Phagocytosis and Phagosome Acidification Are Required for Pathogen Processing and MyD88-Dependent Responses to Staphylococcus aureus
Open accessAbstract
Innate immunity is vital for protection from microbes and is mediated by humoral effectors, such as cytokines, and cellular immune defenses, including phagocytic cells (e.g., macrophages). After internalization by phagocytes, microbes are delivered into a phagosome, a complex intracellular organelle with a well-established and important role in microbial killing. However, the role of this organelle in cytokine responses and microbial sensing is less well defined. In this study, we assess the role of the phagosome in innate immune sensing and demonstrate the critical interdependence of phagocytosis and pattern recognition receptor signaling during response to the Gram-positive bacteria Staphylococcus aureus. We show that phagocytosis is essential to initiate an optimal MyD88-dependent response to Staphylococcus aureus. Prior to TLR-dependent cytokine production, bacteria must be engulfed and delivered into acidic phagosomes where acid-activated host enzymes digest the internalized bacteria to liberate otherwise cryptic bacterial-derived ligands that initiate responses from the vacuole. Importantly, in macrophages in which phagosome acidification is perturbed, the impaired response to S. aureus can be rescued by the addition of lysostaphin, a bacterial endopeptidase active at neutral pH that can substitute for the acid-activated host enzymes. Together, these observations delineate the interdependence of phagocytosis with pattern recognition receptor signaling and suggest that therapeutics to augment functions and signaling from the vacuole may be useful strategies to increase host responses to S. aureus.
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The acidic environment of phagosomes provides the right conditions to produce RNS leading to lysis of pathogens.
“This mechanism is important during phagocytosis, as the acidic environment of phagosomes provides the right conditions to produce RNS leading to the lysis of pathogens [129].”
From The Role of Reactive Species on Innate Immunity (2022) · cites this paper as [129]
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- Authors
- Ip, W. K. E., Sokolovska, A., Charriere, G. M., Boyer, L., Dejardin, S., Cappillino, M. P., Yantosca, L. M., Takahashi, K., Moore, K. J., Lacy-Hulbert, A., & Stuart, L. M.
- Affiliations
- Harvard University (US)
- Developmental Immunology
- Corresponding author
- Sokolovska, Anna
- Boyer, Laurent
- Takahashi, Kazue
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-06
- Volume
- 184
- Issue
- 12
- Pages
- 7071-7081
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- PMC
- PMC2935932
- OpenAlex
- W2098650503
- Cited by
- 148
- References
- 33
- Citations by year
- 2026: 6 · 2025: 2 · 2024: 3 · 2023: 7 · 2022: 6 · 2021: 12 · 2020: 11 · 2019: 11 · 2018: 12 · 2017: 12 · 2016: 7 · 2015: 11 · 2014: 17 · 2013: 9 · 2012: 13
- FWCI
- 4.26
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Massachusetts General Hospital
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (R01AI079198)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK043351)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Keywords
- phagocytosis, phagosome acidification, Staphylococcus aureus, MyD88 signaling, macrophages, innate immunity, pattern recognition receptors, lysostaphin, cytokine production, Gram-positive bacteria
- MeSH terms
- Animals, Enzyme-Linked Immunosorbent Assay, Hydrogen-Ion Concentration, Macrophage Activation, Macrophages, Mice, Inbred C57BL, Phagocytosis, Phagosomes, Staphylococcal Infections, Staphylococcus aureus, Cytokines, Reverse Transcriptase Polymerase Chain Reaction, Mice, Myeloid Differentiation Factor 88
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