A model symbiosis reveals a role for sheathed-flagellum rotation in the release of immunogenic lipopolysaccharide

被引:42
作者
Brennan, Caitlin A. [1 ]
Hunt, Jason R. [2 ,3 ]
Kremer, Natacha [1 ]
Krasity, Benjamin C. [1 ]
Apicella, Michael A. [2 ,3 ]
McFall-Ngai, Margaret J. [1 ]
Ruby, Edward G. [1 ]
机构
[1] Univ Wisconsin, Dept Med Microbiol & Immunol, Madison, WI 53706 USA
[2] Univ Iowa, Carver Coll Med, Dept Microbiol, Iowa City, IA USA
[3] Univ Iowa, Carver Coll Med, Dept Internal Med, Iowa City, IA USA
基金
美国国家卫生研究院;
关键词
VIBRIO-FISCHERI; LIGHT-ORGAN; ESCHERICHIA-COLI; HELICOBACTER-PYLORI; MOTILITY; CHOLERAE; COLONIZATION; APOPTOSIS; MORPHOGENESIS; ACTIVATION;
D O I
10.7554/eLife.01579
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Bacterial flagella mediate host-microbe interactions through tissue tropism during colonization, as well as by activating immune responses. The flagellar shaft of some bacteria, including several human pathogens, is encased in a membranous sheath of unknown function. While it has been hypothesized that the sheath may allow these bacteria to evade host responses to the immunogenic flagellin subunit, this unusual structural feature has remained an enigma. Here we demonstrate that the rotation of the sheathed flagellum in both the mutualist Vibrio fischeri and the pathogen Vibrio cholerae promotes release of a potent bacteria-derived immunogen, lipopolysaccharide, found in the flagellar sheath. We further present a new role for the flagellar sheath in triggering, rather than circumventing, host immune responses in the model squid-vibrio symbiosis. Such an observation not only has implications for the study of bacterial pathogens with sheathed flagella, but also raises important biophysical questions of sheathed-flagellum function.
引用
收藏
页数:11
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共 43 条
[1]   Cutting edge:: Tlr5-/- mice are more susceptible to Escherichia coli urinary tract infection [J].
Andersen-Nissen, Erica ;
Hawn, Thomas R. ;
Smith, Kelly D. ;
Nachman, Alex ;
Lampano, Aaron E. ;
Uematsu, Satoshi ;
Akira, Shizuo ;
Aderem, Alan .
JOURNAL OF IMMUNOLOGY, 2007, 178 (08) :4717-4720
[2]   DEPRESSED LIGHT-EMISSION BY SYMBIOTIC VIBRIO-FISCHERI OF THE SEPIOLID SQUID EUPRYMNA-SCOLOPES [J].
BOETTCHER, KJ ;
RUBY, EG .
JOURNAL OF BACTERIOLOGY, 1990, 172 (07) :3701-3706
[3]   Genetic determinants of swimming motility in the squid light-organ symbiont Vibrio fischeri [J].
Brennan, Caitlin A. ;
Mandel, Mark J. ;
Gyllborg, Mattias C. ;
Thomasgard, Krista A. ;
Ruby, Edward G. .
MICROBIOLOGYOPEN, 2013, 2 (04) :576-594
[4]   Structural diversity of bacterial flagellar motors [J].
Chen, Songye ;
Beeby, Morgan ;
Murphy, Gavin E. ;
Leadbetter, Jared R. ;
Hendrixson, David R. ;
Briegel, Ariane ;
Li, Zhuo ;
Shi, Jian ;
Tocheva, Elitza I. ;
Mueller, Axel ;
Dobro, Megan J. ;
Jensen, Grant J. .
EMBO JOURNAL, 2011, 30 (14) :2972-2981
[5]   Lipopolysaccharide mediates endothelial apoptosis by a FADD-dependent pathway [J].
Choi, KB ;
Wong, F ;
Harlan, JM ;
Chaudhary, PM ;
Hood, L ;
Karsan, A .
JOURNAL OF BIOLOGICAL CHEMISTRY, 1998, 273 (32) :20185-20188
[6]   IMPOSSIBILITY OF ACRIDINE-ORANGE INTERCALATION IN NUCLEAR-DNA OF THE LIVING CELL [J].
DELIC, J ;
COPPEY, J ;
MAGDELENAT, H ;
COPPEYMOISAN, M .
EXPERIMENTAL CELL RESEARCH, 1991, 194 (01) :147-153
[7]   New rfp- and pES213-derived tools for analyzing symbiotic Vibrio fischeri reveal patterns of infection and lux expression in situ [J].
Dunn, AK ;
Millikan, DS ;
Adin, DM ;
Bose, JL ;
Stabb, EV .
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2006, 72 (01) :802-810
[8]   Morphological analysis of the sheathed flagellum of Brucella melitensis [J].
Ferooz J. ;
Letesson J.-J. .
BMC Research Notes, 3 (1)
[9]   Involvement of Toll-like receptor 5 in the recognition of flagellated bacteria [J].
Feuillet, Vincent ;
Medjane, Samir ;
Mondor, Isabelle ;
Demaria, Olivier ;
Pagni, Philippe P. ;
Galan, Jorge E. ;
Flavell, Richard A. ;
Alexopoulou, Lena .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2006, 103 (33) :12487-12492
[10]   Vibrio fischeri lipopolysaccharide induces developmental apoptosis, but not complete morphogenesis, of the Euprymna scolopes symbiotic light organ [J].
Foster, JS ;
Apicella, MA ;
McFall-Ngai, MJ .
DEVELOPMENTAL BIOLOGY, 2000, 226 (02) :242-254