Peptidoglycan induces loss of a nuclear peptidoglycan recognition protein during host tissue development in a beneficial animal-bacterial symbiosis |
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Authors: | Joshua V. Troll Dawn M. Adin rew M. Wier Nicholas Paquette Neal Silverman William E. Goldman Frank J. Stadermann Eric V. Stabb Margaret J. McFall-Ngai |
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Affiliation: | Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, WI 53706, USA.; Department of Microbiology, University of Georgia, Athens, GA 30602, USA.; Division of Infectious Diseases, Department of Medicine, University of Massachusetts Medical School, Worcester, MA 01605, USA.; Department of Microbiology and Immunology, University of North Carolina, Chapel Hill, NC 27599, USA.; Department of Physics, Laboratory of Space Sciences, Washington University, St. Louis, MO 63130, USA. |
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Abstract: | Peptidoglycan recognition proteins (PGRPs) are mediators of innate immunity and recently have been implicated in developmental regulation. To explore the interplay between these two roles, we characterized a PGRP in the host squid Euprymna scolopes (EsPGRP1) during colonization by the mutualistic bacterium Vibrio fischeri . Previous research on the squid-vibrio symbiosis had shown that, upon colonization of deep epithelium-lined crypts of the host light organ, symbiont-derived peptidoglycan monomers induce apoptosis-mediated regression of remote epithelial fields involved in the inoculation process. In this study, immunofluorescence microscopy revealed that EsPGRP1 localizes to the nuclei of epithelial cells, and symbiont colonization induces the loss of EsPGRP1 from apoptotic nuclei. The loss of nuclear EsPGRP1 occurred prior to DNA cleavage and breakdown of the nuclear membrane, but followed chromatin condensation, suggesting that it occurs during late-stage apoptosis. Experiments with purified peptidoglycan monomers and with V. fischeri mutants defective in peptidoglycan-monomer release provided evidence that these molecules trigger nuclear loss of EsPGRP1 and apoptosis. The demonstration of a nuclear PGRP is unprecedented, and the dynamics of EsPGRP1 during apoptosis provide a striking example of a connection between microbial recognition and developmental responses in the establishment of symbiosis. |
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