Mycobacterium marinum induces a marked LC3 recruitment to its containing phagosome that depends on a functional ESX-1 secretion system: Live M. marinum transiently resides in LC3-labelled compartments
Open accessAbstract
Autophagy has been implicated as part of the innate immune system against different intracellular microorganisms. Mycobacterium marinum is the causative agent of the fish-tank granuloma and has been widely used as an alternative model to study pathogenic mycobacteria. In this report, we show an active interaction of M. marinum with the autophagic protein LC3, an event that requires pathogen viability and bacterial protein synthesis. Interestingly, M. marinum lacking the region of difference 1 (RD1) is unable to recruit LC3, indicating that a functional ESX-1 secretion system is an absolute requirement for this process. In addition, phagocytosis of the bacteria is also a condition for the LC3 rearrangement induced by M. marinum. We present evidence that this pathogen resides temporarily in a LC3-decorated compartment with late endocytic features but mostly devoid of lysosomal enzymes or degradative properties. In addition our results indicate that autophagy induction by rapamycin treatment leads to maturation of the M. marinum-containing compartment.
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LC3 can be recruited to single-membrane phagosomes in a process termed LC3-associated phagocytosis (LAP).
“Recently, it has been demonstrated that LC3 can be recruited to other membranes including single-membrane phagosomes, in a process termed LC3-associated phagocytosis (LAP).”
From LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy (2012) · cites this paper as [15]
The Discussion (page unavailable) states that most LC3-decorated M. marinum phagosomes had a single bilayer, supporting LC3 recruitment to single-membrane phagosomes. Our copy does not call this process LC3-associated phagocytosis (LAP); the GFP-LC3 results section also reports occasional fusion of an autophagosome with a phagosome, so the paper does not establish that its observed recruitment is specifically LAP. (LLM, conf=0.83)
Experimental — accuracy not yet measuredIn pathogen-related LAP, bacterial viability is required to initiate recruitment of LC3 to the phagosome.
“In these instances of pathogen-related LAP, bacterial viability is required in order to initiate the recruitment of LC3 to the phagosome [15].”
From LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy (2012) · cites this paper as [15]
The section ‘LC3 recruitment to the M. marinum-containing phagosome depends on bacterial viability’ (page not provided) reports markedly reduced LC3 recruitment with heat-inactivated or antibiotic-treated M. marinum. It supports a viability requirement for this bacterium under the tested control and starvation conditions, but not for pathogen-related LAP generally; the paper also reports LC3 recruitment to phagosomes containing nonviable bacteria after rapamycin treatment. (LLM, conf=0.86)
Experimental — accuracy not yet measuredLC3 decorated Mycobacterium marinum-containing phagosomes after infection of RAW cells.
“Furthermore, by following the indirect immunofluorescence staining of endogenous LC3, Lerena and Colombo [15] showed that LC3 decorated Mycobacterium marinum-containing phagosomes after infection of RAW cells.”
From LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy (2012) · cites this paper as [15]
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Yamamoto, A., Tagawa, Y., Yoshimori, T., Moriyama, Y., Masaki, R., & Tashiro, Y. (1998) · Cell Structure and Function · doi:10.1247/csf.23.33 · Cited by 1,312 · see citing works
Mestre, M. B., Fader, C. M., Sola, C., & Colombo, M. I. (2010) · Autophagy · doi:10.4161/auto.6.1.10698 · Cited by 152 · see citing works
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Watson, R. O., Manzanillo, P. S., & Cox, J. S. (2012) · Cell · doi:10.1016/j.cell.2012.06.040 · Cited by 755 · see citing works
LC3-Associated Phagocytosis and Inflammation
Heckmann, B. L., Boada-Romero, E., Cunha, L. D., Magne, J., & Green, D. R. (2017) · Journal of Molecular Biology · doi:10.1016/j.jmb.2017.08.012 · Cited by 276 · see citing works
LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy
Lai, S.-C., & Devenish, R. J. (2012) · Cells · doi:10.3390/cells1030396 · Cited by 116 · see citing works
“Furthermore, by following the indirect immunofluorescence staining of endogenous LC3, Lerena and Colombo [15] showed that LC3 decorated Mycobacterium marinumcontaining phagosomes after infection of RAW cells.”
BackgroundInfluentialRovetta, A. I., Peña, D., Hernández Del Pino, R. E., Recalde, G. M., Pellegrini, J., Bigi, F., Musella, R. M., Palmero, D. J., Gutierrez, M., Colombo, M. I., et al. (2014) · Autophagy · doi:10.4161/15548627.2014.981791 · Cited by 71 · see citing works
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- Authors
- Lerena, M. C., & Colombo, M. I.
- Affiliations
- Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
- Corresponding author
- Colombo, María Isabel
- Venue
- Cellular Microbiology
- Publisher
- Wiley
- Published
- 2011-03-30
- Volume
- 13
- Issue
- 6
- Pages
- 814-835
- ISSN
- 1462-5814 (ISSN-L)
- OpenAlex
- W1843159017
- Cited by
- 85
- References
- 2
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 4 · 2023: 3 · 2022: 3 · 2021: 6 · 2020: 2 · 2019: 7 · 2018: 5 · 2017: 9 · 2016: 9 · 2015: 4 · 2014: 12 · 2013: 8 · 2012: 6
- FWCI
- 5.85
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Cellular Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Consejo Nacional de Investigaciones Científicas y Técnicas
- Universidad Nacional de Cuyo
- Agencia Nacional de Promoción Científica y Tecnológica
- Topics
- Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Health Sciences › Medicine › Epidemiology › Mycobacterium research and diagnosis
- Keywords
- Mycobacterium marinum, autophagy, ESX-1 secretion system, phagosome, phagocytosis, fish tank granuloma, mycobacterial pathogenesis, rapamycin
- MeSH terms
- Bacterial Proteins, Humans, Macrophages, Microtubule-Associated Proteins, Phagosomes, Mycobacterium marinum, Membrane Transport Proteins
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