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Peptidoglycan
induces loss of a nuclear peptidoglycan recognition protein during host
tissue development in a beneficial animal-bacterial symbiosis.
Troll J. V., Adin D. M., Wier A. M., Paquette N.,
Silverman N., Goldman W. E., Stadermann F. J., Stabb E. V., and
McFall-Ngai M. J. (2009)
Cellular Microbiology, 11(7), 1114-1127.
doi: 10.1111/j.1462-5822.2009.01315.x
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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