Author:
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Reference Manager
BibTeX
Zotero
EndNote
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In Vivo Imaging of Bioluminescent Mycobacterium ulcerans: A Tool to Refine the Murine Buruli Ulcer Tail Model
Till F. Omansen
Till F. Omansen
Department of Microbiology and Immunology, The Peter Doherty Institute for Infection and Immunity, University of Melbourne, Parkville, Australia;
Department of Internal Medicine/Infectious Diseases, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands;
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Department of Internal Medicine/Infectious Diseases, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands;
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Renee A. Marcsisin
Renee A. Marcsisin
Department of Microbiology and Immunology, The Peter Doherty Institute for Infection and Immunity, University of Melbourne, Parkville, Australia;
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Brendon Y. Chua
Brendon Y. Chua
Department of Microbiology and Immunology, The Peter Doherty Institute for Infection and Immunity, University of Melbourne, Parkville, Australia;
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Weiguang Zeng
Weiguang Zeng
Department of Microbiology and Immunology, The Peter Doherty Institute for Infection and Immunity, University of Melbourne, Parkville, Australia;
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David C. Jackson
David C. Jackson
Department of Microbiology and Immunology, The Peter Doherty Institute for Infection and Immunity, University of Melbourne, Parkville, Australia;
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Jessica L. Porter
Jessica L. Porter
Department of Microbiology and Immunology, The Peter Doherty Institute for Infection and Immunity, University of Melbourne, Parkville, Australia;
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Ymkje Stienstra
Ymkje Stienstra
Department of Internal Medicine/Infectious Diseases, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands;
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Tjip S. van der Werf
Tjip S. van der Werf
Department of Internal Medicine/Infectious Diseases, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands;
Department of Pulmonary Diseases and Tuberculosis, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands
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Department of Pulmonary Diseases and Tuberculosis, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands
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Timothy P. Stinear
Timothy P. Stinear
Department of Microbiology and Immunology, The Peter Doherty Institute for Infection and Immunity, University of Melbourne, Parkville, Australia;
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Buruli ulcer (BU) is a neglected tropical disease caused by infection with Mycobacterium ulcerans. Unclear transmission, no available vaccine, and suboptimal treatment regimens hamper the control of this disease. Carefully designed preclinical research is needed to address these shortcomings. In vivo imaging (IVIS®, Perkin Elmer, Waltham, MA) of infection is an emerging tool that permits monitoring of disease progression and reduces the need to using large numbers of mice at different time-points during the experiment, as individual mice can be imaged at multiple time-points. We aimed to further describe the use of in vivo imaging (IVIS) in BU. We studied the detection of M. ulcerans in experimentally infected BALB/c mouse tails and the subsequent histopathology and immune response in this pilot study. IVIS-monitoring was performed weekly in ten infected BALB/c mice to measure light emitted as a proxy for bacterial load. Nine of 10 (90%) BALB/c mice infected subcutaneously with 3.3 × 105 M. ulcerans JKD8049 (containing pMV306 hsp16+luxG13) exhibited light emission from the site of infection, indicating M. ulcerans growth in vivo, whereas only five of 10 (50%) animals developed clinical signs of the disease. Specific antibody titers were detected within 2 weeks of the infection. Interferon (IFN)-γ and interleukin (IL)-10 were elevated in animals with pathology. Histopathology revealed clusters of acid-fast bacilli in the subcutaneous tissue, with macrophage infiltration and granuloma formation resembling human BU. Our study successfully showed the utility of M. ulcerans IVIS monitoring and lays a foundation for further research.
Author Notes
Authors’ addresses: Till F. Omansen and Ymkje Stienstra, Department of Internal Medicine/Infectious Diseases, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands, E-mails: t.f.omansen@umcg.nl and y.stienstra@umcg.nl. Renee A. Marcsisin, Brendon Y. Chua, Weiguang Zeng, David C. Jackson, Jessica L. Porter, and Timothy P. Stinear, Department of Microbiology and Immunology, The Peter Doherty Institute for Infection and Immunity, University of Melbourne, Parkville, Australia, E-mails: reneemarcsisin@gmail.com, bychua@unimelb.edu.au, weiguang@unimelb.edu.au, davidcj@unimelb.edu.au, jlporter@unimelb.edu.au, and tstinear@unimelb.edu.au. Tjip S. van der Werf, Department of Pulmonary Diseases and Tuberculosis, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands, E-mail: t.s.van.der.werf@umcg.nl.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
van der Werf TS et al. 2005. Mycobacterium ulcerans disease. Bull World Health Organ 83: 785–791.
-
2.
WHO, 2019. Buruli Ulcer Fact Sheet. Available at: https://www.who.int/news-room/fact-sheets/detail/buruli-ulcer-(mycobacterium-ulcerans-infection). Accessed May 21, 2019.
-
3.
de Zeeuw J et al. 2014. Persisting social participation restrictions among former Buruli ulcer patients in Ghana and Benin. PLoS Negl Trop Dis 8: e3303.
-
4.
George KM, Chatterjee D, Gunawardana G, Welty D, Hayman J, Lee R, Small PL, 1999. Mycolactone: a polyketide toxin from Mycobacterium ulcerans required for virulence. Science 283: 854–857.
-
5.
George KM, Pascopella L, Welty DM, Small PL, 2000. A Mycobacterium ulcerans toxin, mycolactone, causes apoptosis in Guinea pig ulcers and tissue culture cells. Infect Immun 68: 877–883.
-
6.
Hall BS, Hill K, McKenna M, Ogbechi J, High S, Willis AE, Simmonds RE, 2014. The pathogenic mechanism of the Mycobacterium ulcerans virulence factor, mycolactone, depends on blockade of protein translocation into the ER. PLoS Pathog 10: e1004061.
-
7.
Demangel C, High S, 2018. Sec61 blockade by mycolactone: a central mechanism in Buruli ulcer disease. Biol Cell 110: 237–248.
-
8.
Stinear TP et al. 2004. Giant plasmid-encoded polyketide synthases produce the macrolide toxin of Mycobacterium ulcerans. Proc Natl Acad Sci USA 101: 1345–1349.
-
9.
Meyers WM, Shelly WM, Connor DH, 1974. Heat treatment of Mycobacterium ulcerans infections without surgical excision. Am J Trop Med Hyg 23: 924–929.
-
10.
Wallace JR et al. 2017. Mycobacterium ulcerans low infectious dose and mechanical transmission support insect bites and puncturing injuries in the spread of Buruli ulcer. PLoS Negl Trop Dis 11: e0005553.
-
11.
Johnson PD, Azuolas J, Lavender CJ, Wishart E, Stinear TP, Hayman JA, Brown L, Jenkin GA, Fyfe JA, 2007. Mycobacterium ulcerans in mosquitoes captured during outbreak of Buruli ulcer, southeastern Australia. Emerg Infect Dis 13: 1653–1660.
-
12.
Lavender CJ, Fyfe JA, Azuolas J, Brown K, Evans RN, Ray LR, Johnson PD, 2011. Risk of Buruli ulcer and detection of Mycobacterium ulcerans in mosquitoes in southeastern Australia. PLoS Negl Trop Dis 5: e1305.
-
13.
Etuaful S et al. 2005. Efficacy of the combination rifampin-streptomycin in preventing growth of Mycobacterium ulcerans in early lesions of Buruli ulcer in humans. Antimicrob Agents Chemother 49: 3182–3186.
-
14.
Nienhuis WA et al. 2010. Antimicrobial treatment for early, limited Mycobacterium ulcerans infection: a randomised controlled trial. Lancet 375: 664–672.
-
15.
Kibadi K et al. 2010. Response to treatment in a prospective cohort of patients with large ulcerated lesions suspected to be Buruli ulcer (Mycobacterium ulcerans disease). PLoS Negl Trop Dis 4: e736.
-
16.
Wadagni AC, Barogui YT, Johnson RC, Sopoh GE, Affolabi D, van der Werf TS, de Zeeuw J, Kleinnijenhuis J, Stienstra Y, 2018. Delayed versus standard assessment for excision surgery in patients with Buruli ulcer in Benin: a randomised controlled trial. Lancet Infect Dis 18: 650–656.
-
17.
Einarsdottir T, Huygen K, 2011. Buruli ulcer. Hum Vaccin 7: 1198–1203.
-
18.
Dega H, Robert J, Bonnafous P, Jarlier V, Grosset J, 2000. Activities of several antimicrobials against Mycobacterium ulcerans infection in mice. Antimicrob Agents Chemother 44: 2367–2372.
-
19.
Bentoucha A, Robert J, Dega H, Lounis N, Jarlier V, Grosset J, 2001. Activities of new macrolides and fluoroquinolones against Mycobacterium ulcerans infection in mice. Antimicrob Agents Chemother 45: 3109–3112.
-
20.
Dega H, Bentoucha A, Robert J, Jarlier V, Grosset J, 2002. Bactericidal activity of rifampin-amikacin against Mycobacterium ulcerans in mice. Antimicrob Agents Chemother 46: 3193–3196.
-
21.
Marsollier L, Robert R, Aubry J, Saint André J-P, Kouakou H, Legras P, Manceau AL, Mahaza C, Carbonnelle B, 2002. Aquatic insects as a vector for Mycobacterium ulcerans. Appl Environ Microbiol 68: 4623–4628.
-
22.
Shepard CC, 1960. The experimental disease that follows the injection of human leprosy bacilli into foot-pads of mice. J Exp Med 112: 445–454.
-
23.
Tanghe A, Dangy J-P, Pluschke G, Huygen K, 2008. Improved protective efficacy of a species-specific DNA vaccine encoding mycolyl-transferase Ag85A from Mycobacterium ulcerans by homologous protein boosting. PLoS Negl Trop Dis 2: e199.
-
24.
Tanghe A, Adnet P-Y, Gartner T, Huygen K, 2007. A booster vaccination with Mycobacterium bovis BCG does not increase the protective effect of the vaccine against experimental Mycobacterium ulcerans infection in mice. Infect Immun 75: 2642–2644.
-
25.
Dhople AM, Namba K, 2003. Activities of sitafloxacin (DU-6859a), either singly or in combination with rifampin, against Mycobacterium ulcerans infection in mice. J Chemother 15: 47–52.
-
26.
Converse PJ et al. 2018. Shorter-course treatment for Mycobacterium ulcerans disease with high-dose rifamycins and clofazimine in a mouse model of Buruli ulcer. PLoS Negl Trop Dis 12: e0006728.
-
27.
Converse PJ, Xing Y, Kim KH, Tyagi S, Li S-Y, Almeida DV, Nuermberger EL, Grosset JH, Kishi Y, 2014. Accelerated detection of mycolactone production and response to antibiotic treatment in a mouse model of Mycobacterium ulcerans disease. PLoS Negl Trop Dis 8: e2618.
-
28.
Sarfo FS, Converse PJ, Almeida DV, Zhang J, Robinson C, Wansbrough-Jones M, Grosset JH, 2013. Microbiological, histological, immunological, and toxin response to antibiotic treatment in the mouse model of Mycobacterium ulcerans disease. PLoS Negl Trop Dis 7: e2101.
-
29.
Converse PJ, Almeida DV, Nuermberger EL, Grosset JH, 2011. BCG-mediated protection against Mycobacterium ulcerans infection in the mouse. PLoS Negl Trop Dis 5: e985.
-
30.
Zhang T, Li SY, Converse PJ, Almeida DV, Grosset JH, Nuermberger EL, 2011. Using bioluminescence to monitor treatment response in real time in mice with Mycobacterium ulcerans infection. Antimicrob Agents Chemother 55: 56–61.
-
31.
Zhang T, Bishai WR, Grosset JH, Nuermberger EL, 2010. Rapid assessment of antibacterial activity against Mycobacterium ulcerans by using recombinant luminescent strains. Antimicrob Agents Chemother 54: 2806–2813.
-
32.
Almeida D, Converse PJ, Ahmad Z, Dooley KE, Nuermberger EL, Grosset JH, 2011. Activities of rifampin, rifapentine and clarithromycin alone and in combination against Mycobacterium ulcerans disease in mice. PLoS Negl Trop Dis 5: e933.
-
33.
Almeida DV, Converse PJ, Li S-Y, Tyagi S, Nuermberger EL, Grosset JH, 2013. Bactericidal activity does not predict sterilizing activity: the case of rifapentine in the murine model of Mycobacterium ulcerans disease. PLoS Negl Trop Dis 7: e2085.
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