Acid stress response of a mycobacterial proteome: Insight from a gene ontology analysis

International Journal of Clinical and Experimental Medicine

Volumn 2, Issue 4, 2009, Pages 309-328

  Roxas, Bryan A P ^a,c   Li, Qingbo ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

Acid stress; Gene ontology; Label free proteomics; Membrane transport; Mycobacterium smegmatis; Systems biology

Indexed keywords

FATTY ACID;

ACID TOLERANCE; ACIDITY; ADAPTATION; ARTICLE; DOWN REGULATION; ENZYME REGULATION; FATTY ACID METABOLISM; MEMBRANE POTENTIAL; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PROTEIN ANALYSIS; PROTEOMICS; QUANTITATIVE ANALYSIS; STRESS;

CORYNEBACTERINEAE; MYCOBACTERIUM SMEGMATIS;

EID: 74549162675     PISSN: None     EISSN: 19405901     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Hestvik AL, Hmama Z and Av-Gay Y. Mycobacterial manipulation of the host cell. FEMS Microbiol Rev 2005; 29: 1041-1050.
2. Crowle AJ, Dahl R, Ross E and May MH. Evidence that vesicles containing living, virulent Mycobacterium tuberculosis or Mycobacterium avium in cultured human macrophages are not acidic. Infect Immun 1991; 59: 1823-1831.
3. Sturgill-Koszycki S, Schlesinger PH, Chakraborty P, Haddix PL, Collins HL, Fok AK, Allen RD, Gluck SL, Heuser J and Russell DG. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 1994; 263: 678-681.
4. Brown CA, Draper P and Hart PD. Mycobacteria and lysosomes: a paradox. Nature 1969; 221: 658-660.
5. Vandal OH, Pierini LM, Schnappinger D, Nathan CF and Ehrt S. A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat Med 2008; 14: 849-854.
6. McDonough KA, Kress Y and Bloom BR. Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages. Infect Immun 1993; 61: 2763-2773.
7. McDonough KA, Florczyk MA and Kress Y. Intracellular passage within macrophages affects the trafficking of virulent tubercle bacilli upon reinfection of other macrophages in a serum-dependent manner. Tuber Lung Dis 2000; 80: 259-271.
8. Singh AK and Reyrat JM. Laboratory maintenance of Mycobacterium smegmatis. Curr Protoc Microbiol 2009; Chapter 10: Unit10C 11.
9. Jhamb SS and Singh PP. A short-term model for preliminary screening of potential anti-tubercular compounds. Scand J Infect Dis 2009; 1-4.
10. Purdy GE, Niederweis M and Russell DG. Decreased outer membrane permeability protects mycobacteria from killing by ubiquitin-derived peptides. Mol Microbiol 2009; 73: 844-857.
11. Lee JM, Cho HY, Cho HJ, Ko IJ, Park SW, Baik HS, Oh JH, Eom CY, Kim YM, Kang BS and Oh JI. O2- and NO-sensing mechanism through the DevSR two-component system in Mycobacterium smegmatis. J Bacteriol 2008; 190: 6795-6804.
12. Anes E, Peyron P, Staali L, Jordao L, Gutierrez MG, Kress H, Hagedorn M, Maridonneau-Parini I, Skinner MA, Wildeman AG, Kalamidas SA, Kuehnel M and Griffiths G. Dynamic life and death interactions between Mycobacterium smegmatis and J774 macrophages. Cell Microbiol 2006; 8: 939-960.
13. Li Q and Roxas BA. An assessment of false discovery rates and statistical significance in label-free quantitative proteomics with combined filters. BMC Bioinformatics 2009; 10: 43.
14. Roxas BA and Li Q. Significance analysis of microarray for relative quantitation of LC/MS data in proteomics. BMC Bioinformatics 2008; 9: 187.
15. Rao PK, Rodriguez GM, Smith I and Li Q. Protein dynamics in iron-starved Mycobacterium tuberculosis revealed by turnover and abundance measurement using hybrid-linear ion trap-fourier transform mass spectrometry. Anal Chem 2008; 80: 6860-6869.
16. Andreev VP, Li L, Cao L, Gu Y, Rejtar T, Wu SL and Karger BL. A new algorithm using cross-assignment for label-free quantitation with LC-LTQ-FT MS. J Proteome Res 2007; 6: 2186-2194.
17. Rao PK, Singh CR, Jagannath C and Li Q. A systems biology approach to study the phagosomal proteome modulated by mycobacterial infections. Int J Clin Exp Med 2009; 2: 233-247.
18. Katti MK, Dai G, Armitige LY, Rivera Marrero C, Daniel S, Singh CR, Lindsey DR, Dhandayuthapani S, Hunter RL and Jagannath C. The Delta fbpA mutant derived from Mycobacterium tuberculosis H37Rv has an enhanced susceptibility to intracellular antimicrobial oxidative mechanisms, undergoes limited phagosome maturation and activates macrophages and dendritic cells. Cell Microbiol 2008; 10: 1286-1303.
19. Geisow MJ, D'Arcy Hart P and Young MR. Temporal changes of lysosome and phagosome pH during phagolysosome formation in macrophages: studies by fluorescence spectroscopy. J Cell Biol 1981; 89: 645-652.
20. Pethe K, Swenson DL, Alonso S, Anderson J, Wang C and Russell DG. Isolation of Mycobacterium tuberculosis mutants defective in the arrest of phagosome maturation. Proc Natl Acad Sci U S A 2004; 101: 13642-13647.
21. Rao PK, Roxas BA and Li Q. Determination of global protein turnover in stressed mycobacterium cells using hybrid-linear ion trap-fourier transform mass spectrometry. Anal Chem 2008; 80: 396-406.
22. http://string.embl.de/.
23. O'Toole R, Smeulders MJ, Blokpoel MC, Kay EJ, Lougheed K and Williams HD. A two-component regulator of universal stress protein expression and adaptation to oxygen starvation in Mycobacterium smegmatis. J Bacteriol 2003; 185: 1543-1554.
24. Roback P, Beard J, Baumann D, Gille C, Henry K, Krohn S, Wiste H, Voskuil MI, Rainville C and Rutherford R. A predicted operon map for Mycobacterium tuberculosis. Nucleic Acids Res 2007; 35: 5085-5095.
25. Matsoso LG, Kana BD, Crellin PK, Lea-Smith DJ, Pelosi A, Powell D, Dawes SS, Rubin H, Coppel RL and Mizrahi V. Function of the cytochrome bc1-aa3 branch of the respiratory network in mycobacteria and network adaptation occurring in response to its disruption. J Bacteriol 2005; 187: 6300-6308.
26. Mayuri, Bagchi G, Das TK and Tyagi JS. Molecular analysis of the dormancy response in Mycobacterium smegmatis: expression analysis of genes encoding the DevR-DevS two-component system, Rv3134c and chaperone alpha-crystallin homologues. FEMS Microbiol Lett 2002; 211: 231-237.
27. Sinha S, Rappu P, Lange SC, Mantsala P, Zalkin H and Smith JL. Crystal structure of Bacillus subtilis YabJ, a purine regulatory protein and member of the highly conserved YjgF family. Proc Natl Acad Sci U S A 1999; 96: 13074-13079.
28. Dietrich LE, Teal TK, Price-Whelan A and Newman DK. Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 2008; 321: 1203-1206.
29. Cundliffe E. How antibiotic-producing organisms avoid suicide. Annu Rev Microbiol 1989; 43: 207-233.
30. Morishita R, Kawagoshi A, Sawasaki T, Madin K, Ogasawara T, Oka T and Endo Y. Ribonuclease activity of rat liver perchloric acid-soluble protein, a potent inhibitor of protein synthesis. J Biol Chem 1999; 274: 20688-20692.
31. Cashman JR. Role of flavin-containing monooxygenase in drug development. Expert Opin Drug Metab Toxicol 2008; 4: 1507-1521.
32. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM and Sherlock G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000; 25: 25-29.
33. ftp://ftp.ebi.ac.uk/pub/databases/GO/goa/.
34. Maere S, Heymans K and Kuiper M. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 2005; 21: 3448-3449.
35. http://www.cytoscape.org/.
36. Postma PW, Lengeler JW and Jacobson GR. Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 1993; 57: 543-594.
37. Kights KM. Long-Chain-Fatty-Acid CoA Ligases: The Key to Fatty Acid Activation, Formation of Xenobiotic Acyl-CoA Thioesters and Lipophilic Xenobiotic Conjugates. Current Medicinal Chemistry - Immunology, Endocrine & Metabolic Agents 2003; 3: 235-244.
38. Deb C, Lee CM, Dubey VS, Daniel J, Abomoelak B, Sirakova TD, Pawar S, Rogers L and Kolattukudy PE. A novel in vitro multiple-stress dormancy model for Mycobacterium tuberculosis generates a lipid-loaded, drug-tolerant, dormant pathogen. PLoS One 2009; 4: e6077.
39. Fisher MA, Plikaytis BB and Shinnick TM. Microarray analysis of the Mycobacterium tuberculosis transcriptional response to the acidic conditions found in phagosomes. J Bacteriol 2002; 184: 4025-4032.
40. Xia Q, Hendrickson EL, Zhang Y, Wang T, Taub F, Moore BC, Porat I, Whitman WB, Hackett M and Leigh JA. Quantitative proteomics of the archaeon Methanococcus maripaludis validated by microarray analysis and real time PCR. Mol Cell Proteomics 2006; 5: 868-881.
41. Li Q. Advances in protein turnover analysis at the global level and biological insights. Mass Spectrom Rev 2009; Sep 15 [Epub ahead of print].
42. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, Monahan IM, Dolganov G, Efron B, Butcher PD, Nathan C and Schoolnik GK. Transcriptional Adaptation of Mycobacterium tuberculosis within Macrophages: Insights into the Phagosomal Environment. J Exp Med 2003; 198: 693-704.
43. Gillespie E. Effects of S-lactoylglutathione and inhibitors of glyoxalase I on histamine release from human leukocytes. Nature 1979; 277: 135-137.
44. Kim NS, Umezawa Y, Ohmura S and Kato S. Human glyoxalase I. cDNA cloning, expression, and sequence similarity to glyoxalase I from Pseudomonas putida. J Biol Chem 1993; 268: 11217-11221.
45. Thornalley PJ. Glyoxalase I - structure, function and a critical role in the enzymatic defence against glycation. Biochem Soc Trans 2003; 31: 1343-1348.
46. Hao da C, Chen SL, Mu J and Xiao PG. Molecular phylogeny, long-term evolution, and functional divergence of flavin-containing monooxygenases. Genetica 2009; 137: 173-187.
47. Betts JC, Lukey PT, Robb LC, McAdam RA and Duncan K. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol Microbiol 2002; 43: 717-731.
48. Qian L and Ortiz de Montellano PR. Oxidative activation of thiacetazone by the Mycobacterium tuberculosis flavin monooxygenase EtaA and human FMO1 and FMO3. Chem Res Toxicol 2006; 19: 443-449.
49. http://www.geneontology.org/.
50. http://www.ncbi.nlm.nih.gov/Structure/index.shtml.
51. Dick T, Lee BH and Murugasu-Oei B. Oxygen depletion induced dormancy in Mycobacterium smegmatis. FEMS Microbiol Lett 1998; 163: 159-164.
52. Hampshire T, Soneji S, Bacon J, James BW, Hinds J, Laing K, Stabler RA, Marsh PD and Butcher PD. Stationary phase gene expression of Mycobacterium tuberculosis following a progressive nutrient depletion: a model for persistent organisms? Tuberculosis (Edinb) 2004; 84: 228-238.
53. Nissom PM, Sanny A, Kok YJ, Hiang YT, Chuah SH, Shing TK, Lee YY, Wong KT, Hu WS, Sim MY and Philp R. Transcriptome and proteome profiling to understanding the biology of high productivity CHO cells. Mol Biotechnol 2006; 34: 125-140.
54. Trost M, English L, Lemieux S, Courcelles M, Desjardins M and Thibault P. The phagosomal proteome in interferon-gamma-activated macrophages. Immunity 2009; 30: 143-154.
55. Dumas E, Desvaux M, Chambon C and Hebraud M. Insight into the core and variant exoproteomes of Listeria monocytogenes species by comparative subproteomic analysis. Proteomics 2009; 9: 3136-3155.
56. Feltrin E, Campanaro S, Diehl AD, Ehler E, Faulkner G, Fordham J, Gardin C, Harris M, Hill D, Knoell R, Laveder P, Mittempergher L, Nori A, Reggiani C, Sorrentino V, Volpe P, Zara I, Valle G and Deegan Nee Clark J. Muscle Research and Gene Ontology: New standards for improved data integration. BMC Med Genomics 2009; 2: 6.
57. Kuehnel MP, Goethe R, Habermann A, Mueller E, Rohde M, Griffiths G and Valentin-Weigand P. Characterization of the intracellular survival of Mycobacterium avium ssp. paratuberculosis: phagosomal pH and fusogenicity in J774 macrophages compared with other mycobacteria. Cell Microbiol 2001; 3: 551-566.
58. Borelli V, Vita F, Soranzo MR, Banfi E and Zabucchi G. Ultrastructure of the interaction between mycobacterium tuberculosis- H37Rv-containing phagosomes and the lysosomal compartment in human alveolar macrophages. Exp Mol Pathol 2002; 73: 128-134.
59. Armstrong JA and Hart PD. Phagosome-lysosome interactions in cultured macrophages infected with virulent tubercle bacilli. Reversal of the usual nonfusion pattern and observations on bacterial survival. J Exp Med 1975; 142: 1-16.
60. Chan K, Knaak T, Satkamp L, Humbert O, Falkow S and Ramakrishnan L. Complex pattern of Mycobacterium marinum gene expression during long-term granulomatous infection. Proc Natl Acad Sci U S A 2002; 99: 3920-3925.
61. Cosma CL, Sherman DR and Ramakrishnan L. The secret lives of the pathogenic mycobacteria. Annu Rev Microbiol 2003; 57: 641-676.
62. Ramakrishnan L, Federspiel NA and Falkow S. Granuloma-specific expression of Mycobacterium virulence proteins from the glycine-rich PE-PGRS family. Science 2000; 288: 1436-1439.
63. Wang R, Prince JT and Marcotte EM. Mass spectrometry of the M. smegmatis proteome: protein expression levels correlate with function, operons, and codon bias. Genome Res 2005; 15: 1118-1126.
64. Pomposiello PJ, Bennik MH and Demple B. Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J Bacteriol 2001; 183: 3890-3902.
65. Balazsi G, Heath AP, Shi L and Gennaro ML. The temporal response of the Mycobacterium tuberculosis gene regulatory network during growth arrest. Mol Syst Biol 2008; 4: 225.