordin O, Beggs JD, (2013) RNA helicases in splicing. RNA Biol 10.
27. Marintchev A, (2013) Roles of helicases in translation initiation: A mechanistic view. Biochim Biophys Acta 1829: 799-809.
28. Klostermeier D, (2013) Lifelong companions: RNA helicases and their roles in RNA metabolism. RNA Biol 10.
29. Kaberdin VR, Blasi U, (2013) Bacterial helicases in post-transcriptional control. Biochim Biophys Acta 1829: 878-883.
30. Steimer L, Klostermeier D, (2012) RNA helicases in infection and disease. RNA Biol 9: 751-771.
31. Jankowsky E, (2011) RNA helicases at work: binding and rearranging. Trends Biochem Sci 36: 19-29.
32. Moriya H, Kasai H, Isono K, (1995) Cloning and characterization of the hrpA gene in the terC region of Escherichia coli that is highly similar to the DEAH family RNA helicase genes of Saccharomyces cerevisiae. Nucleic Acids Res 23: 595-598.
33. Koo JT, Choe J, Moseley SL, (2004) HrpA, a DEAH-box RNA helicase, is involved in mRNA processing of a fimbrial operon in Escherichia coli. Mol Microbiol 52: 1813-1826.
34. Butland G, Peregrin-Alvarez JM, Li J, Yang W, Yang X, et al. (2005) Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433: 531-537.
35. Salman-Dilgimen A, Hardy P-O, Dresser AR, Chaconas G, (2011) HrpA, a DEAH-box RNA helicase, is a global regulator of gene expression in the Lyme disease spirochete. PLoS ONE 6: e22168.
36. Linder P, Jankowsky E, (2011) From unwinding to clamping- the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 12: 505-516.
37. Dethoff EA, Chugh J, Mustoe AM, Al-Hashimi HM, (2012) Functional complexity and regulation through RNA dynamics. Nature 482: 322-330.
38. Schneider S, Schwer B, (2001) Functional domains of the yeast splicing factor Prp22p. J Biol Chem 276: 21184-21191.
39. Lee CG, Hurwitz J, (1992) A new RNA helicase isolated from HeLa cells that catalytically translocates in the 3′ to 5′ direction. J Biol Chem 267: 4398-4407.
40. Utama A, Shimizu H, Morikawa S, Hasebe F, Morita K, et al. (2000) Identification and characterization of the RNA helicase activity of Japanese encephalitis virus NS3 protein. FEBS Lett 465: 74-78.
41. Schneider S, Hotz HR, Schwer B, (2002) Characterization of dominant-negative mutants of the DEAH-box splicing factors Prp22 and Prp16. J Biol Chem 277: 15452-15458.
42. Kim DW, Kim J, Gwack Y, Han JH, Choe J, (1997) Mutational analysis of the hepatitis C virus RNA helicase. J Virol 71: 9400-9409.
43. Gross CH, Shuman S, (1995) Mutational analysis of vaccinia virus nucleoside triphosphate phosphohydrolase II, a DExH box RNA helicase. J Virol 69: 4727-4736.
44. Schneider S, Campodonico E, Schwer B, (2004) Motifs IV and V in the DEAH box splicing factor Prp22 are important for RNA unwinding, and helicase-defective Prp22 mutants are suppressed by Prp8. J Biol Chem 279: 8617-8626.
45. Newton CR, Graham A, Heptinstall LE, Powell SJ, Summers C, et al. (1989) Analysis of any point mutation in DNA. The amplification refractory mutation system (ARMS). Nucleic Acids Res 17: 2503-2516.
46. Knight SW, Kimmel BJ, Eggers CH, Samuels DS, (2000) Disruption of the Borrelia burgdorferi gac gene, encoding the naturally synthesized GyrA C-terminal domain. J Bacteriol 182: 2048-2051.
47. Policastro PF, Schwan TG, (2003) Experimental infection of Ixodes scapularis larvae (Acari: Ixodidae) by immersion in low passage cultures of Borrelia burgdorferi. J Med Entomol 40: 364-370.
48. Dunham-Ems SM, Caimano MJ, Eggers CH, Radolf JD, (2012) Borrelia burgdorferi requires the alternative sigma factor RpoS for dissemination within the vector during tick-to-mammal transmission. PLoS Pathog 8: e1002532.
49. Tilly K, Bestor A, Jewett MW, Rosa P, (2007) Rapid clearance of Lyme disease spirochetes lacking OspC from skin. Infect Immun 75: 1517-1519.
50. Grimm D, Tilly K, Byram R, Stewart PE, Krum JG, et al. (2004) Outer-surface protein C of the Lyme disease spirochete: a protein induced in ticks for infection of mammals. Proc Natl Acad Sci U S A 101: 3142-3147.
51. Kim DW, Gwack Y, Han JH, Choe J, (1995) C-Terminal Domain of the Hepatitis C Virus NS3 Protein Contains an RNA Helicase Activity. Biochemical and Biophysical Research Communications 215: 160-166.
52. Tanaka N, Schwer B, (2005) Characterization of the NTPase, RNA-Binding, and RNA helicase activities of the DEAH-box splicing factor Prp22. Biochemistry 44: 9795-9803.
53. Gwack Y, Yoo H, Song I, Choe J, Han JH, (1999) RNA-Stimulated ATPase and RNA helicase activities and RNA binding domain of hepatitis G virus nonstructural protein 3. J Virol 73: 2909-2915.
54. Iost I, Dreyfus M, (2006) DEAD-box RNA helicases in Escherichia coli. Nucleic Acids Res 34: 4189-4197.
55. Perutka J, Wang W, Goerlitz D, Lambowitz AM, (2004) Use of computer-designed group II introns to disrupt Escherichia coli DExH/D-box protein and DNA helicase genes. J Mol Biol 336: 421-439.
56. de la Cruz J, Kressler D, Linder P, (1999) Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem Sci 24: 192-198.
57. Ristow LC, Miller HE, Padmore LJ, Chettri R, Salzman N, et al. (2012) The β3-integrin ligand of Borrelia burgdorferi is critical for infection of mice but not ticks. Mol Microbiol 85: 1105-1118.
58. Ouyang Z, Blevins JS, Norgard MV, (2008) Transcriptional interplay among the regulators Rrp2, RpoN and RpoS in Borrelia burgdorferi. Microbiology 154: 2641-2658.
59. Zhao X, Jain C, (2011) DEAD-box proteins from Escherichia coli exhibit multiple ATP-independent activities. J Bacteriol 193: 2236-2241.
60. Pappas CJ, Iyer R, Petzke MM, Caimano MJ, Radolf JD, et al. (2011) Borrelia burgdorferi requires glycerol for maximum fitness during the tick phase of the enzootic cycle. PLoS Pathog 7: e1002102.
61. He M, Ouyang Z, Troxell B, Xu H, Moh A, et al. (2011) Cyclic di-GMP is essential for the survival of the lyme disease spirochete in ticks. PLoS Pathog 7: e1002133.
62. Moriarty TJ, Chaconas G, (2009) Identification of the determinant conferring permissive substrate usage in the telomere resolvase, ResT. J Biol Chem 284: 23293-23301.
63. Bankhead T, Chaconas G, (2004) Mixing active site components: A recipe for the unique enzymatic activity of a telomere resolvase. Proc Natl Acad Sci USA 101: 13768-13773.
64. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
65. Barbour AG, (1984) Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57: 521-525.
66. Hardy P-O, Chaconas G, (2013) The nucleotide excision repair system of Borrelia burgdorferi is the sole pathway involved in repair of DNA damage by uv light. J Bacteriol 195: 2220-2231.
67. Samuels DS, (1995) Electrotransformation of the spirochete Borrelia burgdorferi. Methods Mol Biol 47: 253-259.
68. Bono JL, Elias AF, Kupko JJ III, Stevenson B, Tilly K, et al. (2000) Efficient targeted mutagenesis in Borrelia burgdorferi. J Bacteriol 182: 2445-2452.
69. Chen Q, Fischer JR, Benoit VM, Dufour NP, Youderian P, et al. (2008) In vitro CpG methylation increases the transformation efficiency of Borrelia burgdorferi strains harboring the endogenous linear plasmid lp56. J Bacteriol 190: 7885-7891.
70. Bunikis I, Kutschan-Bunikis S, Bonde M, Bergström S, (2011) Multiplex PCR as a tool for validating plasmid content of Borrelia burgdorferi. Journal of Microbiological Methods 86: 243-247.
71. 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.
72. Knight SW, Samuels DS, (1999) Natural synthesis of a DNA-binding protein from the C-terminal domain of DNA gyrase A in Borrelia burgdorferi. EMBO J 18: 4875-4881.
73. Mulay VB, Caimano MJ, Iyer R, Dunham-Ems S, Liveris D, et al. (2009) Borrelia burgdorferi bba74 is expressed exclusively during tick feeding and is regulated by both arthropod- and mammalian host-specific signals. J Bacteriol 191: 2783-2794.
74. Dresser AR, Hardy P-O, Chaconas G, (2009) Investigation of the role of DNA replication, recombination and repair genes in antigenic switching at the vlsE locus in Borrelia burgdorferi: an essential role for the RuvAB branch migrase. PLoS Pathogens 5: e1000680.
75. Caimano MJ, Kenedy MR, Kairu T, Desrosiers DC, Harman M, et al. (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.