The role of the novel exopolyphosphatase MT0516 in Mycobacterium tuberculosis drug tolerance and persistence

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Thayil, Seema M ^a   Morrison, Norman ^a   Schechter, Norman ^b   Rubin, Harvey ^b   Karakousis, Petros C ^a,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISONIAZID; POLYPHOSPHATE; ACID ANHYDRIDE HYDROLASE; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; EXOPOLYPHOSPHATASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BIOACCUMULATION; CONTROLLED STUDY; DRUG TOLERANCE; EXPERIMENTAL GUINEA PIG; FEMALE; GENE ACTIVITY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GROWTH INHIBITION; HISTOLOGY; HUMAN; HUMAN CELL; HYDROLYSIS; LUNG TUBERCULOSIS; MPRB GENE; MT0516 GENE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; REL GENE; SIGE GENE; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; ANTIBIOTIC RESISTANCE; CHEMICAL STRUCTURE; DRUG EFFECT; ENZYMOLOGY; GENETIC COMPLEMENTATION; GENETIC RECOMBINATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; GUINEA PIG; LUNG; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PATHOLOGY; STRUCTURAL HOMOLOGY; TRANSPOSON; VIRULENCE;

BACTERIA (MICROORGANISMS); CAVIA; MYCOBACTERIUM TUBERCULOSIS; SIGE;

ACID ANHYDRIDE HYDROLASES; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, BACTERIAL; FEMALE; GENETIC COMPLEMENTATION TEST; GUINEA PIGS; HUMANS; HYDROLYSIS; ISONIAZID; LUNG; MODELS, MOLECULAR; MUTATION; MYCOBACTERIUM TUBERCULOSIS; POLYPHOSPHATES; RECOMBINATION, GENETIC; STRUCTURAL HOMOLOGY, PROTEIN; VIRULENCE;

EID: 81455127376     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028076     Document Type: Article

References (58)

1. Fauci AS, (2008) Multidrug-resistant and extensively drug-resistant tuberculosis: the National Institute of Allergy and Infectious Diseases Research agenda and recommendations for priority research. J Infect Dis 197: 1493-1498.
2. Nuermberger E, Bishai WR, Grosset JH, (2004) Latent tuberculosis infection. Semin Respir Crit Care Med 25: 317-336.
3. Opie EL, Aronson JD, (1927) Tubercle bacilli in latent tuberculous lesions and in lung tissue without tuberculous lesions. Arch Pathol Lab Med 4: 1-21.
4. Haapanen JH, Kass I, Gensini G, Middlebrook G, (1959) Studies on the gaseous content of tuberculous cavities. Am Rev Respir Dis 80: 1-5.
5. Gomez JE, McKinney JD, (2004) Persistence and drug tolerance. In: Rom WN, Garay SM, editors. Tuberculosis. 2nd ed Philadelphia Lippincott Williams & Wilkins pp. 101-114.
6. McDermott W, (1959) Inapparent infection: relation of latent and dormant infections to microbial persistence. Public Health Rep 74: 485-499.
7. Winder FG, Collins PB, (1970) Inhibition by isoniazid of synthesis of mycolic acids in Mycobacterium tuberculosis. J Gen Microbiol 63: 41-48.
8. Takayama K, Wang L, David HL, (1972) Effect of isoniazid on the in vivo mycolic acid synthesis, cell growth, and viability of Mycobacterium tuberculosis. Antimicrob Agents Chemother 2: 29-35.
9. Primm TP, Andersen SJ, Mizrahi V, Avarbock D, Rubin H, et al. (2000) The stringent response of Mycobacterium tuberculosis is required for long-term survival. J Bacteriol 182: 4889-4898.
10. Dahl JL, Kraus CN, Boshoff HI, Doan B, Foley K, et al. (2003) The role of RelMtb-mediated adaptation to stationary phase in long-term persistence of Mycobacterium tuberculosis in mice. Proc Natl Acad Sci U S A 100: 10026-10031.
11. Bloch H, Segal W, (1956) Biochemical differentiation of Mycobacterium tuberculosis grown in vivo and in vitro. J Bacteriol 72: 132-141.
12. Rao NN, Kornberg A, (1999) Inorganic polyphosphate regulates responses of Escherichia coli to nutritional stringencies, environmental stresses and survival in the stationary phase. Prog Mol Subcell Biol 23: 183-195.
13. Kornberg A, Rao NN, Ault-Riche D, (1999) Inorganic polyphosphate: a molecule of many functions. Annu Rev Biochem 68: 89-125.
14. Kuroda A, Murphy H, Cashel M, Kornberg A, (1997) Guanosine tetra- and pentaphosphate promote accumulation of inorganic polyphosphate in Escherichia coli. J Biol Chem 272: 21240-21243.
15. Potrykus K, Cashel M, (2008) (p)ppGpp: Still Magical? Annu Rev Microbiol.
16. Rao NN, Kornberg A, (1996) Inorganic polyphosphate supports resistance and survival of stationary-phase Escherichia coli. J Bacteriol 178: 1394-1400.
17. Shiba T, Tsutsumi K, Yano H, Ihara Y, Kameda A, et al. (1997) Inorganic polyphosphate and the induction of rpoS expression. Proc Natl Acad Sci U S A 94: 11210-11215.
18. Hengge-Aronis R, (2002) Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66: 373-395.
19. Sureka K, Dey S, Datta P, Singh AK, Dasgupta A, et al. (2007) Polyphosphate kinase is involved in stress-induced mprAB-sigE-rel signalling in mycobacteria. Mol Microbiol 65: 261-276.
20. Sureka K, Ghosh B, Dasgupta A, Basu J, Kundu M, et al. (2008) Positive feedback and noise activate the stringent response regulator rel in mycobacteria. PLoS ONE 3: e1771.
21. 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.
22. Lindner SN, Knebel S, Wesseling H, Schoberth SM, Wendisch VF, (2009) Exopolyphosphatases PPX1 and PPX2 from Corynebacterium glutamicum. Appl Environ Microbiol 75: 3161-3170.
23. Kelley LA, Sternberg MJ, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
24. Rangarajan ES, Nadeau G, Li Y, Wagner J, Hung MN, et al. (2006) The structure of the exopolyphosphatase (PPX) from Escherichia coli O157:H7 suggests a binding mode for long polyphosphate chains. J Mol Biol 359: 1249-1260.
25. Kristensen O, Ross B, Gajhede M, (2008) Structure of the PPX/GPPA phosphatase from Aquifex aeolicus in complex with the alarmone ppGpp. J Mol Biol 375: 1469-1476.
26. Cole ST, Eiglmeier K, Parkhill J, James KD, Thomson NR, et al. (2001) Massive gene decay in the leprosy bacillus. Nature 409: 1007-1011.
27. Lamichhane G, Zignol M, Blades NJ, Geiman DE, Dougherty A, et al. (2003) A postgenomic method for predicting essential genes at subsaturation levels of mutagenesis: application to Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 100: 7213-7218.
28. Ault-Riche D, Fraley CD, Tzeng CM, Kornberg A, (1998) Novel assay reveals multiple pathways regulating stress-induced accumulations of inorganic polyphosphate in Escherichia coli. J Bacteriol 180: 1841-1847.
29. Aschar-Sobbi R, Abramov AY, Diao C, Kargacin ME, Kargacin GJ, et al. (2008) High Sensitivity, Quantitative Measurements of Polyphosphate Using a New DAPI-Based Approach. J Fluoresc 18: 859-866.
30. Werner TP, Amrhein N, Freimoser FM, (2005) Novel method for the quantification of inorganic polyphosphate (iPoP) in Saccharomyces cerevisiae shows dependence of iPoP content on the growth phase. Arch Microbiol 184: 129-136.
31. Shi X, Rao NN, Kornberg A, (2004) Inorganic polyphosphate in Bacillus cereus: motility, biofilm formation, and sporulation. Proc Natl Acad Sci U S A 101: 17061-17065.
32. Wayne LG, Hayes LG, (1996) An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 64: 2062-2069.
33. Klinkenberg LG, Sutherland LA, Bishai WR, Karakousis PC, (2008) Metronidazole lacks activity against Mycobacterium tuberculosis in an in vivo hypoxic granuloma model of latency. J Infect Dis 198: 275-283.
34. Wayne LG, Sramek HA, (1994) Metronidazole is bactericidal to dormant cells of Mycobacterium tuberculosis. Antimicrob Agents Chemother 38: 2054-2058.
35. Via LE, Lin PL, Ray SM, Carrillo J, Allen SS, et al. (2008) Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun 76: 2333-2340.
36. Lenaerts AJ, Hoff D, Aly S, Ehlers S, Andries K, et al. (2007) Location of persisting mycobacteria in a Guinea pig model of tuberculosis revealed by r207910. Antimicrob Agents Chemother 51: 3338-3345.
37. Keasling JD, Bertsch L, Kornberg A, (1993) Guanosine pentaphosphate phosphohydrolase of Escherichia coli is a long-chain exopolyphosphatase. Proc Natl Acad Sci U S A 90: 7029-7033.
38. Rao NN, Gomez-Garcia MR, Kornberg A, (2009) Inorganic polyphosphate: essential for growth and survival. Annu Rev Biochem 78: 605-647.
39. Winder FG, Denneny JM, (1957) The metabolism of inorganic polyphosphate in mycobacteria. J Gen Microbiol 17: 573-585.
40. Rifat D, Bishai WR, Karakousis PC, (2009) Phosphate depletion: a novel trigger for Mycobacterium tuberculosis persistence. J Infect Dis 200: 1126-1135.
41. Tomasz A, Albino A, Zanati E, (1970) Multiple antibiotic resistance in a bacterium with suppressed autolytic system. Nature 227: 138-140.
42. Avarbock D, Avarbock A, Rubin H, (2000) Differential regulation of opposing RelMtb activities by the aminoacylation state of a tRNA.ribosome.mRNA.RelMtb complex. Biochemistry 39: 11640-11648.
43. Karakousis PC, (2009) Mechanisms of action and resistance of antimycobacterial agents. In: Mayers DL, editors. Antimicrobial Drug Resistance New York Humana Press pp. 271-291.
44. Horsburgh CR Jr, Rubin EJ, (2011) Clinical practice. Latent tuberculosis infection in the United States. N Engl J Med 364: 1441-1448.
45. Xie Z, Siddiqi N, Rubin EJ, (2005) Differential antibiotic susceptibilities of starved Mycobacterium tuberculosis isolates. Antimicrob Agents Chemother 49: 4778-4780.
46. Karakousis PC, Yoshimatsu T, Lamichhane G, Woolwine SC, Nuermberger EL, et al. (2004) Dormancy phenotype displayed by extracellular Mycobacterium tuberculosis within artificial granulomas in mice. J Exp Med 200: 647-657.
47. Zhang T, Zhang M, Rosenthal IM, Grosset JH, Nuermberger EL, (2009) Short-course therapy with daily rifapentine in a murine model of latent tuberculosis infection. Am J Respir Crit Care Med 180: 1151-1157.
48. Adams KN, Takaki K, Connolly LE, Wiedenhoft H, Winglee K, et al. (2011) Drug tolerance in replicating mycobacteria mediated by a macrophage-induced efflux mechanism. Cell 145: 39-53.
49. Rao NN, Liu S, Kornberg A, (1998) Inorganic polyphosphate in Escherichia coli: the phosphate regulon and the stringent response. J Bacteriol 180: 2186-2193.
50. Zhang Q, Li Y, Tang CM, (2010) The role of the exopolyphosphatase PPX in avoidance by Neisseria meningitidis of complement-mediated killing. J Biol Chem 285: 34259-34268.
51. Sable SB, Kumar R, Kalra M, Verma I, Khuller GK, et al. (2005) Peripheral blood and pleural fluid mononuclear cell responses to low-molecular-mass secretory polypeptides of Mycobacterium tuberculosis in human models of immunity to tuberculosis. Infect Immun 73: 3547-3558.
52. Lamichhane G, Tyagi S, Bishai WR, (2005) Designer arrays for defined mutant analysis to detect genes essential for survival of Mycobacterium tuberculosis in mouse lungs. Infect Immun 73: 2533-2540.
53. Klinkenberg LG, Lee JH, Bishai WR, Karakousis PC, (2010) The stringent response is required for full virulence of Mycobacterium tuberculosis in guinea pigs. J Infect Dis 202: 1397-1404.
54. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
55. Manganelli R, Dubnau E, Tyagi S, Kramer FR, Smith I, (1999) Differential expression of 10 sigma factor genes in Mycobacterium tuberculosis. Mol Microbiol 31: 715-724.
56. Rengarajan J, Bloom BR, Rubin EJ, (2005) Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci U S A 102: 8327-8332.
57. Ahmad Z, Fraig MM, Bisson GP, Nuermberger EL, Grosset JH, et al. (2011) Dose-dependent activity of pyrazinamide in animal models of intracellular and extracellular tuberculosis. Antimicrob Agents Chemother.
58. Ahmad Z, Klinkenberg LG, Pinn ML, Fraig MM, Peloquin CA, et al. (2009) Biphasic Kill Curve of Isoniazid Reveals the Presence of Drug-Tolerant, Not Drug-Resistant, Mycobacterium tuberculosis in the Guinea Pig. J Infect Dis 200: 1136-1143.