Optimisation of bioluminescent reporters for use with mycobacteria
Mycobacterium tuberculosis, the causative agent of tuberculosis, still represents a major public health threat in many countries. Bioluminescence, the production of light by luciferase-catalyzed reactions, is a versatile reporter technology with multiple applications both in vitro and in vivo. In vi...
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| Published in | PloS one Vol. 5; no. 5; p. e10777 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
24.05.2010
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Mycobacterium tuberculosis, the causative agent of tuberculosis, still represents a major public health threat in many countries. Bioluminescence, the production of light by luciferase-catalyzed reactions, is a versatile reporter technology with multiple applications both in vitro and in vivo. In vivo bioluminescence imaging (BLI) represents one of its most outstanding uses by allowing the non-invasive localization of luciferase-expressing cells within a live animal. Despite the extensive use of luminescent reporters in mycobacteria, the resultant luminescent strains have not been fully applied to BLI.
One of the main obstacles to the use of bioluminescence for in vivo imaging is the achievement of reporter protein expression levels high enough to obtain a signal that can be detected externally. Therefore, as a first step in the application of this technology to the study of mycobacterial infection in vivo, we have optimised the use of firefly, Gaussia and bacterial luciferases in mycobacteria using a combination of vectors, promoters, and codon-optimised genes. We report for the first time the functional expression of the whole bacterial lux operon in Mycobacterium tuberculosis and M. smegmatis thus allowing the development of auto-luminescent mycobacteria. We demonstrate that the Gaussia luciferase is secreted from bacterial cells and that this secretion does not require a signal sequence. Finally we prove that the signal produced by recombinant mycobacteria expressing either the firefly or bacterial luciferases can be non-invasively detected in the lungs of infected mice by bioluminescence imaging.
While much work remains to be done, the finding that both firefly and bacterial luciferases can be detected non-invasively in live mice is an important first step to using these reporters to study the pathogenesis of M. tuberculosis and other mycobacterial species in vivo. Furthermore, the development of auto-luminescent mycobacteria has enormous ramifications for high throughput mycobacterial drug screening assays which are currently carried out either in a destructive manner using LuxAB or the firefly luciferase. |
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| AbstractList | Background
Mycobacterium tuberculosis , the causative agent of tuberculosis, still represents a major public health threat in many countries. Bioluminescence, the production of light by luciferase-catalyzed reactions, is a versatile reporter technology with multiple applications both in vitro and in vivo. In vivo bioluminescence imaging (BLI) represents one of its most outstanding uses by allowing the non-invasive localization of luciferase-expressing cells within a live animal. Despite the extensive use of luminescent reporters in mycobacteria, the resultant luminescent strains have not been fully applied to BLI.
Methodology/Principal Findings
One of the main obstacles to the use of bioluminescence for in vivo imaging is the achievement of reporter protein expression levels high enough to obtain a signal that can be detected externally. Therefore, as a first step in the application of this technology to the study of mycobacterial infection in vivo , we have optimised the use of firefly, Gaussia and bacterial luciferases in mycobacteria using a combination of vectors, promoters, and codon-optimised genes. We report for the first time the functional expression of the whole bacterial lux operon in Mycobacterium tuberculosis and M. smegmatis thus allowing the development of auto-luminescent mycobacteria. We demonstrate that the Gaussia luciferase is secreted from bacterial cells and that this secretion does not require a signal sequence. Finally we prove that the signal produced by recombinant mycobacteria expressing either the firefly or bacterial luciferases can be non-invasively detected in the lungs of infected mice by bioluminescence imaging.
Conclusions/Significance
While much work remains to be done, the finding that both firefly and bacterial luciferases can be detected non-invasively in live mice is an important first step to using these reporters to study the pathogenesis of M. tuberculosis and other mycobacterial species in vivo . Furthermore, the development of auto-luminescent mycobacteria has enormous ramifications for high throughput mycobacterial drug screening assays which are currently carried out either in a destructive manner using LuxAB or the firefly luciferase. Mycobacterium tuberculosis, the causative agent of tuberculosis, still represents a major public health threat in many countries. Bioluminescence, the production of light by luciferase-catalyzed reactions, is a versatile reporter technology with multiple applications both in vitro and in vivo. In vivo bioluminescence imaging (BLI) represents one of its most outstanding uses by allowing the non-invasive localization of luciferase-expressing cells within a live animal. Despite the extensive use of luminescent reporters in mycobacteria, the resultant luminescent strains have not been fully applied to BLI.One of the main obstacles to the use of bioluminescence for in vivo imaging is the achievement of reporter protein expression levels high enough to obtain a signal that can be detected externally. Therefore, as a first step in the application of this technology to the study of mycobacterial infection in vivo, we have optimised the use of firefly, Gaussia and bacterial luciferases in mycobacteria using a combination of vectors, promoters, and codon-optimised genes. We report for the first time the functional expression of the whole bacterial lux operon in Mycobacterium tuberculosis and M. smegmatis thus allowing the development of auto-luminescent mycobacteria. We demonstrate that the Gaussia luciferase is secreted from bacterial cells and that this secretion does not require a signal sequence. Finally we prove that the signal produced by recombinant mycobacteria expressing either the firefly or bacterial luciferases can be non-invasively detected in the lungs of infected mice by bioluminescence imaging.While much work remains to be done, the finding that both firefly and bacterial luciferases can be detected non-invasively in live mice is an important first step to using these reporters to study the pathogenesis of M. tuberculosis and other mycobacterial species in vivo. Furthermore, the development of auto-luminescent mycobacteria has enormous ramifications for high throughput mycobacterial drug screening assays which are currently carried out either in a destructive manner using LuxAB or the firefly luciferase. BACKGROUNDMycobacterium tuberculosis, the causative agent of tuberculosis, still represents a major public health threat in many countries. Bioluminescence, the production of light by luciferase-catalyzed reactions, is a versatile reporter technology with multiple applications both in vitro and in vivo. In vivo bioluminescence imaging (BLI) represents one of its most outstanding uses by allowing the non-invasive localization of luciferase-expressing cells within a live animal. Despite the extensive use of luminescent reporters in mycobacteria, the resultant luminescent strains have not been fully applied to BLI. METHODOLOGY/PRINCIPAL FINDINGSOne of the main obstacles to the use of bioluminescence for in vivo imaging is the achievement of reporter protein expression levels high enough to obtain a signal that can be detected externally. Therefore, as a first step in the application of this technology to the study of mycobacterial infection in vivo, we have optimised the use of firefly, Gaussia and bacterial luciferases in mycobacteria using a combination of vectors, promoters, and codon-optimised genes. We report for the first time the functional expression of the whole bacterial lux operon in Mycobacterium tuberculosis and M. smegmatis thus allowing the development of auto-luminescent mycobacteria. We demonstrate that the Gaussia luciferase is secreted from bacterial cells and that this secretion does not require a signal sequence. Finally we prove that the signal produced by recombinant mycobacteria expressing either the firefly or bacterial luciferases can be non-invasively detected in the lungs of infected mice by bioluminescence imaging. CONCLUSIONS/SIGNIFICANCEWhile much work remains to be done, the finding that both firefly and bacterial luciferases can be detected non-invasively in live mice is an important first step to using these reporters to study the pathogenesis of M. tuberculosis and other mycobacterial species in vivo. Furthermore, the development of auto-luminescent mycobacteria has enormous ramifications for high throughput mycobacterial drug screening assays which are currently carried out either in a destructive manner using LuxAB or the firefly luciferase. Background Mycobacterium tuberculosis, the causative agent of tuberculosis, still represents a major public health threat in many countries. Bioluminescence, the production of light by luciferase-catalyzed reactions, is a versatile reporter technology with multiple applications both in vitro and in vivo. In vivo bioluminescence imaging (BLI) represents one of its most outstanding uses by allowing the non-invasive localization of luciferase-expressing cells within a live animal. Despite the extensive use of luminescent reporters in mycobacteria, the resultant luminescent strains have not been fully applied to BLI. Methodology/Principal Findings One of the main obstacles to the use of bioluminescence for in vivo imaging is the achievement of reporter protein expression levels high enough to obtain a signal that can be detected externally. Therefore, as a first step in the application of this technology to the study of mycobacterial infection in vivo, we have optimised the use of firefly, Gaussia and bacterial luciferases in mycobacteria using a combination of vectors, promoters, and codon-optimised genes. We report for the first time the functional expression of the whole bacterial lux operon in Mycobacterium tuberculosis and M. smegmatis thus allowing the development of auto-luminescent mycobacteria. We demonstrate that the Gaussia luciferase is secreted from bacterial cells and that this secretion does not require a signal sequence. Finally we prove that the signal produced by recombinant mycobacteria expressing either the firefly or bacterial luciferases can be non-invasively detected in the lungs of infected mice by bioluminescence imaging. Conclusions/Significance While much work remains to be done, the finding that both firefly and bacterial luciferases can be detected non-invasively in live mice is an important first step to using these reporters to study the pathogenesis of M. tuberculosis and other mycobacterial species in vivo. Furthermore, the development of auto-luminescent mycobacteria has enormous ramifications for high throughput mycobacterial drug screening assays which are currently carried out either in a destructive manner using LuxAB or the firefly luciferase. Mycobacterium tuberculosis, the causative agent of tuberculosis, still represents a major public health threat in many countries. Bioluminescence, the production of light by luciferase-catalyzed reactions, is a versatile reporter technology with multiple applications both in vitro and in vivo. In vivo bioluminescence imaging (BLI) represents one of its most outstanding uses by allowing the non-invasive localization of luciferase-expressing cells within a live animal. Despite the extensive use of luminescent reporters in mycobacteria, the resultant luminescent strains have not been fully applied to BLI. One of the main obstacles to the use of bioluminescence for in vivo imaging is the achievement of reporter protein expression levels high enough to obtain a signal that can be detected externally. Therefore, as a first step in the application of this technology to the study of mycobacterial infection in vivo, we have optimised the use of firefly, Gaussia and bacterial luciferases in mycobacteria using a combination of vectors, promoters, and codon-optimised genes. We report for the first time the functional expression of the whole bacterial lux operon in Mycobacterium tuberculosis and M. smegmatis thus allowing the development of auto-luminescent mycobacteria. We demonstrate that the Gaussia luciferase is secreted from bacterial cells and that this secretion does not require a signal sequence. Finally we prove that the signal produced by recombinant mycobacteria expressing either the firefly or bacterial luciferases can be non-invasively detected in the lungs of infected mice by bioluminescence imaging. While much work remains to be done, the finding that both firefly and bacterial luciferases can be detected non-invasively in live mice is an important first step to using these reporters to study the pathogenesis of M. tuberculosis and other mycobacterial species in vivo. Furthermore, the development of auto-luminescent mycobacteria has enormous ramifications for high throughput mycobacterial drug screening assays which are currently carried out either in a destructive manner using LuxAB or the firefly luciferase. |
| Audience | Academic |
| Author | Parish, Tanya Bancroft, Gregory J Schaible, Ulrich Robertson, Brian D Zelmer, Andrea Elkington, Paul T Fletcher, Taryn Andreu, Nuria Ward, Theresa H Ripoll, Jorge Wiles, Siouxsie |
| AuthorAffiliation | 4 Barts and the London School of Medicine and Dentistry, Queen Mary University of London, London, United Kingdom 2 Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom 3 Institute of Electronic Structure and Laser, Foundation for Research and Technology-Hellas, Heraklion, Crete, Greece Statens Serum Institute, Denmark 6 Department of Molecular Infection Research, Research Center Borstel, Borstel, Germany 7 Department of Molecular Medicine and Pathology, University of Auckland, Auckland, New Zealand 1 Department of Medicine, Imperial College London, London, United Kingdom 5 Infectious Diseases Research Institute, Seattle, Washington, United States of America |
| AuthorAffiliation_xml | – name: 6 Department of Molecular Infection Research, Research Center Borstel, Borstel, Germany – name: 2 Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom – name: 5 Infectious Diseases Research Institute, Seattle, Washington, United States of America – name: 1 Department of Medicine, Imperial College London, London, United Kingdom – name: 4 Barts and the London School of Medicine and Dentistry, Queen Mary University of London, London, United Kingdom – name: Statens Serum Institute, Denmark – name: 3 Institute of Electronic Structure and Laser, Foundation for Research and Technology-Hellas, Heraklion, Crete, Greece – name: 7 Department of Molecular Medicine and Pathology, University of Auckland, Auckland, New Zealand |
| Author_xml | – sequence: 1 givenname: Nuria surname: Andreu fullname: Andreu, Nuria organization: Department of Medicine, Imperial College London, London, UK – sequence: 2 givenname: Andrea surname: Zelmer fullname: Zelmer, Andrea – sequence: 3 givenname: Taryn surname: Fletcher fullname: Fletcher, Taryn – sequence: 4 givenname: Paul T surname: Elkington fullname: Elkington, Paul T – sequence: 5 givenname: Theresa H surname: Ward fullname: Ward, Theresa H – sequence: 6 givenname: Jorge surname: Ripoll fullname: Ripoll, Jorge – sequence: 7 givenname: Tanya surname: Parish fullname: Parish, Tanya – sequence: 8 givenname: Gregory J surname: Bancroft fullname: Bancroft, Gregory J – sequence: 9 givenname: Ulrich surname: Schaible fullname: Schaible, Ulrich – sequence: 10 givenname: Brian D surname: Robertson fullname: Robertson, Brian D – sequence: 11 givenname: Siouxsie surname: Wiles fullname: Wiles, Siouxsie |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/20520722$$D View this record in MEDLINE/PubMed |
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| Snippet | Mycobacterium tuberculosis, the causative agent of tuberculosis, still represents a major public health threat in many countries. Bioluminescence, the... Background Mycobacterium tuberculosis, the causative agent of tuberculosis, still represents a major public health threat in many countries. Bioluminescence,... BACKGROUNDMycobacterium tuberculosis, the causative agent of tuberculosis, still represents a major public health threat in many countries. Bioluminescence,... Background Mycobacterium tuberculosis , the causative agent of tuberculosis, still represents a major public health threat in many countries. Bioluminescence,... |
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| SubjectTerms | Animals Bacteria Bacterial infections Bioluminescence Biosensors Chemical reactions Chromosomes Codon - genetics Codons Drug resistance Drug screening E coli Enzymes Escherichia coli Fireflies Gaussia Gene Expression Genes, Reporter - genetics Genetic Vectors - genetics Health aspects Health risks House mouse Hygiene Imaging Imaging, Three-Dimensional - methods Immunology In vivo methods and tests Infectious diseases Infectious Diseases/Bacterial Infections Infectious Diseases/Respiratory Infections Kinetics Localization Luciferase Luciferases - metabolism Luminescent Proteins - genetics Luminescent Proteins - metabolism Lungs Medicine Mice Microbiology Microbiology/Medical Microbiology Molecular Biology Mycobacterium smegmatis Mycobacterium smegmatis - cytology Mycobacterium smegmatis - growth & development Mycobacterium smegmatis - metabolism Mycobacterium tuberculosis Pathogenesis Pharmaceutical sciences Plasmids Public health Radiology and Medical Imaging Secretion Streptococcus infections Streptococcus mutans Streptococcus pneumoniae Technology Technology application Tropical diseases Tuberculosis Vibrio cholerae Whole Body Imaging |
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| Title | Optimisation of bioluminescent reporters for use with mycobacteria |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/20520722 https://www.proquest.com/docview/1292618334/abstract/ https://search.proquest.com/docview/733143732 https://search.proquest.com/docview/746311612 https://pubmed.ncbi.nlm.nih.gov/PMC2875389 https://doaj.org/article/fd1d49049ccc428898603c2b2218c112 http://dx.doi.org/10.1371/journal.pone.0010777 |
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