The PhoP-Dependent ncRNA Mcr7 Modulates the TAT Secretion System in Mycobacterium tuberculosis

PLoS Pathogens

Volumn 10, Issue 5, 2014, Pages

  Solans, Luis ^a,b   Gonzalo Asensio, Jesús ^b,c   Sala, Claudia ^d   Benjak, Andrej ^d   Uplekar, Swapna ^d   Rougemont, Jacques ^d   Guilhot, Christophe ^e,f   Malaga, Wladimir ^e,f   Martín, Carlos ^a,b,c   Cole, Stewart T ^d  

^a UNIVERSITY OF ZARAGOZA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c HOSPITAL UNIVERSITARIO MIGUEL SERVET   (Spain)

^d EPFL   (Switzerland)

^e INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^f UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PHOP PROTEIN; TRANSACTIVATOR PROTEIN; BACTERIAL PROTEIN; BETA LACTAMASE; CARRIER PROTEIN; UNTRANSLATED RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL SECRETION SYSTEM; CHROMATIN IMMUNOPRECIPITATION; CONSENSUS SEQUENCE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; HIGH THROUGHPUT SEQUENCING; MASS SPECTROMETRY; MOLECULAR GENETICS; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NORTHERN BLOTTING; OPEN READING FRAME; PLASMID; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; VALIDATION PROCESS; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MUTATION; OPERON; PATHOGENICITY; PHYSIOLOGY; PROCEDURES; VIRULENCE;

ANIMALS; BACTERIAL PROTEINS; BETA-LACTAMASES; GENE EXPRESSION REGULATION, BACTERIAL; GENE PRODUCTS, TAT; HUMANS; MEMBRANE TRANSPORT PROTEINS; MICE, INBRED C57BL; MUTATION; MYCOBACTERIUM TUBERCULOSIS; OPERON; PROTEOMICS; RNA, UNTRANSLATED; VIRULENCE;

EID: 84901687221     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004183     Document Type: Article

References (64)

1. Ernst JD, (2012) The immunological life cycle of tuberculosis. Nat Rev Immunol 12: 581-591.
2. Russell DG, (2011) Mycobacterium tuberculosis and the intimate discourse of a chronic infection. Immunol Rev 240: 252-268.
3. Bretl DJ, Demetriadou C, Zahrt TC, (2011) Adaptation to environmental stimuli within the host: two-component signal transduction systems of Mycobacterium tuberculosis. Microbiol Mol Biol Rev 75: 566-582.
4. Perez E, Samper S, Bordas Y, Guilhot C, Gicquel B, et al. (2001) An essential role for phoP in Mycobacterium tuberculosis virulence. Mol Microbiol 41: 179-187.
5. Walters SB, Dubnau E, Kolesnikova I, Laval F, Daffe M, et al. (2006) The Mycobacterium tuberculosis PhoPR two-component system regulates genes essential for virulence and complex lipid biosynthesis. Mol Microbiol 60: 312-330.
6. Lee JS, Krause R, Schreiber J, Mollenkopf HJ, Kowall J, et al. (2008) Mutation in the transcriptional regulator PhoP contributes to avirulence of Mycobacterium tuberculosis H37Ra strain. Cell Host Microbe 3: 97-103.
7. Frigui W, Bottai D, Majlessi L, Monot M, Josselin E, et al. (2008) Control of M. tuberculosis ESAT-6 Secretion and Specific T Cell Recognition by PhoP. PLoS Pathogens 4: e33.
8. Gonzalo Asensio J, Maia C, Ferrer NL, Barilone N, Laval F, et al. (2006) The virulence-associated two-component PhoP-PhoR system controls the biosynthesis of polyketide-derived lipids in Mycobacterium tuberculosis. J Biol Chem 281: 1313-1316.
9. Arbues A, Aguilo JI, Gonzalo-Asensio J, Marinova D, Uranga S, et al. (2013) Construction, characterization and preclinical evaluation of MTBVAC, the first live-attenuated M. tuberculosis-based vaccine to enter clinical trials. Vaccine 31: 4867-4873.
10. Menon S, Wang S, (2011) Structure of the response regulator PhoP from Mycobacterium tuberculosis reveals a dimer through the receiver domain. Biochemistry 50: 5948-5957.
11. Gonzalo-Asensio J, Soto CY, Arbues A, Sancho J, del Carmen Menendez M, et al. (2008) The Mycobacterium tuberculosis phoPR Operon Is Positively Autoregulated in the Virulent Strain H37Rv. Journal of Bacteriology 190: 7068-7078.
12. Gupta S, Sinha A, Sarkar D, (2006) Transcriptional autoregulation by Mycobacterium tuberculosis PhoP involves recognition of novel direct repeat sequences in the regulatory region of the promoter. FEBS Lett 580: 5328-5338.
13. Cimino M, Thomas C, Namouchi A, Dubrac S, Gicquel B, et al. (2012) Identification of DNA binding motifs of the Mycobacterium tuberculosis PhoP/PhoR two-component signal transduction system. PLoS One 7: e42876.
14. Gonzalo-Asensio J, Mostowy S, Harders-Westerveen J, Huygen K, Hernandez-Pando R, et al. (2008) PhoP: a missing piece in the intricate puzzle of Mycobacterium tuberculosis virulence. PLoS One 3: e3496.
15. Galagan JE, Minch K, Peterson M, Lyubetskaya A, Azizi E, et al. (2013) The Mycobacterium tuberculosis regulatory network and hypoxia. Nature 499: 178-183.
16. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544.
17. Uplekar S, Rougemont J, Cole ST, Sala C, (2013) High-resolution transcriptome and genome-wide dynamics of RNA polymerase and NusA in Mycobacterium tuberculosis. Nucleic Acids Res 41: 961-977.
18. Roback P, Beard J, Baumann D, Gille C, Henry K, et al. (2007) A predicted operon map for Mycobacterium tuberculosis. Nucleic Acids Res 35: 5085-5095.
19. Price MN, Huang KH, Alm EJ, Arkin AP, (2005) A novel method for accurate operon predictions in all sequenced prokaryotes. Nucleic Acids Res 33: 880-892.
20. DiChiara JM, Contreras-Martinez LM, Livny J, Smith D, McDonough KA, et al. (2010) Multiple small RNAs identified in Mycobacterium bovis BCG are also expressed in Mycobacterium tuberculosis and Mycobacterium smegmatis. Nucleic Acids Res 38: 4067-4078.
21. Caminero JA, Pena MJ, Campos-Herrero MI, Rodriguez JC, Garcia I, et al. (2001) Epidemiological evidence of the spread of a Mycobacterium tuberculosis strain of the Beijing genotype on Gran Canaria Island. Am J Respir Crit Care Med 164: 1165-1170.
22. Gottesman S, Storz G (2011) Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol 3.
23. Romilly C, Chevalier C, Marzi S, Masquida B, Geissmann T, et al. (2012) Loop-loop interactions involved in antisense regulation are processed by the endoribonuclease III in Staphylococcus aureus. RNA Biol 9: 1461-1472.
24. Saint-Joanis B, Demangel C, Jackson M, Brodin P, Marsollier L, et al. (2006) Inactivation of Rv2525c, a substrate of the twin arginine translocation (Tat) system of Mycobacterium tuberculosis, increases beta-lactam susceptibility and virulence. J Bacteriol 188: 6669-6679.
25. Palmer T, Berks BC, (2012) The twin-arginine translocation (Tat) protein export pathway. Nat Rev Microbiol 10: 483-496.
26. Marrichi M, Camacho L, Russell DG, DeLisa MP, (2008) Genetic toggling of alkaline phosphatase folding reveals signal peptides for all major modes of transport across the inner membrane of bacteria. J Biol Chem 283: 35223-35235.
27. Dilks K, Rose RW, Hartmann E, Pohlschroder M, (2003) Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey. J Bacteriol 185: 1478-1483.
28. McDonough JA, Hacker KE, Flores AR, Pavelka MS Jr, Braunstein M, (2005) The twin-arginine translocation pathway of Mycobacterium smegmatis is functional and required for the export of mycobacterial beta-lactamases. J Bacteriol 187: 7667-7679.
29. Arnvig KB, Comas I, Thomson NR, Houghton J, Boshoff HI, et al. (2011) Sequence-based analysis uncovers an abundance of non-coding RNA in the total transcriptome of Mycobacterium tuberculosis. PLoS Pathog 7: e1002342.
30. Blasco B, Chen JM, Hartkoorn R, Sala C, Uplekar S, et al. (2012) Virulence regulator EspR of Mycobacterium tuberculosis is a nucleoid-associated protein. PLoS Pathog 8: e1002621.
31. Singh A, Crossman DK, Mai D, Guidry L, Voskuil MI, et al. (2009) Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathog 5: e1000545.
32. Raghavan S, Manzanillo P, Chan K, Dovey C, Cox JS, (2008) Secreted transcription factor controls Mycobacterium tuberculosis virulence. Nature 454: 717-721.
33. Kroger C, Dillon SC, Cameron AD, Papenfort K, Sivasankaran SK, et al. (2012) The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc Natl Acad Sci U S A 109: E1277-1286.
34. Sahr T, Bruggemann H, Jules M, Lomma M, Albert-Weissenberger C, et al. (2009) Two small ncRNAs jointly govern virulence and transmission in Legionella pneumophila. Mol Microbiol 72: 741-762.
35. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, et al. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature 459: 950-956.
36. 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.
37. Abramovitch RB, Rohde KH, Hsu FF, Russell DG, (2011) aprABC: a Mycobacterium tuberculosis complex-specific locus that modulates pH-driven adaptation to the macrophage phagosome. Mol Microbiol 80: 678-694.
38. Fleischmann RD, Alland D, Eisen JA, Carpenter L, White O, et al. (2002) Whole-genome comparison of Mycobacterium tuberculosis clinical and laboratory strains. J Bacteriol 184: 5479-5490.
39. Brosch R, Gordon SV, Marmiesse M, Brodin P, Buchrieser C, et al. (2002) A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci U S A 99: 3684-3689.
40. Gu S, Chen J, Dobos KM, Bradbury EM, Belisle JT, et al. (2003) Comprehensive proteomic profiling of the membrane constituents of a Mycobacterium tuberculosis strain. Mol Cell Proteomics 2: 1284-1296.
41. Mawuenyega KG, Forst CV, Dobos KM, Belisle JT, Chen J, et al. (2005) Mycobacterium tuberculosis functional network analysis by global subcellular protein profiling. Mol Biol Cell 16: 396-404.
42. Malen H, Pathak S, Softeland T, de Souza GA, Wiker HG, (2010) Definition of novel cell envelope associated proteins in Triton X-114 extracts of Mycobacterium tuberculosis H37Rv. BMC Microbiol 10: 132.
43. Schubert OT, Mouritsen J, Ludwig C, Rost HL, Rosenberger G, et al. (2013) The Mtb proteome library: a resource of assays to quantify the complete proteome of Mycobacterium tuberculosis. Cell Host Microbe 13: 602-612.
44. Naito M, Ohara N, Matsumoto S, Yamada T, (1998) The novel fibronectin-binding motif and key residues of mycobacteria. J Biol Chem 273: 2905-2909.
45. Kuo CJ, Bell H, Hsieh CL, Ptak CP, Chang YF, (2012) Novel mycobacteria antigen 85 complex binding motif on fibronectin. J Biol Chem 287: 1892-1902.
46. Garnier T, Eiglmeier K, Camus JC, Medina N, Mansoor H, et al. (2003) The complete genome sequence of Mycobacterium bovis. Proc Natl Acad Sci U S A 100: 7877-7882.
47. Malaga W, Constant P, Euphrasie D, Cataldi A, Daffe M, et al. (2008) Deciphering the genetic bases of the structural diversity of phenolic glycolipids in strains of the Mycobacterium tuberculosis complex. J Biol Chem 283: 15177-15184.
48. Stover CK, de la Cruz VF, Fuerst TR, Burlein JE, Benson LA, et al. (1991) New use of BCG for recombinant vaccines. Nature 351: 456-460.
49. Sala C, Haouz A, Saul FA, Miras I, Rosenkrands I, et al. (2009) Genome-wide regulon and crystal structure of BlaI (Rv1846c) from Mycobacterium tuberculosis. Mol Microbiol 71: 1102-1116.
50. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
51. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137.
52. Dreszer TR, Karolchik D, Zweig AS, Hinrichs AS, Raney BJ, et al. (2012) The UCSC Genome Browser database: extensions and updates 2011. Nucleic Acids Res 40: D918-923.
53. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, et al. (2010) The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464: 250-255.
54. Langmead B, Salzberg SL, (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359.
55. Anders S, Huber W, (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.
56. Boersema PJ, Raijmakers R, Lemeer S, Mohammed S, Heck AJ, (2009) Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc 4: 484-494.
57. Wisniewski JR, Zougman A, Mann M, (2009) Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome. J Proteome Res 8: 5674-5678.
58. Cox J, Matic I, Hilger M, Nagaraj N, Selbach M, et al. (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat Protoc 4: 698-705.
59. Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, et al. (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 10: 1794-1805.
60. Lew JM, Kapopoulou A, Jones LM, Cole ST, (2011) TubercuList-10 years after. Tuberculosis (Edinb) 91: 1-7.
61. Chen JM, Zhang M, Rybniker J, Basterra L, Dhar N, et al. (2013) Phenotypic profiling of Mycobacterium tuberculosis EspA point mutants reveals that blockage of ESAT-6 and CFP-10 secretion in vitro does not always correlate with attenuation of virulence. J Bacteriol 195: 5421-5430.
62. Kolly GS, Boldrin F, Sala C, Dhar N, Hartkoorn RC, et al. (2014) Assessing the essentiality of the decaprenyl-phospho-d-arabinofuranose pathway in Mycobacterium tuberculosis using conditional mutants. Mol Microbiol 92: 194-211.
63. Edgar R, Domrachev M, Lash AE, (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210.
64. Vizcaino JA, Cote RG, Csordas A, Dianes JA, Fabregat A, et al. (2013) The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res 41: D1063-1069.