Cytosolic detection of phagosomal bacteria—Mechanisms underlying PAMP exodus from the phagosome into the cytosol

The metazoan innate immune system senses bacterial infections by detecting highly conserved bacterial molecules, termed pathogen‐associated molecular patterns (PAMPs). PAMPs are detected by a variety of host pattern recognition receptors (PRRs), whose function is to coordinate downstream immune resp...

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Vydáno v:	Molecular microbiology Ročník 116; číslo 6; s. 1420 - 1432
Hlavní autoři:	Ragland, Stephanie A., Kagan, Jonathan C.
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	England Blackwell Publishing Ltd 01.12.2021
Témata:	Animals Bacteria Bacteria - genetics Bacteria - metabolism Bacterial diseases Bacterial infections Bacterial Infections - genetics Bacterial Infections - metabolism Bacterial Infections - microbiology Bacterial Infections - physiopathology caspase‐11 caspase‐4 caspase‐5 cGAS cyclic dinucleotides Cytosol Cytosol - metabolism Cytosol - microbiology guanylate binding proteins Humans Immune response Immune system Innate immunity lipopolysaccharide macrophage Membranes Pathogen-Associated Molecular Pattern Molecules - metabolism pathogen‐associated molecular pattern Pattern recognition pattern recognition receptor Pattern recognition receptors Phagocytes Phagocytosis phagosome Phagosomes Phagosomes - genetics Phagosomes - metabolism Phagosomes - microbiology Receptor mechanisms Receptors, Pattern Recognition - genetics Receptors, Pattern Recognition - metabolism STING caspase-5 cyclic dinucleotides cGAS STING macrophage phagosome caspase-11 lipopolysaccharide guanylate binding proteins pathogen-associated molecular pattern caspase-4 pattern recognition receptor
ISSN:	0950-382X, 1365-2958, 1365-2958
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Abstract	The metazoan innate immune system senses bacterial infections by detecting highly conserved bacterial molecules, termed pathogen‐associated molecular patterns (PAMPs). PAMPs are detected by a variety of host pattern recognition receptors (PRRs), whose function is to coordinate downstream immune responses. PRR activities are, in part, regulated by their subcellular localizations. Accordingly, professional phagocytes can detect extracellular bacteria and their PAMPs via plasma membrane‐oriented PRRs. Conversely, phagocytosed bacteria and their PAMPs are detected by transmembrane PRRs oriented toward the phagosomal lumen. Even though PAMPs are unable to passively diffuse across membranes, phagocytosed bacteria are also detected by PRRs localized within the host cell cytosol. This phenomenon is explained by phagocytosis of bacteria that specialize in phagosomal escape and cytosolic residence. Contrary to this cytosolic lifestyle, most bacteria studied to date spend their entire intracellular lifestyle contained within phagosomes, yet they also stimulate cytosolic PRRs. Herein, we will review our current understanding of how phagosomal PAMPs become accessible to cytosolic PRRs, as well as highlight knowledge gaps that should inspire future investigations. The graphical illustrates the several means by which bacterial products may exit phagosomes to stimulate innate immune receptors present in the cytoplasm of eukaryotic cells. Each of these means of pathogen‐associated molecular pattern exodus is discussed in this review.
AbstractList	The metazoan innate immune system senses bacterial infections by detecting highly conserved bacterial molecules, termed pathogen-associated molecular patterns (PAMPs). PAMPs are detected by a variety of host pattern recognition receptors (PRRs), whose function is to coordinate downstream immune responses. PRR activities are, in part, regulated by their subcellular localizations. Accordingly, professional phagocytes can detect extracellular bacteria and their PAMPs via plasma membrane-oriented PRRs. Conversely, phagocytosed bacteria and their PAMPs are detected by transmembrane PRRs oriented toward the phagosomal lumen. Even though PAMPs are unable to passively diffuse across membranes, phagocytosed bacteria are also detected by PRRs localized within the host cell cytosol. This phenomenon is explained by phagocytosis of bacteria that specialize in phagosomal escape and cytosolic residence. Contrary to this cytosolic lifestyle, most bacteria studied to date spend their entire intracellular lifestyle contained within phagosomes, yet they also stimulate cytosolic PRRs. Herein, we will review our current understanding of how phagosomal PAMPs become accessible to cytosolic PRRs, as well as highlight knowledge gaps that should inspire future investigations.The metazoan innate immune system senses bacterial infections by detecting highly conserved bacterial molecules, termed pathogen-associated molecular patterns (PAMPs). PAMPs are detected by a variety of host pattern recognition receptors (PRRs), whose function is to coordinate downstream immune responses. PRR activities are, in part, regulated by their subcellular localizations. Accordingly, professional phagocytes can detect extracellular bacteria and their PAMPs via plasma membrane-oriented PRRs. Conversely, phagocytosed bacteria and their PAMPs are detected by transmembrane PRRs oriented toward the phagosomal lumen. Even though PAMPs are unable to passively diffuse across membranes, phagocytosed bacteria are also detected by PRRs localized within the host cell cytosol. This phenomenon is explained by phagocytosis of bacteria that specialize in phagosomal escape and cytosolic residence. Contrary to this cytosolic lifestyle, most bacteria studied to date spend their entire intracellular lifestyle contained within phagosomes, yet they also stimulate cytosolic PRRs. Herein, we will review our current understanding of how phagosomal PAMPs become accessible to cytosolic PRRs, as well as highlight knowledge gaps that should inspire future investigations. The metazoan innate immune system senses bacterial infections by detecting highly conserved bacterial molecules, termed pathogen-associated molecular patterns (PAMPs). PAMPs are detected by a variety of host pattern recognition receptors (PRRs), whose function is to coordinate downstream immune responses. PRR activities are, in part, regulated by their subcellular localizations. Accordingly, professional phagocytes can detect extracellular bacteria and their PAMPs via plasma membrane-oriented PRRs. Conversely, phagocytosed bacteria and their PAMPs are detected by transmembrane PRRs oriented towards the phagosomal lumen. Even though PAMPs are unable to passively diffuse across membranes, phagocytosed bacteria are also detected by PRRs localized within the host cell cytosol. This phenomenon is explained upon phagocytosis of bacteria that specialize in phagosomal escape and cytosolic residence. Contrary to this cytosolic lifestyle, most bacteria studied to date spend their entire intracellular lifestyle contained within phagosomes, yet they also stimulate cytosolic PRRs. Herein, we will review our current understanding for how phagosomal PAMPs become accessible to cytosolic PRRs, as well as highlight knowledge gaps that should inspire future investigations. The graphical abstract illustrates the several means by which bacterial products may exit phagosomes to stimulate innate immune receptors present in the cytoplasm of eukaryotic cells. Each of these means of PAMP exodus are discussion in this review. Although the phagosomal membrane separates phagosomal bacteria and their PAMPs from the cytosol, phagosomal bacteria can stimulate cytosolic PRRs.Bacteria produce factors (e.g., toxins and secretion systems) that potentiate PAMP exodus from the phagosome into the cytosol to activate cytosolic PRRs.Host cells produce PAMP transporters and membranolytic proteins that aid in PAMP exodus from the phagosome into the cytosol to activate cytosolic PRRs. The metazoan innate immune system senses bacterial infections by detecting highly conserved bacterial molecules, termed pathogen‐associated molecular patterns (PAMPs). PAMPs are detected by a variety of host pattern recognition receptors (PRRs), whose function is to coordinate downstream immune responses. PRR activities are, in part, regulated by their subcellular localizations. Accordingly, professional phagocytes can detect extracellular bacteria and their PAMPs via plasma membrane‐oriented PRRs. Conversely, phagocytosed bacteria and their PAMPs are detected by transmembrane PRRs oriented toward the phagosomal lumen. Even though PAMPs are unable to passively diffuse across membranes, phagocytosed bacteria are also detected by PRRs localized within the host cell cytosol. This phenomenon is explained by phagocytosis of bacteria that specialize in phagosomal escape and cytosolic residence. Contrary to this cytosolic lifestyle, most bacteria studied to date spend their entire intracellular lifestyle contained within phagosomes, yet they also stimulate cytosolic PRRs. Herein, we will review our current understanding of how phagosomal PAMPs become accessible to cytosolic PRRs, as well as highlight knowledge gaps that should inspire future investigations. The metazoan innate immune system senses bacterial infections by detecting highly conserved bacterial molecules, termed pathogen‐associated molecular patterns (PAMPs). PAMPs are detected by a variety of host pattern recognition receptors (PRRs), whose function is to coordinate downstream immune responses. PRR activities are, in part, regulated by their subcellular localizations. Accordingly, professional phagocytes can detect extracellular bacteria and their PAMPs via plasma membrane‐oriented PRRs. Conversely, phagocytosed bacteria and their PAMPs are detected by transmembrane PRRs oriented toward the phagosomal lumen. Even though PAMPs are unable to passively diffuse across membranes, phagocytosed bacteria are also detected by PRRs localized within the host cell cytosol. This phenomenon is explained by phagocytosis of bacteria that specialize in phagosomal escape and cytosolic residence. Contrary to this cytosolic lifestyle, most bacteria studied to date spend their entire intracellular lifestyle contained within phagosomes, yet they also stimulate cytosolic PRRs. Herein, we will review our current understanding of how phagosomal PAMPs become accessible to cytosolic PRRs, as well as highlight knowledge gaps that should inspire future investigations. The graphical illustrates the several means by which bacterial products may exit phagosomes to stimulate innate immune receptors present in the cytoplasm of eukaryotic cells. Each of these means of pathogen‐associated molecular pattern exodus is discussed in this review.
Author	Ragland, Stephanie A. Kagan, Jonathan C.
Author_xml	– sequence: 1 givenname: Stephanie A. orcidid: 0000-0003-3614-2652 surname: Ragland fullname: Ragland, Stephanie A. organization: Boston Children’s Hospital and Harvard Medical School – sequence: 2 givenname: Jonathan C. orcidid: 0000-0003-2364-2746 surname: Kagan fullname: Kagan, Jonathan C. email: jonathan.kagan@childrens.harvard.edu organization: Boston Children’s Hospital and Harvard Medical School
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Keywords	caspase-5 cyclic dinucleotides cGAS STING macrophage phagosome caspase-11 lipopolysaccharide guanylate binding proteins pathogen-associated molecular pattern caspase-4 pattern recognition receptor
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Snippet	The metazoan innate immune system senses bacterial infections by detecting highly conserved bacterial molecules, termed pathogen‐associated molecular patterns... The metazoan innate immune system senses bacterial infections by detecting highly conserved bacterial molecules, termed pathogen-associated molecular patterns...
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SubjectTerms	Animals Bacteria Bacteria - genetics Bacteria - metabolism Bacterial diseases Bacterial infections Bacterial Infections - genetics Bacterial Infections - metabolism Bacterial Infections - microbiology Bacterial Infections - physiopathology caspase‐11 caspase‐4 caspase‐5 cGAS cyclic dinucleotides Cytosol Cytosol - metabolism Cytosol - microbiology guanylate binding proteins Humans Immune response Immune system Innate immunity lipopolysaccharide macrophage Membranes Pathogen-Associated Molecular Pattern Molecules - metabolism pathogen‐associated molecular pattern Pattern recognition pattern recognition receptor Pattern recognition receptors Phagocytes Phagocytosis phagosome Phagosomes Phagosomes - genetics Phagosomes - metabolism Phagosomes - microbiology Receptor mechanisms Receptors, Pattern Recognition - genetics Receptors, Pattern Recognition - metabolism STING
Title	Cytosolic detection of phagosomal bacteria—Mechanisms underlying PAMP exodus from the phagosome into the cytosol
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