Metal-dependent gene regulation in the causative agent of lyme disease

Frontiers in Cellular and Infection Microbiology

Volumn 4, Issue NOV, 2013, Pages

  Troxell, Bryan ^a   Yang, X Frank ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Borrelia burgdorferi; Calprotectin; Copper; Lyme disease; Manganese; Zinc

Indexed keywords

BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BORRELIA BURGDORFERI; GENE CONTROL; GENE EXPRESSION; GLYCOLYSIS; HOMEOSTASIS; LIFE CYCLE; LYME DISEASE; NONHUMAN; PARASITE SURVIVAL; PROTEIN EXPRESSION; REVIEW; TICK; ANIMAL; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IXODES; METABOLISM; MOUSE; DRUG EFFECTS;

CALGRANULIN; COPPER; MANGANESE; METAL; ZINC;

BORRELIA BURGDORFERI; CALPROTECTIN; COPPER; LYME DISEASE; MANGANESE; ZINC;

ANIMALS; BORRELIA BURGDORFERI; GENE EXPRESSION REGULATION, BACTERIAL; HOMEOSTASIS; HUMANS; IXODES; METALS; MICE;

EID: 84897918165     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2013.00079     Document Type: Review

References (76)

1. Aguirre, J. D., Clark, H. M., McIlvin, M., Vazquez, C., Palmere, S. L., Grab, D. J., et al. (2013). A manganese-rich environment supports superoxide dismutase activity in a Lyme disease pathogen, Borrelia burgdorferi. J. Biol. Chem. 288, 8468-8478. doi: 10.1074/jbc.M112.433540
2. Alverson, J., Bundle, S. F., Sohaskey, C. D., Lybecker, M. C., and Samuels, D. S. (2003). Transcriptional regulation of the ospAB and ospC promoters from Borrelia burgdorferi. Mol. Microbiol. 48, 1665-1677. doi: 10.1046/j.1365-2958.2003.03537.x
3. Anjem, A., Varghese, S., and Imlay, J. A. (2009). Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol. Microbiol. 72, 844-858. doi: 10.1111/j.1365-2958.2009.06699.x
4. Archibald, F. S., and Fridovich, I. (1981). Manganese and defenses against oxygen toxicity in Lactobacillus plantarum. J. Bacteriol. 145, 442-451.
5. Archibald, F. S., and Fridovich, I. (1982). The scavenging of superoxide radical by manganous complexes: in vitro. Arch. Biochem. Biophys. 214, 452-463. doi: 10.1016/0003-9861(82)90049-2
6. Barbour, A. G. (1984). Isolation and cultivation of Lyme disease spirochetes. Yale J. Biol. Med. 57, 521-525.
7. Blevins, J. S., Xu, H., He, M., Norgard, M. V., Reitzer, L., and Yang, X. F. (2009). Rrp2, a sigma54-dependent transcriptional activator of Borrelia burgdorferi, activates rpoS in an enhancer-independent manner. J. Bacteriol. 191, 2902-2905. doi: 10.1128/JB.01721-08
8. Boardman, B. K., He, M., Ouyang, Z., Xu, H., Pang, X., and Yang, X. F. (2008). Essential role of the response regulator Rrp2 in the infectious cycle of Borrelia burgdorferi. Infect. Immun. 76, 3844-3853. doi: 10.1128/IAI.00467-08
9. Bourret, T. J., Boylan, J. A., Lawrence, K. A., and Gherardini, F. C. (2011). Nitrosative damage to free and zinc-bound cysteine thiols underlies nitric oxide toxicity in wild-type Borrelia burgdorferi. Mol. Microbiol. 81, 259-273. doi: 10.1111/j.1365-2958.2011.07691.x
10. Boylan, J. A., Posey, J. E., and Gherardini, F. C. (2003). Borrelia oxidative stress response regulator, BosR: a distinctive Zn-dependent transcriptional activator. Proc. Natl. Acad. Sci. U.S.A. 100, 11684-11689. doi: 10.1073/pnas.2032956100
11. 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. doi: 10.1128/IAI.73.8.4972-4981.2005
12. Caimano, M. J., Eggers, C. H., Hazlett, K. R., and Radolf, J. D. (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. doi: 10.1128/IAI.72.11.6433-6445.2004
13. Caimano, M. J., Iyer, R., Eggers, C. H., Gonzalez, C., Morton, E. A., and Gilbert, M. A., 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. doi: 10.1111/j.1365-2958.2007.05860.x
14. Changela, A., Chen, K., Xue, Y., Holschen, J., Outten, C. E., O'Halloran, T. V., et al. (2003). Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301, 1383-1387. doi: 10.1126/science.1085950
15. Concepcion, M. B., and Nelson, D. R. (2003). Expression of spoT in Borrelia burgdorferi during serum starvation. J. Bacteriol. 185, 444-452. doi: 10.1128/JB.185.2.444-452.2003
16. Corbin, B. D., Seeley, E. H., Raab, A., Feldmann, J., Miller, M. R., Torres, V. J., et al. (2008). Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319, 962-965. doi: 10.1126/science.1152449
17. Damo, S. M., Kehl-Fie, T. E., Sugitani, N., Holt, M. E., Rathi, S., Murphy, W. J., et al. (2013). Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Proc. Natl. Acad. Sci. U.S.A. 110, 3841-3846. doi: 10.1073/pnas.1220341110
18. De Silva, A. M., and Fikrig, E. (1995). Growth and migration of Borrelia burgdorferi in Ixodes ticks during blood feeding. Am. J. Trop. Med. Hyg. 53, 397-404.
19. 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. doi: 10.1371/journal.ppat.1002532
20. 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. doi: 10.1111/j.1365-2958.2008.06549.x
21. Esteves, E., Fogaca, A. C., Maldonado, R., Silva, F. D., Manso, P. P., Pelajo-Machado, M., et al. (2009). Antimicrobial activity in the tick Rhipicephalus (Boophilus) microplus eggs: cellular localization and temporal expression of microplusin during oogenesis and embryogenesis. Dev. Comp. Immunol. 33, 913-919. doi: 10.1016/j.dci.2009.02.009
22. Fisher, M. A., Grimm, D., Henion, A. K., Elias, A. F., Stewart, P. E., Rosa, P. A., 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. doi: 10.1073/pnas.0408536102
23. Fraser, C. M., Casjens, S., Huang, W. M., Sutton, G. G., Clayton, R., Lathigra, R., et al. (1997). Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390, 580-586. doi: 10.1038/37551
24. Gilbert, M. A., Morton, E. A., Bundle, S. F., and Samuels, D. S. (2007). Artificial regulation of ospC expression in Borrelia burgdorferi. Mol. Microbiol. 63, 1259-1273. doi: 10.1111/j.1365-2958.2007.05593.x
25. Gomez-Santos, N., Perez, J., Sanchez-Sutil, M. C., Moraleda-Munoz, A., and Munoz-Dorado, J. (2011). CorE from Myxococcus xanthus is a copper-dependent RNA polymerase sigma factor. PLoS Genet. 7:e1002106. doi: 10.1371/journal.pgen.1002106
26. Grimm, D., Tilly, K., Byram, R., Stewart, P. E., Krum, J. G., Bueschel, D. M., 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. doi: 10.1073/pnas.0306845101
27. Gu, M., and Imlay, J. A. (2013). Superoxide poisons mononuclear iron enzymes by causing mismetallation. Mol. Microbiol. 89, 123-134. doi: 10.1111/mmi.12263
28. Guerinot, M. L. (2000). The ZIP family of metal transporters. Biochim. Biophys. Acta 1465, 190-198. doi: 10.1016/S0005-2736(00)00138-3
29. 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. U.S.A. 98, 12724-12729. doi: 10.1073/pnas.231442498
30. Hyde, J. A., Shaw, D. K., Smith Iii, R., Trzeciakowski, J. P., and Skare, J. T. (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. doi: 10.1111/j.1365-2958.2009.06951.x
31. Hyde, J. A., Trzeciakowski, J. P., and Skare, J. T. (2007). Borrelia burgdorferi alters its gene expression and antigenic profile in response to CO2 levels. J. Bacteriol. 189, 437-445. doi: 10.1128/JB.01109-06
32. Jain, R., Chen, D., White, R. J., Patel, D. V., and Yuan, Z. (2005). Bacterial Peptide deformylase inhibitors: a new class of antibacterial agents. Curr. Med. Chem. 12, 1607-1621. doi: 10.2174/0929867054367194
33. Jenkins, D. E., Schultz, J. E., and Matin, A. (1988). Starvation-induced cross protection against heat or H2O2 challenge in Escherichia coli. J. Bacteriol. 170, 3910-3914.
34. Katona, L. I., Tokarz, R., Kuhlow, C. J., Benach, J., and Benach, J. L. (2004). The fur homologue in Borrelia burgdorferi. J. Bacteriol. 186, 6443-6456. doi: 10.1128/JB.186.19.6443-6456.2004
35. Kehl-Fie, T. E., Chitayat, S., Hood, M. I., Damo, S., Restrepo, N., Garcia, C., et al. (2011). Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus. Cell Host Microbe 10, 158-164. doi: 10.1016/j.chom.2011.07.004
36. Kehl-Fie, T. E., and Skaar, E. P. (2010). Nutritional immunity beyond iron: a role for manganese and zinc. Curr. Opin. Chem. Biol. 14, 218-224. doi: 10.1016/j.cbpa.2009.11.008
37. Li, X., Pal, U., Ramamoorthi, N., Liu, X., Desrosiers, D. C., Eggers, C. H., et al. (2007). The Lyme disease agent Borrelia burgdorferi requires BB0690, a Dps homologue, to persist within ticks. Mol. Microbiol. 63, 694-710. doi: 10.1111/j.1365-2958.2006.05550.x
38. Liang, F. T., Jacobs, M. B., Bowers, L. C., and Philipp, M. T. (2002). An immune evasion mechanism for spirochetal persistence in Lyme borreliosis. J. Exp. Med. 195, 415-422. doi: 10.1084/jem.20011870
39. Liu, J. Z., Jellbauer, S., Poe, A. J., Ton, V., Pesciaroli, M., Kehl-Fie, T. E., et al. (2012). Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11, 227-239. doi: 10.1016/j.chom.2012.01.017
40. Lusitani, D., Malawista, S. E., and Montgomery, R. R. (2003). Calprotectin, an abundant cytosolic protein from human polymorphonuclear leukocytes, inhibits the growth of Borrelia burgdorferi. Infect. Immun. 71, 4711-4716. doi: 10.1128/IAI.71.8.4711-4716.2003
41. Magnusson, L. U., Farewell, A., and Nystrom, T. (2005). ppGpp: a global regulator in Escherichia coli. Trends Microbiol. 13, 236-242. doi: 10.1016/j.tim.2005.03.008
42. Nguyen, K. T., Wu, J. C., Boylan, J. A., Gherardini, F. C., and Pei, D. (2007). Zinc is the metal cofactor of Borrelia burgdorferi peptide deformylase. Arch. Biochem. Biophys. 468, 217-225. doi: 10.1016/j.abb.2007.09.023
43. Nystrom, T., Larsson, C., and Gustafsson, L. (1996). Bacterial defense against aging: role of the Escherichia coli ArcA regulator in gene expression, readjusted energy flux and survival during stasis. EMBO J. 15, 3219-3228.
44. Obonyo, M., Munderloh, U. G., Fingerle, V., Wilske, B., and Kurtti, T. J. (1999). Borrelia burgdorferi in tick cell culture modulates expression of outer surface proteins A and C in response to temperature. J. Clin. Microbiol. 37, 2137-2141.
45. Ojaimi, C., Brooks, C., Casjens, S., Rosa, P., Elias, A., Barbour, A., et al. (2003). Profiling of temperature-induced changes in Borrelia burgdorferi gene expression by using whole genome arrays. Infect. Immun. 71, 1689-1705. doi: 10.1128/IAI.71.4.1689-1705.2003
46. Ose, D. E., and Fridovich, I. (1976). Superoxide dismutase. Reversible removal of manganese and its substitution by cobalt, nickel or zinc. J. Biol. Chem. 251, 1217-1218.
47. Ouyang, Z., Blevins, J. S., and Norgard, M. V. (2008). Transcriptional interplay among the regulators Rrp2, RpoN, and RpoS in Borrelia burgdorferi. Microbiology 154, 2641-2658. doi: 10.1099/mic.0.2008/019992-0
48. Ouyang, Z., Deka, R. K., and Norgard, M. V. (2011). Bos R (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
49. Ouyang, Z., He, M., Oman, T., Yang, X. F., and Norgard, M. V. (2009a). A manganese transporter, BB0219 (BmtA), is required for virulence by the Lyme disease spirochete, Borrelia burgdorferi. Proc. Natl. Acad. Sci. U.S.A. 106, 3449-3454. doi: 10.1073/pnas.0812999106
50. Ouyang, Z., Kumar, M., Kariu, T., Haq, S., Goldberg, M., Pal, U., et al. (2009b). BosR (BB0647) governs virulence expression in Borrelia burgdorferi. Mol. Microbiol. 74, 1331-1343. doi: 10.1111/j.1365-2958.2009.06945.x
51. Pal, U., Yang, X., Chen, M., Bockenstedt, L. K., Anderson, J. F., Flavell, R. A., et al. (2004). OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J. Clin. Invest. 113, 220-230. doi: 10.1172/JCI19894
52. Posey, J. E., and Gherardini, F. C. (2000). Lack of a role for iron in the Lyme disease pathogen. Science 288, 1651-1653. doi: 10.1126/science.288.5471.1651
53. Privalle, C. T., and Fridovich, I. (1993). Iron specificity of the Fur-dependent regulation of the biosynthesis of the manganese-containing superoxide dismutase in Escherichia coli. J. Biol. Chem. 268, 5178-5181.
54. 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. doi: 10.1038/nrmicro2714
55. Radolf, J. D., and Samuels, D. S. (eds.). (2010). Borrelia: Molecular Biology, Host Interaction, and Pathogenesis. Norfolk: Caister Academic Press.
56. Samuels, D. S. (2011). Gene regulation in Borrelia burgdorferi. Annu. Rev. Microbiol. 65, 479-499. doi: 10.1146/annurev.micro.112408.134040
57. Silva, F. D., Rezende, C. A., Rossi, D. C., Esteves, E., Dyszy, F. H., Schreier, S., et al. (2009). Structure and mode of action of microplusin, a copper II-chelating antimicrobial peptide from the cattle tick Rhipicephalus (Boophilus) microplus. J. Biol. Chem. 284, 34735-34746. doi: 10.1074/jbc.M109.016410
58. Silva, F. D., Rossi, D. C., Martinez, L. R., Frases, S., Fonseca, F. L., Campos, C. B., et al. (2011). Effects of microplusin, a copper-chelating antimicrobial peptide, against Cryptococcus neoformans. FEMS Microbiol. Lett. 324, 64-72. doi: 10.1111/j.1574-6968.2011.02386.x
59. Smith, A. H., Blevins, J. S., Bachlani, G. N., Yang, X. F., and Norgard, M. V. (2007). Evidence that RpoS (sigmaS) in Borrelia burgdorferi is controlled directly by RpoN (sigma54/sigmaN). J. Bacteriol. 189, 2139-2144. doi: 10.1128/JB.01653-06
60. Sobota, J. M., and Imlay, J. A. (2011). Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese. Proc. Natl. Acad. Sci. U.S.A. 108, 5402-5407. doi: 10.1073/pnas.1100410108
61. Srinivasan, V. B., Vaidyanathan, V., Mondal, A., Venkataramaiah, M., and Rajamohan, G. (2012). Functional characterization of a novel Mn2+ dependent protein serine/threonine kinase KpnK, produced by Klebsiella pneumoniae strain MGH78578. FEBS Lett. 586, 3778-3786. doi: 10.1016/j.febslet.2012.09.007
62. Stadtman, E. R., Berlett, B. S., and Chock, P. B. (1990). Manganese-dependent disproportionation of hydrogen peroxide in bicarbonate buffer. Proc. Natl. Acad. Sci. U.S.A. 87, 384-388. doi: 10.1073/pnas.87.1.384
63. Stevenson, B., Schwan, T. G., and Rosa, P. A. (1995). Temperature-related differential expression of antigens in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 63, 4535-4539.
64. Sun, D., Lee, G., Lee, J. H., Kim, H. Y., Rhee, H. W., Park, S. Y., et al. (2010). A metazoan ortholog of SpoT hydrolyzes ppGpp and functions in starvation responses. Nat. Struct. Mol. Biol. 17, 1188-1194. doi: 10.1038/nsmb.1906
65. Sy, J. (1977). In vitro degradation of guanosine 5'-diphosphate, 3'-diphosphate. Proc. Natl. Acad. Sci. U.S.A. 74, 5529-5533. doi: 10.1073/pnas.74.12.5529
66. Troxell, B., Xu, H., and Yang, X. F. (2012). Borrelia burgdorferi, a pathogen that lacks iron, encodes manganese-dependent superoxide dismutase essential for resistance to streptonigrin. J. Biol. Chem. 287, 19284-19293. doi: 10.1074/jbc.M112.344903
67. Troxell, B., Ye, M., Yang, Y., Carrasco, S. E., Lou, Y., and Yang, X. F. (2013). Manganese and zinc regulate virulence determinants in Borrelia burgdorferi. Infect. Immun. 81, 2743-2752. doi: 10.1128/IAI.00507-13
68. Wang, P., Dadhwal, P., Cheng, Z., Zianni, M. R., Rikihisa, Y., Liang, F. T., et al. (2013). Borrelia burgdorferi oxidative stress regulator BosR directly represses lipoproteins primarily expressed in the tick during mammalian infection. Mol. Microbiol. 89, 1140-1153. doi: 10.1111/mmi.12337
69. Wang, P., Lutton, A., Olesik, J., Vali, H., and Li, X. (2012). A novel iron- and copper-binding protein in the Lyme disease spirochaete. Mol. Microbiol. 86, 1441-1451. doi: 10.1111/mmi.12068
70. Xu, Q., McShan, K., and Liang, F. T. (2008a). Essential protective role attributed to the surface lipoproteins of Borrelia burgdorferi against innate defences. Mol. Microbiol. 69, 15-29. doi: 10.1111/j.1365-2958.2008.06264.x
71. Xu, Q., McShan, K., and Liang, F. T. (2008b). Modification of Borrelia burgdorferi to overproduce OspA or VlsE alters its infectious behaviour. Microbiology 154, 3420-3429. doi: 10.1099/mic.0.2008/019737-0
72. Xu, Q., Seemanapalli, S. V., McShan, K., and Liang, F. T. (2006). Constitutive expression of outer surface protein C diminishes the ability of Borrelia burgdorferi to evade specific humoral immunity. Infect. Immun. 74, 5177-5184. doi: 10.1128/IAI.00713-06
73. Yang, X., Goldberg, M. S., Popova, T. G., Schoeler, G. B., Wikel, S. K., Hagman, K. E., et al. (2000). Interdependence of environmental factors influencing reciprocal patterns of gene expression in virulent Borrelia burgdorferi. Mol. Microbiol. 37, 1470-1479. doi: 10.1046/j.1365-2958.2000.02104.x
74. 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. U.S.A. 100, 11001-11006. doi: 10.1073/pnas.1834315100
75. Yang, X. F., Lybecker, M. C., Pal, U., Alani, S. M., Blevins, J., Revel, A. T., et al. (2005). Analysis of the ospC regulatory element controlled by the RpoN-RpoS regulatory pathway in Borrelia burgdorferi. J. Bacteriol. 187, 4822-4829. doi: 10.1128/JB.187.14.4822-4829.2005
76. Yui, S., Nakatani, Y., and Mikami, M. (2003). Calprotectin (S100A8/S100A9), an inflammatory protein complex from neutrophils with a broad apoptosis-inducing activity. Biol. Pharm. Bull. 26, 753-760. doi: 10.1248/bpb.26.753