Advertisement

The Pup-Proteasome System of Mycobacterium tuberculosis

  • Marie I. Samanovic
  • Huilin Li
  • K. Heran Darwin
Chapter
Part of the Subcellular Biochemistry book series (SCBI, volume 66)

Abstract

Proteasomes are ATP-dependent protein degradation machines present in all archaea and eukaryotes, and found in several bacterial species of the order Actinomycetales. Mycobacterium tuberculosis (Mtb), an Actinomycete pathogenic to humans, requires proteasome function to cause disease. In this chapter, we describe what is currently understood about the biochemistry of the Mtb proteasome and its role in virulence. The characterization of the Mtb proteasome has led to the discovery that proteins can be targeted for degradation by a small protein modifier in bacteria as they are in eukaryotes. Furthermore, the understanding of proteasome function in Mtb has helped reveal new insight into how the host battles infections.

Keywords

Nitric Oxide Core Particle Proteasome Function Isopeptide Bond Proteasome Substrate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We are grateful to Nadine Bode and Andrew Darwin for critical review of this manuscript. K.H.D is supported by NIH grants AI065437 and HL92774, the Irma T. Hirschl Trust, and holds an Investigators in the Pathogenesis of Infectious Disease Award from the Burroughs Wellcome Fund. H.L. is supported by NIH grant AI070285 and Brookhaven National Laboratory LDRD grant 10-016.

References

  1. 1.
    Nathan C, Shiloh MU (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci U S A 97(16): 8841–8848PubMedGoogle Scholar
  2. 2.
    MacMicking J, Xie QW, Nathan C (1997) Nitric oxide and macrophage function. Annu Rev Immunol 15:323–350PubMedGoogle Scholar
  3. 3.
    Alvarez B, Radi R (2003) Peroxynitrite reactivity with amino acids and proteins. Amino Acids 25(3–4):295–311PubMedGoogle Scholar
  4. 4.
    Szabo C (2003) Multiple pathways of peroxynitrite cytotoxicity. Toxicol Lett 140–141:105–112PubMedGoogle Scholar
  5. 5.
    Darwin KH, Ehrt S, Gutierrez-Ramos JC, Weich N et al (2003) The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302(5652):1963–1966PubMedGoogle Scholar
  6. 6.
    Zwickl P, Ng D, Woo KM, Klenk HP et al (1999) An archaebacterial ATPase, homologous to ATPases in the eukaryotic 26S proteasome, activates protein breakdown by 20S proteasomes. J Biol Chem 274(37):26008–26014PubMedGoogle Scholar
  7. 7.
    Wolf S, Nagy I, Lupas A, Pfeifer G et al (1998) Characterization of ARC, a divergent member of the AAA ATPase family from Rhodococcus erythropolis. J Mol Biol 277(1):13–25PubMedGoogle Scholar
  8. 8.
    Arrigo AP, Tanaka K, Goldberg AL, Welch WJ (1988) Identity of the 19S ‘prosome’ particle with the large multifunctional protease complex of mammalian cells (the proteasome). Nature 331(6152):192–194PubMedGoogle Scholar
  9. 9.
    Pickart CM, Cohen RE (2004) Proteasomes and their kin: proteases in the machine age. Nat Rev Mol Cell Biol 5(3):177–187PubMedGoogle Scholar
  10. 10.
    Coux O, Tanaka K, Goldberg AL (1996) Structure and functions of the 20S and 26S proteasomes. Annu Rev Biochem 65:801–847PubMedGoogle Scholar
  11. 11.
    Finley D (2009) Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 78:477–513PubMedGoogle Scholar
  12. 12.
    Rock KL, Goldberg AL (1999) Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu Rev Immunol 17:739–779PubMedGoogle Scholar
  13. 13.
    Schmidt M, Hanna J, Elsasser S, Finley D (2005) Proteasome-associated proteins: regulation of a proteolytic machine. Biol Chem 386(8):725–737PubMedGoogle Scholar
  14. 14.
    Butler SM, Festa RA, Pearce MJ, Darwin KH (2006) Self-compartmentalized bacterial proteases and pathogenesis. Mol Microbiol 60(3):553–562PubMedGoogle Scholar
  15. 15.
    Gur E, Ottofuelling R, Dougan DA (2013) Machines of destruction – AAA  +  proteases and the adaptors that control them. In: Dougan DA (ed) Regulated proteolysis in microorganisms. Springer, Subcell Biochem 66:3–33Google Scholar
  16. 16.
    Dahlmann B, Kopp F, Kuehn L, Niedel B et al (1989) The multicatalytic proteinase (prosome) is ubiquitous from eukaryotes to archaebacteria. FEBS Lett 251(1–2):125–131PubMedGoogle Scholar
  17. 17.
    Lowe J, Stock D, Jap B, Zwickl P et al (1995) Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 A resolution. Science 268(5210):533–539PubMedGoogle Scholar
  18. 18.
    Tamura T, Nagy I, Lupas A, Lottspeich F et al (1995) The first characterization of a eubacterial proteasome: the 20S complex of Rhodococcus. Curr Biol 5(7):766–774PubMedGoogle Scholar
  19. 19.
    Knipfer N, Shrader TE (1997) Inactivation of the 20S proteasome in Mycobacterium smegmatis. Mol Microbiol 25(2):375–383PubMedGoogle Scholar
  20. 20.
    Nagy I, Tamura T, Vanderleyden J, Baumeister W et al (1998) The 20S proteasome of Streptomyces coelicolor. J Bacteriol 180(20):5448–5453PubMedGoogle Scholar
  21. 21.
    Pouch MN, Cournoyer B, Baumeister W (2000) Characterization of the 20S proteasome from the actinomycete Frankia. Mol Microbiol 35(2):368–377PubMedGoogle Scholar
  22. 22.
    Lupas A, Zuhl F, Tamura T, Wolf S et al (1997) Eubacterial proteasomes. Mol Biol Rep 24(1–2):125–131PubMedGoogle Scholar
  23. 23.
    Cole ST, Brosch R, Parkhill J, Garnier T et al (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393(6685):537–544PubMedGoogle Scholar
  24. 24.
    De Mot R (2007) Actinomycete-like proteasomes in a Gram-negative bacterium. Trends Microbiol 15(8):335–338PubMedGoogle Scholar
  25. 25.
    Gille C, Goede A, Schloetelburg C, Preissner R et al (2003) A comprehensive view on proteasomal sequences: implications for the evolution of the proteasome. J Mol Biol 326(5):1437–1448PubMedGoogle Scholar
  26. 26.
    Groll M, Bochtler M, Brandstetter H, Clausen T et al (2005) Molecular machines for protein degradation. Chembiochem 6(2):222–256PubMedGoogle Scholar
  27. 27.
    Cerda-Maira F, Darwin KH (2009) The Mycobacterium tuberculosis proteasome: more than just a barrel-shaped protease. Microbes Infect 11(14–15):1150–1155PubMedGoogle Scholar
  28. 28.
    Gandotra S, Schnappinger D, Monteleone M, Hillen W et al (2007) In vivo gene silencing identifies the Mycobacterium tuberculosis proteasome as essential for the bacteria to persist in mice. Nat Med 13(12):1515–1520PubMedGoogle Scholar
  29. 29.
    Gandotra S, Lebron MB, Ehrt S (2010) The Mycobacterium tuberculosis proteasome active site threonine is essential for persistence yet dispensable for replication and resistance to nitric oxide. PLoS Pathog 6(8):e140Google Scholar
  30. 30.
    Sassetti CM, Boyd DH, Rubin EJ (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48(1):77–84PubMedGoogle Scholar
  31. 31.
    Maupin-Furlow JA (2013) Archaeal proteasomes and sampylation. In: Dougan DA (ed) Regulated proteolysis in microorganisms. Springer, Subcell Biochem 66:297–327Google Scholar
  32. 32.
    Buchberger A (2013) Roles of Cdc48 in regulated protein degradation in yeast. In: Dougan DA (ed) Regulated proteolysis in microorganisms. Springer, Subcell Biochem 66:195–222Google Scholar
  33. 33.
    Hu G, Lin G, Wang M, Dick L et al (2006) Structure of the Mycobacterium tuberculosis proteasome and mechanism of inhibition by a peptidyl boronate. Mol Microbiol 59(5):1417–1428PubMedGoogle Scholar
  34. 34.
    Witt S, Kwon YD, Sharon M, Felderer K et al (2006) Proteasome assembly triggers a switch required for active-site maturation. Structure 14(7):1179–1188PubMedGoogle Scholar
  35. 35.
    Groll M, Ditzel L, Lowe J, Stock D et al (1997) Structure of 20S proteasome from yeast at 2.4 A resolution. Nature 386(6624):463–471PubMedGoogle Scholar
  36. 36.
    Seemuller E, Lupas A, Baumeister W (1996) Autocatalytic processing of the 20S proteasome. Nature 382(6590):468–471PubMedGoogle Scholar
  37. 37.
    Zuhl F, Seemuller E, Golbik R, Baumeister W (1997) Dissecting the assembly pathway of the 20S proteasome. FEBS Lett 418(1–2):189–194PubMedGoogle Scholar
  38. 38.
    Zuhl F, Tamura T, Dolenc I, Cejka Z et al (1997) Subunit topology of the Rhodococcus proteasome. FEBS Lett 400(1):83–90PubMedGoogle Scholar
  39. 39.
    Mayr J, Seemuller E, Muller SA, Engel A et al (1998) Late events in the assembly of 20S proteasomes. J Struct Biol 124(2–3):179–188PubMedGoogle Scholar
  40. 40.
    Kwon YD, Nagy I, Adams PD, Baumeister W et al (2004) Crystal structures of the Rhodococcus proteasome with and without its pro-peptides: implications for the role of the pro-peptide in proteasome assembly. J Mol Biol 335(1):233–245PubMedGoogle Scholar
  41. 41.
    Zwickl P, Kleinz J, Baumeister W (1994) Critical elements in proteasome assembly. Nat Struct Biol 1(11):765–770PubMedGoogle Scholar
  42. 42.
    Lin G, Hu G, Tsu C, Kunes YZ et al (2006) Mycobacterium tuberculosis prcBA genes encode a gated proteasome with broad oligopeptide specificity. Mol Microbiol 59(5):1405–1416PubMedGoogle Scholar
  43. 43.
    Li D, Li H, Wang T, Pan H et al (2010) Structural basis for the assembly and gate closure mechanisms of the Mycobacterium tuberculosis 20S proteasome. EMBO J 29(12):2037–2047PubMedGoogle Scholar
  44. 44.
    Groll M, Huber R (2003) Substrate access and processing by the 20S proteasome core particle. Int J Biochem Cell Biol 35(5):606–616PubMedGoogle Scholar
  45. 45.
    Zhang F, Wu Z, Zhang P, Tian G et al (2009) Mechanism of substrate unfolding and translocation by the regulatory particle of the proteasome from Methanocaldococcus jannaschii. Mol Cell 34(4):485–496PubMedGoogle Scholar
  46. 46.
    Groll M, Bajorek M, Kohler A, Moroder L et al (2000) A gated channel into the proteasome core particle. Nat Struct Biol 7(11):1062–1067PubMedGoogle Scholar
  47. 47.
    Groll M, Heinemeyer W, Jager S, Ullrich T et al (1999) The catalytic sites of 20S proteasomes and their role in subunit maturation: a mutational and crystallographic study. Proc Natl Acad Sci U S A 96(20):10976–10983PubMedGoogle Scholar
  48. 48.
    Heinemeyer W, Fischer M, Krimmer T, Stachon U et al (1997) The active sites of the eukaryotic 20 S proteasome and their involvement in subunit precursor processing. J Biol Chem 272(40):25200–25209PubMedGoogle Scholar
  49. 49.
    Benaroudj N, Goldberg AL (2000) PAN, the proteasome-activating nucleotidase from archaebacteria, is a protein-unfolding molecular chaperone. Nat Cell Biol 2(11):833–839PubMedGoogle Scholar
  50. 50.
    Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1(8):945–951PubMedGoogle Scholar
  51. 51.
    Darwin KH, Lin G, Chen Z, Li H et al (2005) Characterization of a Mycobacterium tuberculosis proteasomal ATPase homologue. Mol Microbiol 55(2):561–571PubMedGoogle Scholar
  52. 52.
    Wang T, Li H, Lin G, Tang C et al (2009) Structural insights on the Mycobacterium tuberculosis proteasomal ATPase Mpa. Structure 17(10):1377–1385PubMedGoogle Scholar
  53. 53.
    Djuranovic S, Hartmann MD, Habeck M, Ursinus A et al (2009) Structure and activity of the N-terminal substrate recognition domains in proteasomal ATPases. Mol Cell 34(5):580–590PubMedGoogle Scholar
  54. 54.
    Wang T, Darwin KH, Li H (2010) Binding-induced folding of prokaryotic ubiquitin-like protein on the Mycobacterium proteasomal ATPase targets substrates for degradation. Nat Struct Mol Biol 17(11):1352–1357PubMedGoogle Scholar
  55. 55.
    Zhang F, Hu M, Tian G, Zhang P et al (2009) Structural insights into the regulatory particle of the proteasome from Methanocaldococcus jannaschii. Mol Cell 34(4):473–484PubMedGoogle Scholar
  56. 56.
    Smith DM, Kafri G, Cheng Y, Ng D et al (2005) ATP binding to PAN or the 26S ATPases causes association with the 20S proteasome, gate opening, and translocation of unfolded proteins. Mol Cell 20(5):687–698PubMedGoogle Scholar
  57. 57.
    Striebel F, Hunkeler M, Summer H, Weber-Ban E (2010) The mycobacterial Mpa-proteasome unfolds and degrades pupylated substrates by engaging Pup’s N-terminus. EMBO J 29(7):1262–1271PubMedGoogle Scholar
  58. 58.
    Pearce MJ, Arora P, Festa RA, Butler-Wu SM et al (2006) Identification of substrates of the Mycobacterium tuberculosis proteasome. EMBO J 25(22):5423–5432PubMedGoogle Scholar
  59. 59.
    Kusmierczyk AR, Kunjappu MJ, Kim RY, Hochstrasser M (2011) A conserved 20S proteasome assembly factor requires a C-terminal HbYX motif for proteasomal precursor binding. Nat Struct Mol Biol 18(5):622–629PubMedGoogle Scholar
  60. 60.
    Smith DM, Chang SC, Park S, Finley D et al (2007) Docking of the proteasomal ATPases’ carboxyl termini in the 20S proteasome’s alpha ring opens the gate for substrate entry. Mol Cell 27(5):731–744PubMedGoogle Scholar
  61. 61.
    Hochstrasser M (1996) Ubiquitin-dependent protein degradation. Annu Rev Genet 30:405–439PubMedGoogle Scholar
  62. 62.
    Vijay-Kumar S, Bugg CE, Wilkinson KD, Cook WJ (1985) Three-dimensional structure of ubiquitin at 2.8 A resolution. Proc Natl Acad Sci U S A 82(11):3582–3585PubMedGoogle Scholar
  63. 63.
    Wilkinson KD (1997) Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J 11(14):1245–1256PubMedGoogle Scholar
  64. 64.
    Ozkaynak E, Finley D, Solomon MJ, Varshavsky A (1987) The yeast ubiquitin genes: a family of natural gene fusions. EMBO J 6(5):1429–1439PubMedGoogle Scholar
  65. 65.
    Kerscher O, Felberbaum R, Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22:159–180PubMedGoogle Scholar
  66. 66.
    Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479PubMedGoogle Scholar
  67. 67.
    Johnson ES (2004) Protein modification by SUMO. Annu Rev Biochem 73:355–382PubMedGoogle Scholar
  68. 68.
    Rotin D, Kumar S (2009) Physiological functions of the HECT family of ubiquitin ligases. Nat Rev Mol Cell Biol 10(6):398–409PubMedGoogle Scholar
  69. 69.
    Deshaies RJ, Joazeiro CA (2009) RING domain E3 ubiquitin ligases. Annu Rev Biochem 78:399–434PubMedGoogle Scholar
  70. 70.
    Chau V, Tobias JW, Bachmair A, Marriott D et al (1989) A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243(4898):1576–1583PubMedGoogle Scholar
  71. 71.
    Hough R, Rechsteiner M (1986) Ubiquitin-lysozyme conjugates. Purification and susceptibility to proteolysis. J Biol Chem 261(5):2391–2399PubMedGoogle Scholar
  72. 72.
    Scholz O, Thiel A, Hillen W, Niederweis M (2000) Quantitative analysis of gene expression with an improved green fluorescent protein. p6. Eur J Biochem 267(6):1565–1570PubMedGoogle Scholar
  73. 73.
    Karimova G, Pidoux J, Ullmann A, Ladant D (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci U S A 95(10):5752–5756PubMedGoogle Scholar
  74. 74.
    Pearce MJ, Mintseris J, Ferreyra J, Gygi SP et al (2008) Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 322(5904):1104–1107PubMedGoogle Scholar
  75. 75.
    Singh A, Mai D, Kumar A, Steyn AJ (2006) Dissecting virulence pathways of Mycobacterium tuberculosis through protein-protein association. Proc Natl Acad Sci U S A 103(30):11346–11351PubMedGoogle Scholar
  76. 76.
    Burns KE, Liu WT, Boshoff HI, Dorrestein PC et al (2009) Proteasomal protein degradation in Mycobacteria is dependent upon a prokaryotic ubiquitin-like protein. J Biol Chem 284(5):3069–3075PubMedGoogle Scholar
  77. 77.
    Striebel F, Imkamp F, Sutter M, Steiner M et al (2009) Bacterial ubiquitin-like modifier Pup is deamidated and conjugated to substrates by distinct but homologous enzymes. Nat Struct Mol Biol 16(6):647–651PubMedGoogle Scholar
  78. 78.
    Chen X, Solomon WC, Kang Y, Cerda-Maira F et al (2009) Prokaryotic ubiquitin-like protein pup is intrinsically disordered. J Mol Biol 392(1):208–217PubMedGoogle Scholar
  79. 79.
    Sutter M, Striebel F, Damberger FF, Allain FH et al (2009) A distinct structural region of the prokaryotic ubiquitin-like protein (Pup) is recognized by the N-terminal domain of the proteasomal ATPase Mpa. FEBS Lett 583(19):3151–3157PubMedGoogle Scholar
  80. 80.
    Liao S, Shang Q, Zhang X, Zhang J et al (2009) Pup, a prokaryotic ubiquitin-like protein, is an intrinsically disordered protein. Biochem J 422(2):207–215PubMedGoogle Scholar
  81. 81.
    Jackson PK, Eldridge AG, Freed E, Furstenthal L et al (2000) The lore of the RINGs: substrate recognition and catalysis by ubiquitin ligases. Trends Cell Biol 10(10):429–439PubMedGoogle Scholar
  82. 82.
    Festa RA, McAllister F, Pearce MJ, Mintseris J et al (2010) Prokaryotic ubiquitin-like protein (Pup) proteome of Mycobacterium tuberculosis [corrected]. PLoS One 5(1):e8589PubMedGoogle Scholar
  83. 83.
    Watrous J, Burns K, Liu WT, Patel A et al (2010) Expansion of the mycobacterial “PUPylome”. Mol Biosyst 6(2):376–385PubMedGoogle Scholar
  84. 84.
    Poulsen C, Akhter Y, Jeon AH, Schmitt-Ulms G et al (2010) Proteome-wide identification of mycobacterial pupylation targets. Mol Syst Biol 6:386PubMedGoogle Scholar
  85. 85.
    Guth E, Thommen M, Weber-Ban E (2011) Mycobacterial ubiquitin-like protein ligase PafA follows a two-step reaction pathway with a phosphorylated pup intermediate. J Biol Chem 286(6):4412–4419PubMedGoogle Scholar
  86. 86.
    Cerda-Maira FA, McAllister F, Bode NJ, Burns KE et al (2011) Reconstitution of the Mycobacterium tuberculosis pupylation pathway in Escherichia coli. EMBO Rep 12(8):863–870PubMedGoogle Scholar
  87. 87.
    Ghadbane H, Brown AK, Kremer L, Besra GS et al (2007) Structure of Mycobacterium tuberculosis mtFabD, a malonyl-CoA:acyl carrier protein transacylase (MCAT). Acta Crystallogr Sect F Struct Biol Cryst Commun 63(Pt 10):831–835PubMedGoogle Scholar
  88. 88.
    Iyer LM, Burroughs AM, Aravind L (2008) Unraveling the biochemistry and provenance of pupylation: a prokaryotic analog of ubiquitination. Biol Direct 3:45PubMedGoogle Scholar
  89. 89.
    Cerda-Maira FA, Pearce MJ, Fuortes M, Bishai WR et al (2010) Molecular analysis of the prokaryotic ubiquitin-like protein (Pup) conjugation pathway in Mycobacterium tuberculosis. Mol Microbiol 77(5):1123–1135PubMedGoogle Scholar
  90. 90.
    Imkamp F, Rosenberger T, Striebel F, Keller PM et al (2010) Deletion of dop in Mycobacterium smegmatis abolishes pupylation of protein substrates in vivo. Mol Microbiol 75(3):744–754PubMedGoogle Scholar
  91. 91.
    Burns KE, Cerda-Maira FA, Wang T, Li H et al (2010) “Depupylation” of prokaryotic ubiquitin-like protein from mycobacterial proteasome substrates. Mol Cell 39(5):821–827PubMedGoogle Scholar
  92. 92.
    Komander D, Clague MJ, Urbe S (2009) Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 10(8):550–563PubMedGoogle Scholar
  93. 93.
    Imkamp F, Striebel F, Sutter M, Ozcelik D et al (2010) Dop functions as a depupylase in the prokaryotic ubiquitin-like modification pathway. EMBO Rep 11(10):791–797PubMedGoogle Scholar
  94. 94.
    Burns KE, Pearce MJ, Darwin KH (2010) Prokaryotic ubiquitin-like protein provides a two-part degron to Mycobacterium proteasome substrates. J Bacteriol 192(11):2933–2935PubMedGoogle Scholar
  95. 95.
    Lamichhane G, Raghunand TR, Morrison NE, Woolwine SC et al (2006) Deletion of a Mycobacterium tuberculosis proteasomal ATPase homologue gene produces a slow-growing strain that persists in host tissues. J Infect Dis 194(9):1233–1240PubMedGoogle Scholar
  96. 96.
    Gold B, Deng H, Bryk R, Vargas D et al (2008) Identification of a copper-binding metallothionein in pathogenic mycobacteria. Nat Chem Biol 4(10):609–616PubMedGoogle Scholar
  97. 97.
    Gottesman S (2003) Proteolysis in bacterial regulatory circuits. Annu Rev Cell Dev Biol 19:565–587PubMedGoogle Scholar
  98. 98.
    Festa RA, Jones MB, Butler-Wu S, Sinsimer D et al (2011) A novel copper-responsive regulon in Mycobacterium tuberculosis. Mol Microbiol 79(1):133–148PubMedGoogle Scholar
  99. 99.
    Maciag A, Dainese E, Rodriguez GM, Milano A et al (2007) Global analysis of the Mycobacterium tuberculosis Zur (FurB) regulon. J Bacteriol 189(3):730–740PubMedGoogle Scholar
  100. 100.
    Siegrist MS, Unnikrishnan M, McConnell MJ, Borowsky M et al (2009) Mycobacterial Esx-3 is required for mycobactin-mediated iron acquisition. Proc Natl Acad Sci U S A 106(44):18792–18797PubMedGoogle Scholar
  101. 101.
    Serafini A, Boldrin F, Palu G, Manganelli R (2009) Characterization of a Mycobacterium tuberculosis ESX-3 conditional mutant: essentiality and rescue by iron and zinc. J Bacteriol 191(20):6340–6344PubMedGoogle Scholar
  102. 102.
    Nanamiya H, Akanuma G, Natori Y, Murayama R et al (2004) Zinc is a key factor in controlling alternation of two types of L31 protein in the Bacillus subtilis ribosome. Mol Microbiol 52(1):273–283PubMedGoogle Scholar
  103. 103.
    Natori Y, Nanamiya H, Akanuma G, Kosono S et al (2007) A fail-safe system for the ribosome under zinc-limiting conditions in Bacillus subtilis. Mol Microbiol 63(1):294–307PubMedGoogle Scholar
  104. 104.
    Liu T, Ramesh A, Ma Z, Ward SK et al (2007) CsoR is a novel Mycobacterium tuberculosis copper-sensing transcriptional regulator. Nat Chem Biol 3(1):60–68PubMedGoogle Scholar
  105. 105.
    Ward SK, Abomoelak B, Hoye EA, Steinberg H et al (2010) CtpV: a putative copper exporter required for full virulence of Mycobacterium tuberculosis. Mol Microbiol 77(5):1096–1110PubMedGoogle Scholar
  106. 106.
    Ward SK, Hoye EA, Talaat AM (2008) The global responses of Mycobacterium tuberculosis to physiological levels of copper. J Bacteriol 190(8):2939–2946PubMedGoogle Scholar
  107. 107.
    Wolschendorf F, Ackart D, Shrestha TB, Hascall-Dove L et al (2011) Copper resistance is essential for virulence of Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 108(4): 1621–1626PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Marie I. Samanovic
    • 1
  • Huilin Li
    • 2
    • 3
  • K. Heran Darwin
    • 1
  1. 1.Department of MicrobiologyNew York University School of MedicineNew YorkUSA
  2. 2.Department of Biochemistry and Cell BiologyStony Brook UniversityStony BrookUSA
  3. 3.Brookhaven National Laboratory Biology DepartmentBrookhaven National LaboratoryBrookhavenUSA

Personalised recommendations