Molecular characterization of the Borrelia burgdorferi in vivo-essential protein PncA

Microbiology

Volumn 157, Issue 10, 2011, Pages 2831-2840

  Jewett, Mollie W ^a,b   Jain, Sunny ^b   Linowski, Angelika K ^b   Sarkar, Amit ^a   Rosa, Patricia A ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINAMIDASE; PROTEIN PNCA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BORRELIA BURGDORFERI; CATALYSIS; CHEMICAL ANALYSIS; CODON; CONTROLLED STUDY; GENETIC ANALYSIS; IN VIVO STUDY; MOLECULAR GENETICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROCESSING;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; BORRELIA BURGDORFERI; CODON; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; LYME DISEASE; MICE; MICE, INBRED C3H; MOLECULAR SEQUENCE DATA; NAD; NICOTINAMIDASE; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

BORRELIA BURGDORFERI; MAMMALIA; SPIROCHAETA;

EID: 80053459870     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.051706-0     Document Type: Article

References (51)

1. Anderson, R. M., Bitterman, K. J., Wood, J. G., Medvedik, O. & Sinclair, D. A. (2003). Nicotinamide and PNC1 govern lifespan extension by calorie restriction in Saccharomyces cerevisiae. Nature 423, 181-185.
2. Balan, V., Miller, G. S., Kaplun, L., Balan, K., Chong, Z. Z., Li, F., Kaplun, A., VanBerkum, M. F., Arking, R. & other authors (2008). Life span extension and neuronal cell protection by Drosophila nicotinamidase. J Biol Chem 283, 27810-27819.
3. Barbour, A. G. (1984). Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57, 521-525.
4. Bestor, A., Stewart, P. E., Jewett, M. W., Sarkar, A., Tilly, K. & Rosa, P. A. (2010). Use of the Cre-lox recombination system to investigate the lp54 gene requirement in the infectious cycle of Borrelia burgdorferi. Infect Immun 78, 2397-2407.
5. Binns, N. & Masters, M. (2002). Expression of the Escherichia coli pcnB gene is translationally limited using an inefficient start codon: a second chromosomal example of translation initiated at AUU. Mol Microbiol 44, 1287-1298.
6. Bono, J. L., Tilly, K., Stevenson, B., Hogan, D. & Rosa, P. (1998). Oligopeptide permease in Borrelia burgdorferi: putative peptide binding components encoded by both chromosomal and plasmid loci. Microbiology 144, 1033-1044.
7. Byram, R., Stewart, P. E. & Rosa, P. (2004). The essential nature of the ubiquitous 26-kilobase circular replicon of Borrelia burgdorferi. J Bacteriol 186, 3561-3569.
8. Cao, G. J. & Sarkar, N. (1992a). Identification of the gene for an Escherichia coli poly(A) polymerase. Proc Natl Acad Sci U S A 89, 10380-10384.
9. Cao, G. J. & Sarkar, N. (1992b). Poly(A) RNA in Escherichia coli: nucleotide sequence at the junction of the lpp transcript and the polyadenylate moiety. Proc Natl Acad Sci U S A 89, 7546-7550.
10. Casjens, S., Palmer, N., van Vugt, R., Huang, W. M., Stevenson, B., Rosa, P., Lathigra, R., Sutton, G., Peterson, J. & other authors (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.
11. Elias, A. F., Stewart, P. E., Grimm, D., Caimano, M. J., Eggers, C. H., Tilly, K., Bono, J. L., Akins, D. R., Radolf, J. D. & other authors (2002). Clonal polymorphism of Borrelia burgdorferi strain B31 MI: implications for mutagenesis in an infectious strain background. Infect Immun 70, 2139-2150.
12. Elias, A. F., Bono, J. L., Kupko, J. J., III, Stewart, P. E., Krum, J. G. & Rosa, P. A. (2003). New antibiotic resistance cassettes suitable for genetic studies in Borrelia burgdorferi. J Mol Microbiol Biotechnol 6, 29-40.
13. + metabolite levels as a function of vitamins and calorie restriction: evidence for different mechanisms of longevity. BMC Chem Biol 10, 2.
14. Fraser, C. M., Casjens, S., Huang, W. M., Sutton, G. G., Clayton, R., Lathigra, R., White, O., Ketchum, K. A., Dodson, R. & other authors (1997). Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390, 580-586.
15. French, J. B., Cen, Y., Vrablik, T. L., Xu, P., Allen, E., Hanna-Rose, W. & Sauve, A. A. (2010). Characterization of nicotinamidases: steady state kinetic parameters, classwide inhibition by nicotinaldehydes, and catalytic mechanism. Biochemistry 49, 10421-10439.
16. Frothingham, R., Meeker-O'Connell, W. A., Talbot, E. A., George, J. W. & Kreuzer, K. N. (1996). Identification, cloning, and expression of the Escherichia coli pyrazinamidase and nicotinamidase gene, pncA. Antimicrob Agents Chemother 40, 1426-1431.
17. Ghislain, M., Talla, E. & Franç ois, J. M. (2002). Identification and functional analysis of the Saccharomyces cerevisiae nicotinamidase gene, PNC1. Yeast 19, 215-224.
18. Grimm, D., Tilly, K., Byram, R., Stewart, P. E., Krum, J. G., Bueschel, D. M., Schwan, T. G., Policastro, P. F., Elias, A. F. & Rosa, P. A. (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.
19. Grimm, D., Tilly, K., Bueschel, D. M., Fisher, M. A., Policastro, P. F., Gherardini, F. C., Schwan, T. G. & Rosa, P. A. (2005). Defining plasmids required by Borrelia burgdorferi for colonization of tick vector Ixodes scapularis (Acari: Ixodidae). J Med Entomol 42, 676-684.
20. Hu, W. S., Wang, R. Y., Shih, J. W. & Lo, S. C. (1993). Identification of a putative infC-rpmI-rplT operon flanked by long inverted repeats in Mycoplasma fermentans (incognitus strain). Gene 127, 79-85.
21. Hunt, L., Holdsworth, M. J. & Gray, J. E. (2007). Nicotinamidase activity is important for germination. Plant J 51, 341-351.
22. Ivanov, I. P., Loughran, G. & Atkins, J. F. (2008). uORFs with unusual translational start codons autoregulate expression of eukaryotic ornithine decarboxylase homologs. Proc Natl Acad Sci U S A 105, 10079-10084.
23. Jewett, M. W., Lawrence, K., Bestor, A. C., Tilly, K., Grimm, D., Shaw, P., VanRaden, M., Gherardini, F. & Rosa, P. A. (2007). The critical role of the linear plasmid lp36 in the infectious cycle of Borrelia burgdorferi. Mol Microbiol 64, 1358-1374.
24. Jewett, M. W., Lawrence, K. A., Bestor, A., Byram, R., Gherardini, F. & Rosa, P. A. (2009). GuaA and GuaB are essential for Borrelia burgdorferi survival in the tick-mouse infection cycle. J Bacteriol 191, 6231-6241.
25. Kim, S., Kurokawa, D., Watanabe, K., Makino, S., Shirahata, T. & Watarai, M. (2004). Brucella abortus nicotinamidase (PncA) con- tributes to its intracellular replication and infectivity in mice. FEMS Microbiol Lett 234, 289-295.
26. Lawrence, K. A., Jewett, M. W., Rosa, P. A. & Gherardini, F. C. (2009). Borrelia burgdorferi bb0426 encodes a 29-deoxyribosyltransferase that plays a central role in purine salvage. Mol Microbiol 72, 1517-1529.
27. Lescot, M., Audic, S., Robert, C., Nguyen, T. T., Blanc, G., Cutler, S. J., Wincker, P., Couloux, A., Claverie, J. M. & other authors (2008). The genome of Borrelia recurrentis, the agent of deadly louse-borne relapsing fever, is a degraded subset of tick-borne Borrelia duttonii. PLoS Genet 4, e1000185.
28. Liveris, D., Schwartz, J. J., Geertman, R. & Schwartz, I. (1993). Molecular cloning and sequencing of infC, the gene encoding translation initiation factor IF3, from four enterobacterial species. FEMS Microbiol Lett 112, 211-216.
29. Minard, K. I. & McAlister-Henn, L. (2010). Pnc1p supports increases in cellular NAD(H) levels in response to internal or external oxidative stress. Biochemistry 49, 6299-6301.
30. Nivinskas, R., Vaiskunaite, R. & Raudonikiene, A. (1992). An internal AUU codon initiates a smaller peptide encoded by bacteriophage T4 baseplate gene 26. Mol Gen Genet 232, 257-261.
31. Pon, C. L. & Gualerzi, C. O. (1986). Mechanism of translational initiation in prokaryotes. IF3 is released from ribosomes during and not before 70 S initiation complex formation. FEBS Lett 195, 215-219.
32. Prère, M. F., Canal, I., Wills, N. M., Atkins, J. F. & Fayet, O. (2011). The interplay of mRNA stimulatory signals required for AUU-mediated initiation and programmed 21 ribosomal frameshifting in decoding of transposable element IS911. J Bacteriol 193, 2735-2744.
33. Purser, J. E., Lawrenz, M. B., Caimano, M. J., Howell, J. K., Radolf, J. D. & Norris, S. J. (2003). A plasmid-encoded nicotinamidase (PncA) is essential for infectivity of Borrelia burgdorferi in a mammalian host. Mol Microbiol 48, 753-764.
34. Ramamoorthy, R., McClain, N. A., Gautam, A. & Scholl-Meeker, D. (2005). Expression of the bmpB gene of Borrelia burgdorferi is modulated by two distinct transcription termination events. J Bacteriol 187, 2592-2600.
35. Raynaud, C., Etienne, G., Peyron, P., Lanéelle, M. A. & Daffé, M. (1998). Extracellular enzyme activities potentially involved in the pathogenicity of Mycobacterium tuberculosis. Microbiology 144, 577-587.
36. Rosa, P. A. & Hogan, D. (1992). Colony formation by Borrelia burgdorferi in solid medium: clonal analysis of osp locus variants. In Proceedings of the First International Conference on Tick-Borne Pathogens at the Host-Vector Interface, pp. 95-103. Edited by U. G. Munderloh & T. J. Kurtti. St Paul, MN: University of Minnesota.
37. Rosa, P. A., Tilly, K. & Stewart, P. E. (2005). The burgeoning molecular genetics of the Lyme disease spirochaete. Nat Rev Microbiol 3, 129-143.
38. Sacerdot, C., Chiaruttini, C., Engst, K., Graffe, M., Milet, M., Mathy, N., Dondon, J. & Springer, M. (1996). The role of the AUU initiation codon in the negative feedback regulation of the gene for translation initiation factor IF3 in Escherichia coli. Mol Microbiol 21, 331-346.
39. Sambrook, J. & Russell, D. W. (2000). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
40. Samuels, D. S. (1995). Electrotransformation of the spirochete Borrelia burgdorferi. In Methods in Molecular Biology, pp. 253-259. Edited by J. A. Nickoloff. Totowa, NJ: Humana Press, Inc.
41. + and vitamin B3: from metabolism to therapies. J Pharmacol Exp Ther 324, 883-893.
42. Silva, R. M., Duarte, I. C., Paredes, J. A., Lima-Costa, T., Perrot, M., Boucherie, H., Goodfellow, B. J., Gomes, A. C., Mateus, D. D. & other authors (2009). The yeast PNC1 longevity gene is up-regulated by mRNA mistranslation. PLoS One 4, e5212.
43. Stewart, P. E., Thalken, R., Bono, J. L. & Rosa, P. (2001). Isolation of a circular plasmid region sufficient for autonomous replication and transformation of infectious Borrelia burgdorferi. Mol Microbiol 39, 714-721.
44. Strother, K. O. & de Silva, A. (2005). Role of Borrelia burgdorferi linear plasmid 25 in infection of Ixodes scapularis ticks. J Bacteriol 187, 5776-5781.
45. Sussman, J. K., Simons, E. L. & Simons, R. W. (1996). Escherichia coli translation initiation factor 3 discriminates the initiation codon in vivo. Mol Microbiol 21, 347-360.
46. Tilly, K., Grimm, D., Bueschel, D. M., Krum, J. G. & 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.
47. Tilly, K., Rosa, P. A. & Stewart, P. E. (2008). Biology of infection with Borrelia burgdorferi. Infect Dis Clin North Am 22, 217-234, v.
48. van der Horst, A., Schavemaker, J. M., Pellis-van Berkel, W. & Burgering, B. M. (2007). The Caenorhabditis elegans nicotinamidase PNC-1 enhances survival. Mech Ageing Dev 128, 346-349.
49. + biosynthesis and nicotinamide levels separately affect reproductive development and cell survival in C. elegans. Development 136, 3637-3646.
50. Wang, G. & Pichersky, E. (2007). Nicotinamidase participates in the salvage pathway of NAD biosynthesis in Arabidopsis. Plant J 49, 1020-1029.
51. Zhu, N., Olivera, B. M. & Roth, J. R. (1991). Activity of the nicotinamide mononucleotide transport system is regulated in Salmonella typhimurium. J Bacteriol 173, 1311-1320.