Intracellular Growth of Bacterial Pathogens: The Role of Secreted Effector Proteins in the Control of Phagocytosed Microorganisms
- Authors: Valérie Poirier1, Yossef Av-Gay2
- Editors: Indira T. Kudva3, John P. Bannantine4
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VIEW AFFILIATIONS HIDE AFFILIATIONSAffiliations: 1: Division of Infectious Diseases, Department of Medicine, University of British Columbia, Vancouver, BC V6H 3Z6; 2: Division of Infectious Diseases, Department of Medicine, University of British Columbia, Vancouver, BC V6H 3Z6; 3: National Animal Disease Center, Agricultural Research Service, U.S. Department of Agriculture, Ames, IA; 4: National Animal Disease Center, Agricultural Research Service, U.S. Department of Agriculture, Ames, IA
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Received 13 December 2014 Accepted 15 April 2015 Published 18 December 2015
- Correspondence: Yossef Av-Gay, [email protected]

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Abstract:
The ability of intracellular pathogens to subvert the host response, to facilitate invasion and subsequent infection, is the hallmark of microbial pathogenesis. Bacterial pathogens produce and secrete a variety of effector proteins, which are the primary means by which they exert control over the host cell. Secreted effectors work independently, yet in concert with each other, to facilitate microbial invasion, replication, and intracellular survival in host cells. In this review we focus on defined host cell processes targeted by bacterial pathogens. These include phagosome maturation and its subprocesses: phagosome-endosome and phagosome-lysosome fusion events, as well as phagosomal acidification, cytoskeleton remodeling, and lysis of the phagosomal membrane. We further describe the mode of action for selected effectors from six pathogens: the Gram-negative Legionella, Salmonella, Shigella, and Yersinia, the Gram-positive Listeria, and the acid-fast actinomycete Mycobacterium.
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Citation: Poirier V, Av-Gay Y. 2015. Intracellular Growth of Bacterial Pathogens: The Role of Secreted Effector Proteins in the Control of Phagocytosed Microorganisms. Microbiol Spectrum 3(6):VMBF-0003-2014. doi:10.1128/microbiolspec.VMBF-0003-2014.




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Abstract:
The ability of intracellular pathogens to subvert the host response, to facilitate invasion and subsequent infection, is the hallmark of microbial pathogenesis. Bacterial pathogens produce and secrete a variety of effector proteins, which are the primary means by which they exert control over the host cell. Secreted effectors work independently, yet in concert with each other, to facilitate microbial invasion, replication, and intracellular survival in host cells. In this review we focus on defined host cell processes targeted by bacterial pathogens. These include phagosome maturation and its subprocesses: phagosome-endosome and phagosome-lysosome fusion events, as well as phagosomal acidification, cytoskeleton remodeling, and lysis of the phagosomal membrane. We further describe the mode of action for selected effectors from six pathogens: the Gram-negative Legionella, Salmonella, Shigella, and Yersinia, the Gram-positive Listeria, and the acid-fast actinomycete Mycobacterium.

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Figures
Stages of phagosome maturation. During phagocytosis, the phagosome undergoes a series of fusion and fission events with vesicles of the endocytic pathway, culminating in the formation of the phagolysosome. Maturation of the phagosome involves gradual decrease in pH and acquisition of antimicrobial properties, leading to the digestion of the invader and presentation of antigens on the surface of the phagocyte by MHC-II molecules.

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FIGURE 1
Stages of phagosome maturation. During phagocytosis, the phagosome undergoes a series of fusion and fission events with vesicles of the endocytic pathway, culminating in the formation of the phagolysosome. Maturation of the phagosome involves gradual decrease in pH and acquisition of antimicrobial properties, leading to the digestion of the invader and presentation of antigens on the surface of the phagocyte by MHC-II molecules.
Microbial effectors interfering with intracellular trafficking and acidification events. Orange proteins represent Legionella virulence factors; pink, Mycobacterium virulence factors; and blue, Salmonella virulence factors.

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FIGURE 2
Microbial effectors interfering with intracellular trafficking and acidification events. Orange proteins represent Legionella virulence factors; pink, Mycobacterium virulence factors; and blue, Salmonella virulence factors.
Cytoskeleton remodeling, vacuolar membrane lysis, and phagosomal membrane remodeling by microbial pathogens. Orange proteins represent Legionella virulence factors; red, Listeria virulence factors; blue, Salmonella virulence factors; and green, Shigella virulence factors.

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FIGURE 3
Cytoskeleton remodeling, vacuolar membrane lysis, and phagosomal membrane remodeling by microbial pathogens. Orange proteins represent Legionella virulence factors; red, Listeria virulence factors; blue, Salmonella virulence factors; and green, Shigella virulence factors.
Tables
Host physiological events and substrates targeted by effectors secreted by Legionella, Listeria, Mycobacterium, Salmonella, Shigella, and Yersinia species

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TABLE 1
Host physiological events and substrates targeted by effectors secreted by Legionella, Listeria, Mycobacterium, Salmonella, Shigella, and Yersinia species
Supplemental Material
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