Iron-sparing response of mycobacterium avium subsp. paratuberculosis is strain dependent

BMC Microbiology

Volumn 10, Issue , 2010, Pages

  Janagama, Harish K ^a   Senthilkumar, ^a,c   Bannantine, John P ^b   Kugadas, Abirami ^a   Jagtap, Pratik ^a   Higgins, Leeann ^a   Witthuhn, Bruce A ^a   Sreevatsan, Srinand ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b NATIONAL ANIMAL DISEASE CENTER   (United States)

^c MADRAS VETERINARY COLLEGE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ACONITATE HYDRATASE; IRON; RIBOSOME PROTEIN; SUCCINATE DEHYDROGENASE;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CATTLE; CELL DIVISION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENOTYPE; IRON STORAGE; IRON TRANSPORT; MICROARRAY ANALYSIS; MICROBIOLOGICAL EXAMINATION; MYCOBACTERIUM AVIUM; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PROTEIN FUNCTION; PROTEOMICS; SHEEP; TRANSCRIPTION REGULATION; UPREGULATION;

ANTI-BACTERIAL AGENTS; CULTURE MEDIA; IRON; METABOLIC NETWORKS AND PATHWAYS; MICROARRAY ANALYSIS; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS; MYCOBACTERIUM SMEGMATIS; PROTEOME; SPECIES SPECIFICITY; TRANSCRIPTOME;

BOS; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS; OVIS ARIES;

EID: 77958049099     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-10-268     Document Type: Article

References (55)

1. Mycobacterium paratuberculosis. Factors that influence mycobactin dependence. RS Lambrecht MT Collins, Diagn Microbiol Infect Dis 1992 15 3 239 246 10.1016/0732-8893(92)90119-E 1582168
2. Inability to detect mycobactin in mycobacteria-infected tissues suggests an alternative iron acquisition mechanism by mycobacteria in vivo. RS Lambrecht MT Collins, Microb Pathog 1993 14 3 229 238 10.1006/mpat.1993.1022 8321124
3. Mycobactins: iron-chelating growth factors from mycobacteria. GA Snow, Bacteriol Rev 1970 34 2 99 125 4918634
4. Identification and functional characterization of the iron-dependent regulator (IdeR) of Mycobacterium avium subsp. paratuberculosis. HK Janagama TM Senthilkumar JP Bannantine GM Rodriguez I Smith ML Paustian JA McGarvey S Sreevatsan, Microbiology 2009 155 Pt 11 3683 3690 10.1099/mic.0.031948-0 19684064
5. Microarray analysis of whole genome expression of intracellular Mycobacterium tuberculosis. SJ Waddell PD Butcher, Curr Mol Med 2007 7 3 287 296 10.2174/156652407780598548 17504113
6. Protein turnover in mycobacterial proteomics. PK Rao Q Li, Molecules 2009 14 9 3237 3258 10.3390/molecules14093237 19783922
7. Determination of global protein turnover in stressed mycobacterium cells using hybrid-linear ion trap-fourier transform mass spectrometry. PK Rao BA Roxas Q Li, Anal Chem 2008 80 2 396 406 10.1021/ac701690d 18085750
8. Principal Component Analysis of Proteome Dynamics in Iron-starved Mycobacterium Tuberculosis. PK Rao Q Li, J Proteomics Bioinform 2009 2 1 19 31 10.4172/jpb.1000058 19436767
9. Transcriptional profiling of Legionella pneumophila biofilm cells and the influence of iron on biofilm formation. T Hindre H Bruggemann C Buchrieser Y Hechard, Microbiology 2008 154 Pt 1 30 41 10.1099/mic.0.2007/008698-0 18174123
10. Analysis of the growth pattern, survival and proteome of Mycobacteriumavium subsp. paratuberculosis following exposure to heat. S Gumber RJ Whittington, Vet Microbiol 2009 136 1-2 82 90 10.1016/j.vetmic.2008.10.003 19019575
11. Growth pattern and partial proteome of Mycobacterium avium subsp. paratuberculosis during the stress response to hypoxia and nutrient starvation. S Gumber DL Taylor IB Marsh RJ Whittington, Vet Microbiol 2009 133 4 344 357 10.1016/j.vetmic.2008.07.021 18786786
12. Defining the stressome of Mycobacterium avium subsp. paratuberculosis in vitro and in naturally infected cows. CW Wu SK Schmoller SJ Shin AM Talaat, J Bacteriol 2007 189 21 7877 7886 10.1128/JB.00780-07 17693514
13. Control of iron metabolism in Mycobacterium tuberculosis. GM Rodriguez, Trends Microbiol 2006 14 7 320 327 10.1016/j.tim.2006.05.006 16759864
14. Molecular epidemiology of Mycobacterium avium subsp. paratuberculosis: evidence for limited strain diversity, strain sharing, and identification of unique targets for diagnosis. AS Motiwala M Strother A Amonsin B Byrum SA Naser JR Stabel WP Shulaw JP Bannantine V Kapur S Sreevatsan, J Clin Microbiol 2003 41 5 2015 2026 10.1128/JCM.41.5.2015-2026.2003 12734243
15. Rapid detection and typing of strains of Mycobacterium avium subsp. paratuberculosis from broth cultures. AS Motiwala M Strother NE Theus RW Stich B Byrum WP Shulaw V Kapur S Sreevatsan, J Clin Microbiol 2005 43 5 2111 2117 10.1128/JCM.43.5.2111-2117.2005 15872229
16. Genomic comparison of Mycobacterium avium subsp. paratuberculosis sheep and cattle strains by microarray hybridization. IB Marsh JP Bannantine ML Paustian ML Tizard V Kapur RJ Whittington, J Bacteriol 2006 188 6 2290 2293 10.1128/JB.188.6.2290-2293.2006 16513760
17. Genomic diversity in Mycobacterium avium: single nucleotide polymorphisms between the S and C strains of M. avium subsp. paratuberculosis and with M. a. avium. IB Marsh RJ Whittington, Mol Cell Probes 2007 21 1 66 75 10.1016/j.mcp.2006.08.002 17049206
18. Comparative genomic analysis of Mycobacterium avium subspecies obtained from multiple host species. ML Paustian X Zhu S Sreevatsan S Robbe-Austerman V Kapur JP Bannantine, BMC Genomics 2008 9 135 10.1186/1471-2164-9-135 18366709
19. Comparative genomic hybridizations reveal genetic regions within the Mycobacterium avium complex that are divergent from Mycobacterium avium subsp. paratuberculosis isolates. ML Paustian V Kapur JP Bannantine, J Bacteriol 2005 187 7 2406 2415 10.1128/JB.187.7.2406-2415.2005 15774884
20. Mycobacterium avium subsp. paratuberculosis and M. avium subsp. avium are independently evolved pathogenic clones of a much broader group of M. avium organisms. CY Turenne DM Collins DC Alexander MA Behr, J Bacteriol 2008 190 7 2479 2487 10.1128/JB.01691-07 18245284
21. Sequencing of hsp65 distinguishes among subsets of the Mycobacterium avium complex. CY Turenne M Semret DV Cousins DM Collins MA Behr, J Clin Microbiol 2006 44 2 433 440 10.1128/JCM.44.2.433-440.2006 16455896
22. Insertion and deletion events that define the pathogen Mycobacterium avium subsp. paratuberculosis. DC Alexander CY Turenne MA Behr, J Bacteriol 2009 191 3 1018 1025 10.1128/JB.01340-08 19028885
23. Whole-genome plasticity among Mycobacterium avium subspecies: insights from comparative genomic hybridizations. CW Wu J Glasner M Collins S Naser AM Talaat, J Bacteriol 2006 188 2 711 723 10.1128/JB.188.2.711-723.2006 16385061
24. Comparative transcriptional analysis of human macrophages exposed to animal and human isolates of Mycobacterium avium subspecies paratuberculosis with diverse genotypes. AS Motiwala HK Janagama ML Paustian X Zhu JP Bannantine V Kapur S Sreevatsan, Infect Immun 2006 74 11 6046 6056 10.1128/IAI.00326-06 17057086
25. Cytokine responses of bovine macrophages to diverse clinical Mycobacterium avium subspecies paratuberculosis strains. HK Janagama K Jeong V Kapur P Coussens S Sreevatsan, BMC Microbiol 2006 6 10 10.1186/1471-2180-6-10 16478544
26. ideR, An essential gene in mycobacterium tuberculosis: role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response. GM Rodriguez MI Voskuil B Gold GK Schoolnik I Smith, Infect Immun 2002 70 7 3371 3381 10.1128/IAI.70.7.3371-3381.2002 12065475
27. Biomarker discovery in subclinical mycobacterial infections of cattle. M Seth EA Lamont HK Janagama A Widdel L Vulchanova JR Stabel WR Waters MV Palmer S Sreevatsan, PLoS One 2009 4 5 5478 10.1371/journal.pone.0005478 19424492
28. Temporal stability of the urinary proteome after kidney transplant: more sensitive than protein composition? SK Akkina Y Zhang GL Nelsestuen WS Oetting HN Ibrahlm, J Proteome Res 2009 8 1 94 103 10.1021/pr800646j 19012427
29. The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. IV Shilov SL Seymour AA Patel A Loboda WH Tang SP Keating CL Hunter LM Nuwaysir DA Schaeffer, Mol Cell Proteomics 2007 6 9 1638 1655 10.1074/mcp.T600050-MCP200 17533153
30. Mycobacterial Esx-3 is required for mycobactin-mediated iron acquisition. MS Siegrist M Unnikrishnan MJ McConnell M Borowsky TY Cheng N Siddiqi SM Fortune DB Moody EJ Rubin, Proc Natl Acad Sci USA 2009 106 44 18792 18797 10.1073/pnas.0900589106 19846780
31. Protein dynamics in iron-starved Mycobacterium tuberculosis revealed by turnover and abundance measurement using hybrid-linear ion trap-Fourier transform mass spectrometry. PK Rao GM Rodriguez I Smith Q Li, Anal Chem 2008 80 18 6860 6869 10.1021/ac800288t 18690695
32. Mycobacterium tuberculosis WhiB3 responds to O2 and nitric oxide via its [4Fe-4S] cluster and is essential for nutrient starvation survival. A Singh L Guidry KV Narasimhulu D Mai J Trombley KE Redding GI Giles JR Lancaster Jr AJ Steyn, Proc Natl Acad Sci USA 2007 104 28 11562 11567 10.1073/pnas.0700490104 17609386
33. A specific secretion system mediates PPE41 transport in pathogenic mycobacteria. AM Abdallah T Verboom F Hannes M Safi M Strong D Eisenberg RJ Musters CM Vandenbroucke-Grauls BJ Appelmelk J Luirink,, et al. Mol Microbiol 2006 62 3 667 679 10.1111/j.1365-2958.2006.05409.x 17076665
34. The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins. A Gaballa H Antelmann C Aguilar SK Khakh KB Song GT Smaldone JD Helmann, Proc Natl Acad Sci USA 2008 18697947
35. RyhB small RNA modulates the free intracellular iron pool and is essential for normal growth during iron limitation in Escherichia coli. JF Jacques S Jang K Prevost G Desnoyers M Desmarais J Imlay E Masse, Mol Microbiol 2006 62 4 1181 1190 10.1111/j.1365-2958.2006.05439.x 17078818
36. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. E Masse S Gottesman, Proc Natl Acad Sci USA 2002 99 7 4620 4625 10.1073/pnas.032066599 11917098
37. The Mycobacterium avium subsp. paratuberculosis 35 kDa protein plays a role in invasion of bovine epithelial cells. JP Bannantine JF Huntley E Miltner JR Stabel LE Bermudez, Microbiology 2003 149 Pt 8 2061 2069 10.1099/mic.0.26323- 0 12904546
38. Production and characterization of monoclonal antibodies against a major membrane protein of Mycobacterium avium subsp. paratuberculosis. JP Bannantine TJ Radosevich JR Stabel S Berger JF Griffin ML Paustian, Clin Vaccine Immunol 2007 14 3 312 317 10.1128/CVI.00353-06 17267586
39. Growth and metabolic characteristics of Mycobacterium paratuberculosis. RS Merkal BJ Curran, Appl Microbiol 1974 28 2 276 279 4859342
40. Current understanding of the genetic diversity of Mycobacterium avium subsp. paratuberculosis. AS Motiwala L Li V Kapur S Sreevatsan, Microbes Infect 2006 8 5 1406 1418 10.1016/j.micinf.2005.12.003 16697677
41. Effect of egg yolk on the detection of Mycobacterium avium subsp. paratuberculosis using the ESP II liquid culture system. NB Harris S Robbe-Austerman JB Payeur, J Vet Diagn Invest 2005 17 6 554 560 16475513
42. Progress towards understanding the spread, detection and control of Mycobacterium avium subsp paratuberculosis in animal populations. RJ Whittington ES Sergeant, Aust Vet J 2001 79 4 267 278 10.1111/j.1751-0813.2001.tb11980.x 11349414
43. Bacterial iron sources: from siderophores to hemophores. C Wandersman P Delepelaire, Annu Rev Microbiol 2004 58 611 647 10.1146/annurev.micro.58.030603. 123811 15487950
44. Small RNAs controlling iron metabolism. E Masse H Salvail G Desnoyers M Arguin, Curr Opin Microbiol 2007 10 2 140 145 10.1016/j.mib.2007.03.013 17383226
45. Role and regulation of iron-sulfur cluster biosynthesis genes in Shigella flexneri virulence. L Runyen-Janecky A Daugherty B Lloyd C Wellington H Eskandarian M Sagransky, Infect Immun 2008 76 3 1083 1092 10.1128/IAI.01211-07 18195027
46. Mechanisms of iron-sulfur cluster assembly: the SUF machinery. M Fontecave SO Choudens B Py F Barras, J Biol Inorg Chem 2005 10 7 713 721 10.1007/s00775-005-0025-1 16211402
47. Identification of the Mycobacterium tuberculosis SUF machinery as the exclusive mycobacterial system of [Fe-S] cluster assembly: evidence for its implication in the pathogen's survival. G Huet M Daffe I Saves, J Bacteriol 2005 187 17 6137 6146 10.1128/JB.187.17.6137-6146.2005 16109955
48. Functional characterization of a vitamin B12-dependent methylmalonyl pathway in Mycobacterium tuberculosis: implications for propionate metabolism during growth on fatty acids. S Savvi DF Warner BD Kana JD McKinney V Mizrahi SS Dawes, J Bacteriol 2008 190 11 3886 3895 10.1128/JB.01767-07 18375549
49. Characterization of the Mycobacterium tuberculosis 4-diphosphocytidyl-2- C-methyl-D-erythritol synthase: potential for drug development. H Eoh AC Brown L Buetow WN Hunter T Parish D Kaur PJ Brennan DC Crick, J Bacteriol 2007 189 24 8922 8927 10.1128/JB.00925-07 17921290
50. Structure and proposed activity of a member of the VapBC family of toxin-antitoxin systems. VapBC-5 from Mycobacterium tuberculosis. L Miallau M Faller J Chiang M Arbing F Guo D Cascio D Eisenberg, J Biol Chem 2009 284 1 276 283 10.1074/jbc.M805061200 18952600
51. CarD is an essential regulator of rRNA transcription required for Mycobacterium tuberculosis persistence. CL Stallings NC Stephanou L Chu A Hochschild BE Nickels MS Glickman, Cell 2009 138 1 146 159 10.1016/j.cell.2009. 04.041 19596241
52. Eis (enhanced intracellular survival) protein of Mycobacterium tuberculosis disturbs the cross regulation of T-cells. RK Lella C Sharma, J Biol Chem 2007 282 26 18671 18675 10.1074/jbc.C600280200 17449476
53. Bacterial heme oxygenases. N Frankenberg-Dinkel, Antioxid Redox Signal 2004 6 5 825 834 15345142
54. Unusual diheme conformation of the heme-degrading protein from Mycobacterium tuberculosis. N Chim A Iniguez TQ Nguyen CW Goulding, J Mol Biol 395 3 595 608 10.1016/j.jmb.2009.11.025 19917297
55. Differential role of ferritins in iron metabolism and virulence of the plant-pathogenic bacterium Erwinia chrysanthemi 3937. A Boughammoura BF Matzanke L Bottger S Reverchon E Lesuisse D Expert T Franza, J Bacteriol 2008 190 5 1518 1530 10.1128/JB.01640-07 18165304