Disruption of an M. tuberculosis Membrane Protein Causes a Magnesium-dependent Cell Division Defect and Failure to Persist in Mice

PLoS Pathogens

Volumn 11, Issue 2, 2015, Pages

  Goodsmith, Nichole ^a   Guo, Xinzheng V ^a   Vandal, Omar H ^a   Vaubourgeix, Julien ^a   Wang, Ruojun ^a   Botella, Hélène ^a   Song, Shuang ^a   Bhatt, Kamlesh ^b   Liba, Amir ^c   Salgame, Padmini ^b   Schnappinger, Dirk ^a   Ehrt, Sabine ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c AGILENT TECHNOLOGIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BACTERIAL PROTEIN; BETA LACTAM ANTIBIOTIC; BETA LACTAMASE; CEFALEXIN; CHLORAMPHENICOL; CYCLOSERINE; DICYCLOHEXYLCARBODIIMIDE; ETHAMBUTOL; GAMMA INTERFERON; ISONIAZID; MAGNESIUM; MEROPENEM; PIPERACILLIN; POLYMYXIN B; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; RIFAMPICIN; STREPTOMYCIN; TUMOR NECROSIS FACTOR ALPHA; VANCOMYCIN; MEMBRANE PROTEIN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL DIVISION; CELL ELONGATION; CELL SURVIVAL; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CYTOKINE RESPONSE; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLUORESCENCE MICROSCOPY; HISTOLOGY; MASS SPECTROMETRY; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUTRIENT LIMITATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; TRANSCRIPTOMICS; UPREGULATION; ANIMAL; C57BL MOUSE; DISEASE MODEL; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; TUBERCULOSIS;

BACTERIA (MICROORGANISMS); MUS; MYCOBACTERIUM TUBERCULOSIS;

ANIMALS; BACTERIAL PROTEINS; CELL DIVISION; DISEASE MODELS, ANIMAL; FEMALE; MAGNESIUM; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

EID: 84924405226     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004645     Document Type: Article

References (63)

1. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, et al. (1993) An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med 178: 2249–2254. 7504064
2. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, et al. (1993) Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 178: 2243–2247. 8245795
3. Nathan CF, Murray HW, Wiebe ME, Rubin BY, (1983) Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J Exp Med 158: 670–689. 6411853
4. MacMicking JD, North RJ, LaCourse R, Mudgett JS, Shah SK, et al. (1997) Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc Natl Acad Sci USA 94: 5243–5248. 9144222
5. Kim BH, Shenoy AR, Kumar P, Das R, Tiwari S, et al. (2011) A Family of IFN—Inducible 65-kD GTPases Protects Against Bacterial Infection. Science 332: 717–721. doi: 10.1126/science.1201711 21551061
6. MacMicking JD, Taylor GA, Mckinney JD, (2003) Immune control of tuberculosis by IFN-gamma-inducible LRG-47. Science 302: 654–659. doi: 10.1126/science.1088063 14576437
7. Ehrt S, Schnappinger D, Bekiranov S, Drenkow J, Shi S, et al. (2001) Reprogramming of the macrophage transcriptome in response to interferon-gamma and Mycobacterium tuberculosis: signaling roles of nitric oxide synthase-2 and phagocyte oxidase. J Exp Med 194: 1123–1140. 11602641
8. Glickman MS, Jacobs WR, (2001) Microbial pathogenesis of Mycobacterium tuberculosis: dawn of a discipline. Cell 104: 477–485. 11239406
9. McKinney J, zu Bentrup K, Muñoz-Elías E, Miczak A, Chen B, et al. (2000) Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406: 735–738. 10963599
10. Pandey AK, Sassetti CM, (2008) Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci USA 105: 4376–4380. doi: 10.1073/pnas.0711159105 18334639
11. Schaible UE, Sturgill-Koszycki S, Schlesinger PH, Russell DG, (1998) Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J Immunol 160: 1290–1296. 9570546
12. Via LE, Fratti RA, McFalone M, Pagan-Ramos E, Deretic D, et al. (1998) Effects of cytokines on mycobacterial phagosome maturation. J Cell Sci 111 (Pt 7): 897–905.
13. Vandal OH, Pierini LM, Schnappinger D, Nathan CF, Ehrt S, (2008) A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat Med 14: 849–854. doi: 10.1038/nm.1795 18641659
14. 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. 9634230
15. Krogh A, Larsson B, Heijne von G, Sonnhammer EL, (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567–580. doi: 10.1006/jmbi.2000.4315 11152613
16. Spyropoulos IC, Liakopoulos TD, Bagos PG, Hamodrakas SJ, (2004) TMRPres2D: high quality visual representation of transmembrane protein models. Bioinformatics 20: 3258–3260. doi: 10.1093/bioinformatics/bth358 15201184
17. Marmiesse M, Brodin P, Buchrieser C, Gutierrez C, Simoes N, et al. (2004) Macro-array and bioinformatic analyses reveal mycobacterial “core” genes, variation in the ESAT-6 gene family and new phylogenetic markers for the Mycobacterium tuberculosis complex. Microbiology 150: 483–496. 14766927
18. Draper DE, Grilley D, Soto AM, (2005) Ions and RNA folding. Annu Rev Biophys Biomol Struct 34: 221–243. doi: 10.1146/annurev.biophys.34.040204.144511 15869389
19. Smith RL, Maguire ME, (1998) Microbial magnesium transport: unusual transporters searching for identity. Mol Microbiol 28: 217–226. doi: 10.1046/j.1365–2958.1998.00810.x 9622348
20. Guo L, Lim KB, Poduje CM, Daniel M, Gunn JS, et al. (1998) Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95: 189–198. 9790526
21. García Véscovi E, Soncini FC, Groisman EA, (1996) Mg2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84: 165–174. 8548821
22. Walters SB, Dubnau E, Kolesnikova I, Laval F, Daffé 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. doi: 10.1111/j.1365–2958.2006.05102.x 16573683
23. Buchmeier N, Blanc-Potard A, Ehrt S, Piddington D, Riley L, et al. (2000) A parallel intraphagosomal survival strategy shared by Mycobacterium tuberculosis and Salmonella enterica. Mol Microbiol 35: 1375–1382. 10760138
24. Perez JC, Shin D, Zwir I, Latifi T, Hadley TJ, et al. (2009) Evolution of a Bacterial Regulon Controlling Virulence and Mg2+ Homeostasis. PLoS Genet 5: e1000428. doi: 10.1371/journal.pgen.1000428.g005 19300486
25. 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. doi: 10.1074/jbc.C500388200 16326699
26. Lee E-J, Pontes MH, Groisman EA, (2013) A Bacterial Virulence Protein Promotes Pathogenicity by Inhibiting the Bacterium’s Own F1Fo ATP Synthase. Cell 154: 146–156. doi: 10.1016/j.cell.2013.06.004 23827679
27. Roach DR, Bean AGD, Demangel C, France MP, Briscoe H, et al. (2002) TNF regulates chemokine induction essential for cell recruitment, granuloma formation, and clearance of mycobacterial infection. J Immunol 168: 4620–4627. 11971010
28. Ojha AK, Baughn AD, Sambandan D, Hsu T, Trivelli X, et al. (2008) Growth of Mycobacterium tuberculosis biofilms containing free mycolic acids and harbouring drug-tolerant bacteria. Mol Microbiol 69: 164–174. doi: 10.1111/j.1365–2958.2008.06274.x 18466296
29. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, et al. (2003) Transcriptional Adaptation of Mycobacterium tuberculosis within Macrophages: Insights into the Phagosomal Environment. J Exp Med 198: 693–704. doi: 10.1084/jem.20030846 12953091
30. Stallings CL, Glickman MS, (2010) Is Mycobacterium tuberculosis stressed out? A critical assessment of the genetic evidence. Microbes Infect 12: 1091–1101. doi: 10.1016/j.micinf.2010.07.014 20691805
31. Blanc-Potard AB, Groisman EA, (1997) The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J 16: 5376–5385. doi: 10.1093/emboj/16.17.5376 9311997
32. Lavigne J-P, O’callaghan D, Blanc-Potard A-B, (2005) Requirement of MgtC for Brucella suis intramacrophage growth: a potential mechanism shared by Salmonella enterica and Mycobacterium tuberculosis for adaptation to a low-Mg2+ environment. Infect Immun 73: 3160–3163. doi: 10.1128/IAI.73.5.3160–3163.2005 15845525
33. Froschauer E, Kolisek M, Dieterich F, Schweigel M, Schweyen R, (2004) Fluorescence measurements of free [Mg2+] by use of mag‐fura 2 in Salmonella enterica. FEMS Microbiol Lett 237: 49–55. 15268937
34. Mohammadi T, van Dam V, Sijbrandi R, Vernet T, Zapun AE, et al. (2011) Identification of FtsW as a transporter of lipid- linked cell wall precursors across the membrane. EMBO J 30: 1425–1432. doi: 10.1038/emboj.2011.61 21386816
35. Datta P, Dasgupta A, Singh AK, Mukherjee P, Kundu M, et al. (2006) Interaction between FtsW and penicillin-binding protein 3 (PBP3) directs PBP3 to mid-cell, controls cell septation and mediates the formation of a trimeric complex involving FtsZ, FtsW and PBP3 in mycobacteria. Mol Microbiol 62: 1655–1673. doi: 10.1111/j.1365–2958.2006.05491.x 17427288
36. Lew JM, Kapopoulou A, Jones LM, Cole ST, (2011) TubercuList—10 years after. Tuberculosis 91: 1–7. doi: 10.1016/j.tube.2010.09.008 20980199
37. Kaur D, Guerin ME, Scaronkovierovaacute H, Brennan PJ, Jackson M, (2009) Chapter 2: Biogenesis of the cell wall and other glycoconjugates of Mycobacterium tuberculosis. Adv Appl Microbiol 69: 23–78. doi: 10.1016/S0065–2164(09)69002-X 19729090
38. Plocinski P, Ziolkiewicz M, Kiran M, Vadrevu SI, Nguyen HB, et al. (2011) Characterization of CrgA, a New Partner of the Mycobacterium tuberculosis Peptidoglycan Polymerization Complexes. J Bacteriol 193: 3246–3256. doi: 10.1128/JB.00188–11 21531798
39. Rajagopalan M, Maloney E, Dziadek J, Poplawska M, Lofton H, et al. (2005) Genetic evidence that mycobacterial FtsZ and FtsW proteins interact, and colocalize to the division site in Mycobacterium smegmatis. FEMS Microbiol Lett 250: 9–17. doi: 10.1016/j.femsle.2005.06.043 16040206
40. Hett EC, Chao MC, Rubin EJ, (2010) Interaction and Modulation of Two Antagonistic Cell Wall Enzymes of Mycobacteria. PLoS Pathog 6: e1001020. doi: 10.1371/journal.ppat.1001020.s002 20686708
41. Eberhardt C, Kuerschner L, Weiss DS, (2003) Probing the Catalytic Activity of a Cell Division-Specific Transpeptidase In Vivo with ß-Lactams. J Bacteriol 185: 3726–3734. 2003. doi: 10.1128/JB.185.13.3726–3734 12813065
42. Botta GA, Park JT, (1981) Evidence for involvement of penicillin-binding protein 3 in murein synthesis during septation but not during cell elongation. J Bacteriol 145: 333–340. 6450748
43. Hedge PJ, Spratt BG, (1985) Resistance to beta-lactam antibiotics by re-modelling the active site of an E. coli penicillin-binding protein. Nature 318: 478–480. 3906408
44. Slayden RA, Belisle JT, (2009) Morphological features and signature gene response elicited by inactivation of FtsI in Mycobacterium tuberculosis. J of Antimicrob Chemother 63: 451–457. doi: 10.1093/jac/dkn507 19109339
45. Murata T, Tseng W, Guina T, Miller S, Nikaido H, (2007) PhoPQ-mediated regulation produces a more robust permeability barrier in the outer membrane of Salmonella enterica serovar typhimurium. J Bacteriol 189: 7213. 17693506
46. D’Elia MA, Millar KE, Beveridge TJ, Brown ED, (2006) Wall teichoic acid polymers are dispensable for cell viability in Bacillus subtilis. J Bacteriol 188: 8313–8316. doi: 10.1128/JB.01336–06 17012386
47. Formstone A, Errington J, (2005) A magnesium-dependent mreB null mutant: implications for the role of mreB in Bacillus subtilis. Mol Microbiol 55: 1646–1657. doi: 10.1111/j.1365–2958.2005.04506.x 15752190
48. Murray T, Popham DL, Setlow P, (1998) Bacillus subtilis cells lacking penicillin-binding protein 1 require increased levels of divalent cations for growth. J Bacteriol 180: 4555–4563. 9721295
49. Rogers HJ, Thurman PF, Buxton RS, (1976) Magnesium and anion requirements of rodB mutants of Bacillus subtilis. J Bacteriol 125: 556–564. 812869
50. Garrett AJ, (1969) The effect of magnesium ion deprivation on the synthesis of mucopeptide and its precursors in Bacillus subtilis. Biochem J 115: 419–430. 4982084
51. Chastanet A, Carballido-Lopez R, (2012) The actin-like MreB proteins in Bacillus subtilis: a new turn. Front Biosci (Schol Ed) 4: 1582–1606. 22652894
52. Prosser GA, de Carvalho LPS, (2013) Metabolomics Reveal d-Alanine:d-Alanine Ligase As the Target of d-Cycloserine in Mycobacterium tuberculosis. ACS Med Chem Lett 4: 1233–1237. doi: 10.1021/ml400349n 24478820
53. Reynolds PE, (1989) Structure, biochemistry and mechanism of action of glycopeptide antibiotics. Eur J Clin Microbiol Infect Dis 8: 943–950. 2532132
54. Hett EC, Chao MC, Deng LL, Rubin EJ, (2008) A Mycobacterial Enzyme Essential for Cell Division Synergizes with Resuscitation-Promoting Factor. PLoS Pathog 4: e1000001. doi: 10.1371/journal.ppat.1000001 18463693
55. Wagner D, Maser J, Lai B, Cai Z, Barry CE, et al. (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. 15661908
56. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JCD, (2002) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47: 103–118. doi: 10.1046/j.1365–2958.2003.03313.x
57. Portillo FGD, Foster JW, Maguire ME, Finlay BB, (1992) Characterization of the micro-environment of Salmonella typhimurium-containing vacuoles within MDCK epithelial cells. Mol Microbiol 6: 3289–3297. doi: 10.1111/j.1365–2958.1992.tb02197.x 1484485
58. Martin-Orozco N, Touret N, Zaharik ML, Park E, Kopelman R, et al. (2006) Visualization of vacuolar acidification-induced transcription of genes of pathogens inside macrophages. Mol Biol Cell 17: 498–510. doi: 10.1091/mbc.E04–12–1096 16251362
59. Trapani V, Farruggia G, Marraccini C, Iotti S, Cittadini A, et al. (2010) Intracellular magnesium detection: imaging a brighter future. Analyst 135: 1855. doi: 10.1039/c0an00087f 20544083
60. Pandey AK, Yang Y, Jiang Z, Fortune SM, Coulombe F, et al. (2009) NOD2, RIP2 and IRF5 Play a Critical Role in the Type I Interferon Response to Mycobacterium tuberculosis. PLoS Pathog 5: e1000500. doi: 10.1371/journal.ppat.1000500.g008 19578435
61. McBride A, Bhatt K, Salgame P, (2011) Development of a secondary immune response to Mycobacterium tuberculosis is independent of Toll-like receptor 2. Infect Immun 79: 1118–1123. doi: 10.1128/IAI.01076–10 21173309
62. Ehrt S, Voskuil MI, Schoolnik GK, Schnappinger D, (2002) Genome-wide expression profiling of intracellular bacteria: the interaction of Mycobacterium tuberculosis with macrophages. Immunology of Infection: 169–180.
63. Flores AR, Parsons LM, Pavelka MS, (2005) Genetic analysis of the ß-lactamases of Mycobacterium tuberculosis and Mycobacterium smegmatis and susceptibility to ß-lactam antibiotics. Microbiol 151: 521–532.