Zinc regulates a switch between primary and alternative S18 ribosomal proteins in Mycobacterium tuberculosis

Molecular Microbiology

Volumn 97, Issue 2, 2015, Pages 263-280

  Prisic, Sladjana ^a,b   Hwang, Hyonson ^a,d   Dow, Allexa ^b   Barnaby, Omar ^a,e   Pan, Tenny S ^b   Lonzanida, Jaymes A ^b   Chazin, Walter J ^c   Steen, Hanno ^a   Husson, Robert N ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF HAWAII   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TENNESSEE AT MARTIN   (United States)

^e BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALGRANULIN; MESSENGER RNA; PROTEIN S6; RIBOSOME PROTEIN; RIBOSOME PROTEIN S18; RIBOSOME PROTEIN S18 1; RIBOSOME PROTEIN S18 2; UNCLASSIFIED DRUG; ZINC; BACTERIAL RNA; RIBOSOMAL PROTEIN S18; RIBOSOME RNA;

ARTICLE; BACTERIAL GROWTH; BINDING AFFINITY; BINDING COMPETITION; BIOACCUMULATION; BIOGENESIS; CONTROLLED STUDY; DIMERIZATION; GENE; GENE REPRESSION; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOSOME; PREDICTION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; RIBOSOME PROTEIN S18 2 GENE; SIGNAL TRANSDUCTION; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

MYCOBACTERIUM TUBERCULOSIS;

GENE EXPRESSION REGULATION, BACTERIAL; MYCOBACTERIUM TUBERCULOSIS; RIBOSOMAL PROTEIN S6; RIBOSOMAL PROTEINS; RNA, BACTERIAL; RNA, RIBOSOMAL; ZINC;

EID: 84935690552     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13022     Document Type: Article

References (71)

1. Abramovitch, R.B., Rohde, K.H., Hsu, F.-F., and Russell, D.G. (2011) aprABC: a Mycobacterium tuberculosis complex-specific locus that modulates pH-driven adaptation to the macrophage phagosome. Mol Microbiol 80: 678-694.
2. Akanuma, G., Nanamiya, H., Natori, Y., Nomura, N., and Kawamura, F. (2006) Liberation of Zinc-containing L31 (RpmE) from ribosomes by its paralogous gene product, YtiA, in Bacillus subtilis. J Bacteriol 188: 2715-2720.
3. Akanuma, G., Nanamiya, H., Natori, Y., Yano, K., Suzuki, S., Omata, S., etal. (2012) Inactivation of ribosomal protein genes in Bacillus subtilis reveals importance of each ribosomal protein for cell proliferation and cell differentiation. J Bacteriol 194: 6282-6291.
4. Berry, M.P.R., Graham, C.M., McNab, F.W., Xu, Z., Bloch, A.A., Oni, T., etal. (2012) An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466: 973-977.
5. Botella, H., Peyron, P., Levillain, F., Poincloux, R., Poquet, Y., Brandli, I., etal. (2011) Mycobacterial p(1)-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 10: 248-259.
6. Boysen, R.I., and Hearn, M.T. (2001) The metal binding properties of the CCCH motif of the 50S ribosomal protein L36 from Thermus thermophilus. J Pept Res 57: 19-28.
7. Bruell, C.M., Eichholz, C., Kubarenko, A., Post, V., Katunin, V.I., Hobbie, S.N., etal. (2008) Conservation of bacterial protein synthesis machinery: initiation and elongation in Mycobacterium smegmatis. Biochemistry 47: 8828-8839.
8. Castro-Roa, D., Garcia-Pino, A., De Gieter, S., van Nuland, N.A., Loris, R., and Zenkin, N. (2013) The Fic protein Doc uses an inverted substrate to phosphorylate and inactivate EF-Tu. Nat Chem Biol 9: 811-817.
9. Chen, S.S., Sperling, E., Silverman, J.M., Davis, J.H., and Williamson, J.R. (2012) Measuring the dynamics of E. coli ribosome biogenesis using pulse-labeling and quantitative mass spectrometry. Mol Biosyst 8: 3325-3334.
10. Connolly, K., and Culver, G. (2009) Deconstructing ribosome construction. Trends Biochem Sci 34: 256-263.
11. Corbin, B.D., Seeley, E.H., Raab, A., Feldmann, J., Miller, M.R., Torres, V.J., etal. (2008) Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319: 962-965.
12. Cruz, J.W., Rothenbacher, F.P., Maehigashi, T., Lane, W.S., Dunham, C.M., and Woychik, N.A. (2014) Doc toxin is a kinase that inactivates elongation factor Tu. J Biol Chem 289: 7788-7798.
13. Damo, S., Chazin, W.J., Skaar, E.P., and Kehl-Fie, T.E. (2012) Inhibition of bacterial superoxide defense. Virulence 3: 325-328.
14. Damo, S.M., Kehl-Fie, T.E., Sugitani, N., Holt, M.E., Rathi, S., Murphy, W.J., etal. (2013) Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Proc Natl Acad Sci 110: 3841-3846.
15. Festa, R.A., McAllister, F., Pearce, M.J., Mintseris, J., Burns, K.E., Gygi, S.P., and Darwin, K.H. (2010) Prokaryotic ubiquitin-like protein (Pup) proteome of Mycobacterium tuberculosis. PLoS ONE 5: e8589.
16. Gaballa, A., Wang, T., Ye, R.W., John, D., and Helmann, J.D. (2002) Functional analysis of the Bacillus subtilis Zur regulon. J Bacteriol 184: 6508-6514.
17. Gabriel, S.E., and Helmann, J.D. (2009) Contributions of Zur-controlled ribosomal proteins to growth under zinc starvation conditions. J Bacteriol 191: 6116-6122.
18. Germain, E., Castro-Roa, D., Zenkin, N., and Gerdes, K. (2013) Molecular mechanism of bacterial persistence by HipA. Mol Cell 52: 248-254.
19. Gilbert, W.V. (2011) Functional specialization of ribosomes? Trends Biochem Sci 36: 127-132.
20. Gold, B., Deng, H., Bryk, R., Vargas, D., Eliezer, D., Roberts, J., etal. (2008) Identification of a copper-binding metallothionein in pathogenic mycobacteria. Nat Chem Biol 4: 609-616.
21. Gordiyenko, Y., Deroo, S., Zhou, M., Videler, H., and Robinson, C.V. (2008) Acetylation of L12 increases interactions in the Escherichia coli ribosomal stalk complex. J Mol Biol 380: 404-414.
22. Graham, A.I., Hunt, S., Stokes, S.L., Bramall, N., Bunch, J., Cox, A.G., etal. (2009) Severe zinc depletion of Escherichia coli: roles for high affinity zinc binding by ZinT, zinc transport and zinc-independent proteins. J Biol Chem 284: 18377-18389.
23. Held, W.A., Ballou, B., Mizushima, S., and Nomura, M. (1974) Assembly mapping of 30 S ribosomal proteins from Escherichia coli. Further studies. J Biol Chem 249: 3103-3111.
24. Hensley, M.P., Gunasekera, T.S., Easton, J.A., Sigdel, T.K., Stacy, A., Klingbeil, L., etal. (2012) Characterization of Zn(II)-responsive ribosomal proteins YkgM and L31 in E. coli. J Inorg Biochem 111: 164-172.
25. Hunter, M.J., and Chazin, W.J. (1998) High level expression and dimer characterization of the S100 EF-hand proteins, migration inhibitory factor-related proteins 8 and 14. J Biol Chem 273: 12427-12435.
26. Kaspy, I., Rotem, E., Weiss, N., Ronin, I., Balaban, N.Q., and Glaser, G. (2013) HipA-mediated antibiotic persistence via phosphorylation of the glutamyl-tRNA-synthetase. Nat Commun 4: 3001.
27. Koonin, E.V., Wolf, Y.I., Yutin, N., and Puigbo, P. (2012) Phylogenomics of prokaryotic ribosomal proteins. PLoS ONE 7: e36972.
28. Lee, J.-W., and Helmann, J.D. (2006) Biochemical characterization of the structural Zn2+ site in the Bacillus subtilis peroxide sensor PerR. J Biol Chem 281: 23567-23578.
29. Li, Y., Qiu, Y., Gao, H., Guo, Z., Han, Y., Song, Y., etal. (2009) Characterization of Zur-dependent genes and direct Zur targets in Yersinia pestis. BMC Microbiol 9: 128.
30. Lim, C.K., Hassan, K.A., Penesyan, A., Loper, J.E., and Paulsen, I.T. (2013) The effect of zinc limitation on the transcriptome of Pseudomonas protegens Pf-5. Environ Microbiol 15: 702-715.
31. Maciag, A., Dainese, E., Rodriguez, G.M., Milano, A., Provvedi, R., Pasca, M.R., etal. (2007) Global analysis of the Mycobacterium tuberculosis Zur (FurB) regulon. J Bacteriol 189: 730-740.
32. Magnusson, L.U., Farewell, A., and Nyström, T. (2005) ppGpp: a global regulator in Escherichia coli. Trends Microbiol 13: 236-242.
33. Makarova, K.S., Ponomarev, V.A., and Koonin, E.V. (2001) Two C or not two C: recurrent disruption of Zn-ribbons, gene duplication, lineage-specific gene loss, and horizontal gene transfer in evolution of bacterial ribosomal proteins. Genome Biol 2: 1-14.
34. Man, T.-K., Li, Y., Dang, T.A., Shen, J., Perlaky, L., and Lau, C.C. (2006) Optimising the use of TRIzol-extracted proteins in surface enhanced laser desorption/ionization (SELDI) analysis. Proteome Sci 4: 3.
35. Marzi, S., Myasnikov, A.G., Serganov, A., Ehresmann, C., Romby, P., Yusupov, M., and Klaholz, B.P. (2007) Structured mRNAs regulate translation initiation by binding to the platform of the ribosome. Cell 130: 1019-1031.
36. Mizushima, S., and Nomura, M. (1970) Assembly mapping of 30S ribosomal proteins from E. coli. Nature 226: 1214-1218.
37. Moore, C.M., and Helmann, J.D. (2005) Metal ion homeostasis in Bacillus subtilis. Curr Opin Microbiol 8: 188-195.
38. Nanamiya, H., and Kawamura, F. (2010) Towards an elucidation of the roles of the ribosome during different growth phases in Bacillus subtilis. Biosci Biotechnol Biochem 74: 451-461.
39. Nanamiya, H., Akanuma, G., Natori, Y., Murayama, R., Kosono, S., Kudo, T., etal. (2004) Zinc is a key factor in controlling alternation of two types of L31 protein in the Bacillus subtilis ribosome. Mol Microbiol 52: 273-283.
40. Nanamiya, H., Kawamura, F., and Kosono, S. (2006) Proteomic study of the Bacillus subtilis ribosome: finding of zinc-dependent replacement for ribosomal protein L31 paralogues. J Gen Appl Microbiol 52: 249-258.
41. Natori, Y., Nanamiya, H., Akanuma, G., Kosono, S., Kudo, T., Ochi, K., and Kawamura, F. (2007) A fail-safe system for the ribosome under zinc-limiting conditions in Bacillus subtilis. Mol Microbiol 63: 294-307.
42. Owen, G.A., Pascoe, B., Kallifidas, D., and Paget, M.S.B. (2007) Zinc-responsive regulation of alternative ribosomal protein genes in Streptomyces coelicolor involves zur and sigmaR. J Bacteriol 189: 4078-4086.
43. Panina, E.M., Mironov, A.A., and Gelfand, M.S. (2003) Comparative genomics of bacterial zinc regulons: enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc Natl Acad Sci USA 100: 9912-9917.
44. Pawlik, M.-C., Hubert, K., Joseph, B., Claus, H., Schoen, C., and Vogel, U. (2012) The zinc-responsive regulon of Neisseria meningitidis comprises 17 genes under control of a Zur element. J Bacteriol 194: 6594-6603.
45. Pechkovsky, D., V, Zalutskaya, O.M., Ivanov, G.I., and Misuno, N.I. (2000) Calprotectin (MRP8/14 protein complex) release during mycobacterial infection in vitro and in vivo. FEMS Immunol Med Microbiol 29: 27-33.
46. Prisic, S., Dankwa, S., Schwartz, D., Chou, M.F., Locasale, J.W., Kang, C.-M., etal. (2010) Extensive phosphorylation with overlapping specificity by Mycobacterium tuberculosis serine/threonine protein kinases. Proc Natl Acad Sci USA 107: 7521-7526.
47. Raman, S., Hazra, R., Dascher, C.C., and Husson, R.N. (2004) Transcription regulation by the Mycobacterium tuberculosis alternative sigma factor SigD and its role in virulence. J Bacteriol 186: 6605-6616.
48. Recht, M.I., and Williamson, J.R. (2001) Central domain assembly: thermodynamics and kinetics of S6 and S18 binding to an S15-RNA complex. J Mol Biol 313: 35-48.
49. Rowland, J.L., and Niederweis, M. (2012) Resistance mechanisms of Mycobacterium tuberculosis against phagosomal copper overload. Tuberculosis 92: 202-210.
50. Sambandamurthy, V.K., Wang, X., Chen, B., Russell, R.G., Derrick, S., Collins, F.M., etal. (2002) A pantothenate auxotroph of Mycobacterium tuberculosis is highly attenuated and protects mice against tuberculosis. Nat Med 8: 1171-1174.
51. Sampson, S.L., Dascher, C.C., Sambandamurthy, V.K., Russell, R.G., Jacobs, W.R., Bloom, B.R., and Hondalus, M.K. (2004) Protection elicited by a double leucine and pantothenate auxotroph of Mycobacterium tuberculosis in guinea pigs. Infect Immun 72: 3031-3037.
52. Schuwirth, B.S., Borovinskaya, M.A., Hau, C.W., Zhang, W., Vila-Sanjurjo, A., Holton, J.M., and Cate, J.H.D. (2005) Structures of the bacterial ribosome at 3.5 A resolution. Science 310: 827-834.
53. Seidel, S.A., Dijkman, P.M., Lea, W.A., van den Bogaart, G., Jerabek-Willemsen, M., Lazic, A., etal. (2013) Microscale thermophoresis quantifies biomolecular interactions under previously challenging conditions. Methods 59: 301-315.
54. Shepelkova, G., Pommerenke, C., Alberts, R., Geffers, R., Evstifeev, V., Apt, A., etal. (2013) Analysis of the lung transcriptome in Mycobacterium tuberculosis-infected mice reveals major differences in immune response pathways between TB-susceptible and resistant hosts. Tuberculosis 93: 263-269.
55. Shin, J.-H., Oh, S.-Y., Kim, S.-J., and Roe, J.-H. (2007) The zinc-responsive regulator Zur controls a zinc uptake system and some ribosomal proteins in Streptomyces coelicolor A3(2). J Bacteriol 189: 4070-4077.
56. Shoji, S., Dambacher, C.M., Shajani, Z., Williamson, J.R., and Schultz, P.G. (2011) Systematic chromosomal deletion of bacterial ribosomal protein genes. J Mol Biol 413: 751-761.
57. Simons, T.J. (1993) Measurement of free Zn2+ ion concentration with the fluorescent probe mag-fura-2 (furaptra). J Biochem Biophys Methods 27: 25-37.
58. Stover, C., de la Cruz, V., Fuerst, T., Burlein, J., Benson, L., Bennett, L., etal. (1991) New use of BCG for recombinant vaccines. Nature 351: 456-460.
59. Trauner, A., Bennett, M.H., and Williams, H.D. (2011) Isolation of bacterial ribosomes with monolith chromatography. PLoS ONE 6: e16273.
60. Tsiboli, P., Triantafillidou, D., Franceschi, F., and Choli-Papadopoulou, T. (1998) Studies on the Zn-containing S14 ribosomal protein from Thermus thermophilus. Eur J Biochem 256: 136-141.
61. Ueta, M., Ohniwa, R.L., Yoshida, H., Maki, Y., Wada, C., and Wada, A. (2008) Role of HPF (hibernation promoting factor) in translational activity in Escherichia coli. J Biochem 143: 425-433.
62. Ulbrich, B., and Niearhaus, K. (1975) Pools of ribosomal proteins in Escherichia coli. Eur J Biochem 57: 49-54.
63. Wagner, D., Maser, J., Lai, B., Cai, Z., Barry, C.E., Höner zu Bentrup, K., etal. (2005) Elemental analysis of Mycobacterium avium, Mycobacterium tuberculosis, and Mycobacterium smegmatis-containing phagosomes indicates pathogen-induced microenvironments within the host cell's endosomal system. J Immunol 174: 1491-1500.
64. Walkup, G.K., and Imperiali, B. (1997) Fluorescent chemosensors for divalent zinc based on zinc finger domains. Enhanced oxidative stability, metal binding affinity, and structural and functional characterization. J Am Chem Soc 119: 3443-3450.
65. Wang, D., Hurst, T.K., Thompson, R.B., and Fierke, C.A. (2011) Genetically encoded ratiometric biosensors to measure intracellular exchangeable zinc in Escherichia coli. J Biomed Opt 16(8): 087011.
66. Wienken, C.J., Baaske, P., Rothbauer, U., Braun, D., and Duhr, S. (2010) Protein-binding assays in biological liquids using microscale thermophoresis. Nat Commun 1: 100.
67. Wilson, D.N., and Nierhaus, K.H. (2007) The weird and wonderful world of bacterial ribosome regulation. Crit Rev Biochem Mol Biol 42: 187-219.
68. Wimberly, B.T., Brodersen, D.E., Clemons, W.M., Jr, Morgan-Warren, R.J., Carter, A.P., Vonrhein, C., etal. (2000) Structure of the 30S ribosomal subunit. Nature 407: 327-339.
69. Wisniewski, J., Zougman, A., Nagaraj, N., and Mann, M. (2009) Universal sample preparation method for proteome analysis. Nat Methods 6: 359-362.
70. Yusupova, G., Jenner, L., Rees, B., Moras, D., and Yusupov, M. (2006) Structural basis for messenger RNA movement on the ribosome. Nature 444: 391-394.
71. Zhang, Y.J., Ioerger, T.R., Huttenhower, C., Long, J.E., Sassetti, C.M., Sacchettini, J.C., and Rubin, E.J. (2012) Global assessment of genomic regions required for growth in Mycobacterium tuberculosis. PLoS Pathog 8: e1002946.