Abstract
Mycobacterium tuberculosis can persist in an altered physiological state for many years after initial infection, and it may reactivate to cause active disease. An analogous persistent state, possibly consisting of several different subpopulations of bacteria, may arise during chemotherapy; this state is thought to be responsible for the prolonged period required for effective chemotherapy. Using two models of drug-induced persistence, we show that both microaerophilic stationary-phase M. tuberculosis treated with a high dose of rifampin in vitro and pyrazinamide-induced persistent bacteria in mice are nonculturable yet still contain 16S rRNA and mRNA transcripts. Also, the in vitro persistent, plate culture-negative bacteria incorporate radioactive uridine into their RNA in the presence of rifampin and can rapidly up-regulate gene transcription after the replacement of the drug with fresh medium and in response to heat shock. Our results show that persistent M. tuberculosis has transcriptional activity. This finding provides a molecular basis for the rational design of drugs targeted at persistent bacteria.
MeSH Terms
Animals
Antibiotics, Antitubercular/therapeutic use
Antitubercular Agents/therapeutic use
Disease Models, Animal
Drug Resistance, Microbial
Mice
Mice, Inbred BALB C
Mycobacterium tuberculosis/drug effects,isolation & purification,physiology
Pyrazinamide/therapeutic use
RNA, Bacterial/analysis
RNA, Messenger/analysis
RNA, Ribosomal, 16S/analysis
Rifampin/therapeutic use
Time Factors
Transcription, Genetic
Tuberculosis/drug therapy,microbiology
Chemicals
Antibiotics, Antitubercular
Antitubercular Agents
RNA, Bacterial
RNA, Messenger
RNA, Ribosomal, 16S
Pyrazinamide
Rifampin
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Hu Y
Department of Medical Microbiology, St. George's Hospital Medical School, London SW17 0RE, United Kingdom.
Mangan J A
Dhillon J
Sole K M
Mitchison D A
Butcher P D
Coates A R
References (35)
35 references, click to expand
-
Identification of a central regulator of stationary-phase gene expression in Escherichia coli.
Mol Microbiol. 1991 Jan;5(1):49-59
PMID: 1849609
-
The death and resurrection of tuberculosis.
Nat Med. 1999 Aug;5(8):872-4
PMID: 10426305
-
The mystery of the mycobacterial 'persistor'.
Tuber Lung Dis. 1992 Oct;73(5):249-51
PMID: 1493231
-
Determination of Mycobacterium leprae viability by polymerase chain reaction amplification of 71-kDa heat-shock protein mRNA.
J Infect Dis. 1993 Sep;168(3):799-800
PMID: 8354932
-
Effect of stress treatments on the detection of Listeria monocytogenes and enterotoxigenic Escherichia coli by the polymerase chain reaction.
J Appl Bacteriol. 1994 Jul;77(1):73-9
PMID: 7928784
-
Assessment of mycobacterial viability by RNA amplification.
Antimicrob Agents Chemother. 1994 Sep;38(9):1959-65
PMID: 7529012
-
Metronidazole is bactericidal to dormant cells of Mycobacterium tuberculosis.
Antimicrob Agents Chemother. 1994 Sep;38(9):2054-8
PMID: 7811018
-
Genomic organization of the mycobacterial sigma gene cluster.
Gene. 1995 Nov 7;165(1):67-70
PMID: 7489918
-
Mycobacterial dormancy.
Tuber Lung Dis. 1995 Dec;76(6):477-9
PMID: 8593366
-
The bacterial DNA content of mouse organs in the Cornell model of dormant tuberculosis.
Tuber Lung Dis. 1995 Dec;76(6):555-62
PMID: 8593379
-
A stationary-phase stress-response sigma factor from Mycobacterium tuberculosis.
Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2790-4
PMID: 8610119
-
Stationary phase-associated protein expression in Mycobacterium tuberculosis: function of the mycobacterial alpha-crystallin homolog.
J Bacteriol. 1996 Aug;178(15):4484-92
PMID: 8755875
-
An effective method of RNA extraction from bacteria refractory to disruption, including mycobacteria.
Nucleic Acids Res. 1997 Feb 1;25(3):675-6
PMID: 9016612
-
Salmonella DNA persistence in natural seawaters using PCR analysis.
J Appl Microbiol. 1997 Apr;82(4):507-10
PMID: 9134724
-
Low dosage and long treatment duration of beta-lactam: risk factors for carriage of penicillin-resistant Streptococcus pneumoniae.
JAMA. 1998 Feb 4;279(5):365-70
PMID: 9459469
-
Mycobacterial stationary phase induced by low oxygen tension: cell wall thickening and localization of the 16-kilodalton alpha-crystallin homolog.
J Bacteriol. 1998 Feb;180(4):801-8
PMID: 9473032
-
Detection of mRNA by reverse transcription-PCR as an indicator of viability in Escherichia coli cells.
Appl Environ Microbiol. 1998 Apr;64(4):1313-8
PMID: 9546166
-
Mechanisms of latency in Mycobacterium tuberculosis.
Trends Microbiol. 1998 Mar;6(3):107-12
PMID: 9582936
-
Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence.
Nature. 1998 Jun 11;393(6685):537-44
PMID: 9634230
-
rRNA stability in heat-killed and UV-irradiated enterotoxigenic Staphylococcus aureus and Escherichia coli O157:H7.
Appl Environ Microbiol. 1998 Nov;64(11):4264-8
PMID: 9797275
-
Differential inhibition of transcription from sigma70- and sigma32-dependent promoters by rifampicin.
FEBS Lett. 1998 Nov 27;440(1-2):172-4
PMID: 9862449
-
Transcription of two sigma 70 homologue genes, sigA and sigB, in stationary-phase Mycobacterium tuberculosis.
J Bacteriol. 1999 Jan;181(2):469-76
PMID: 9882660
-
The bactericidal activities of antituberculous drugs.
Am Rev Tuberc. 1956 Aug;74(2 Part 2):109-16; discussion, 116-23
PMID: 13340170
-
Identification of viable and non-viable Mycobacterium tuberculosis in mouse organs by directed RT-PCR for antigen 85B mRNA.
Microb Pathog. 2000 Jun;28(6):335-42
PMID: 10839970
-
Role of individual drugs in the chemotherapy of tuberculosis.
Int J Tuberc Lung Dis. 2000 Sep;4(9):796-806
PMID: 10985648
-
Microbial persistence. II. Characteristics of the sterile state of tubercle bacilli.
J Exp Med. 1966 Mar 1;123(3):469-86
PMID: 4957011
-
First-line chemotherapy in the retreatment of bacteriological relapses of pulmonary tuberculosis following a shortcourse regimen.
Lancet. 1976 Jan 24;1(7952):162-3
PMID: 54680
-
Dynamics of submerged growth of Mycobacterium tuberculosis under aerobic and microaerophilic conditions.
Am Rev Respir Dis. 1976 Oct;114(4):807-11
PMID: 823851
-
Experimental models to explain the high sterilizing activity of rifampin in the chemotherapy of tuberculosis.
Am Rev Respir Dis. 1981 Apr;123(4 Pt 1):367-71
PMID: 6784622
-
Whither short-course chemotherapy?
Br J Dis Chest. 1981 Oct;75(4):331-57
PMID: 7030377
-
Quantitative analysis of mRNA as a marker for viability of Mycobacterium tuberculosis.
J Clin Microbiol. 1999 Feb;37(2):290-5
PMID: 9889206
-
Intracellular gene expression. Analysis of RNA from mycobacteria in macrophages using RT-PCR.
Methods Mol Biol. 1998;101:285-306
PMID: 9921487
-
Transcription of the stationary-phase-associated hspX gene of Mycobacterium tuberculosis is inversely related to synthesis of the 16-kilodalton protein.
J Bacteriol. 1999 Mar;181(5):1380-7
PMID: 10049366
-
Therapy of tuberculosis in mice by DNA vaccination.
Nature. 1999 Jul 15;400(6741):269-71
PMID: 10421369
-
The global tuberculosis situation and the new control strategy of the World Health Organization.
Tubercle. 1991 Mar;72(1):1-6
PMID: 1882440