Use of OmpU porins for attachment and invasion of Crassostrea gigas immune cells by the oyster pathogen Vibrio splendidus

Type Article
Date 2011-02
Language English
Author(s) Duperthuy Marylise1, 2, 3, 4, Schmitt Paulina1, 2, 3, 4, Garzon Edwin5, Caro Audrey1, 2, 3, 4, Rosa Rafael D.1, 2, 3, 4, Le Roux Frederique6, 7, Lautredou-Audouy Nicole8, 9, Got Patrice1, 2, 3, 4, Romestand Bernard1, 2, 3, 4, de Lorgeril JulienORCID1, 2, 3, 4, Kieffer-Jaquinod Sylvie10, Bachere Evelyne1, 2, 3, 4, Destoumieux-Garzon Delphine1, 2, 3, 4
Affiliation(s) 1 : Inst Francais Rech Exploitat Mer, F-34095 Montpellier, France.
2 : Ctr Natl Rech Sci, F-34095 Montpellier, France.
3 : Univ Montpellier 2, F-34095 Montpellier, France.
4 : Inst Rech Dev, Lab Ecosyst Lagunaires, Unite Mixte Rech 5119, F-34095 Montpellier, France.
5 : Ctr Cooperat Int Rech Agron Dev, Inst Rech Dev, Unite Mixte Rech 177, F-34094 Montpellier, France.
6 : CNRS, Biol Stn, F-29682 Roscoff, France.
7 : Inst Francais Rech Exploitat Mer, Lab Physiol Invertebres, F-29280 Brest, France.
8 : Ctr Natl Rech Sci, F-34090 Montpellier, France.
9 : Ctr Biochim Struct, Inst Natl Sante & Rech Med U554, Unite Mixte Rech 5048, F-34090 Montpellier, France.
10 : Univ Grenoble 1, Inst Natl Sante & Rech Med U880, Inst Rech Technol & Sci Vivant,Lab Etud Dynam Pro, Comm Energie Atom,Direct Sci Vivant, F-38054 Grenoble, France.
Source Proceedings Of The National Academy Of Sciences Of The United States Of America (0027-8424) (Natl Acad Sciences), 2011-02 , Vol. 108 , N. 7 , P. 2993-2998
DOI 10.1073/pnas.1015326108
WOS© Times Cited 117
Keyword(s) host-pathogen interaction, innate immunity, invertebrate, mollusk, oxidative burst
Abstract OmpU porins are increasingly recognized as key determinants of pathogenic host Vibrio interactions. Although mechanisms remain incompletely understood, various species, including the human pathogen Vibrio cholera, require OmpU for host colonization and virulence. We have shown previously that OmpU is essential for virulence in the oyster pathogen Vibrio splendidus LGP32. Here, we showed that V. splendidus LGP32 invades the oyster immune cells, the hemocytes, through subversion of host-cell actin cytoskeleton. In this process, OmpU serves as an adhesin/invasin required for beta-integrin recognition and host cell invasion. Furthermore, the major protein of oyster plasma, the extracellular superoxide dismutase Cg-EcSOD, is used as an opsonin mediating the OmpU-promoted phagocytosis through its RGD sequence. Finally, the endocytosed bacteria were found to survive intracellularly, evading the host defense by preventing acidic vacuole formation and limiting reactive oxygen species production. We conclude that (i) V. splendidus is a facultative intracellular pathogen that manipulates host defense mechanisms to enter and survive in host immune cells, and (ii) that OmpU is a major determinant of host cell invasion in Vibrio species, used by V. splendidus LGP32 to attach and invade oyster hemocytes through opsonisation by the oyster plasma Cg-EcSOD.
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Duperthuy Marylise, Schmitt Paulina, Garzon Edwin, Caro Audrey, Rosa Rafael D., Le Roux Frederique, Lautredou-Audouy Nicole, Got Patrice, Romestand Bernard, de Lorgeril Julien, Kieffer-Jaquinod Sylvie, Bachere Evelyne, Destoumieux-Garzon Delphine (2011). Use of OmpU porins for attachment and invasion of Crassostrea gigas immune cells by the oyster pathogen Vibrio splendidus. Proceedings Of The National Academy Of Sciences Of The United States Of America, 108(7), 2993-2998. Publisher's official version : https://doi.org/10.1073/pnas.1015326108 , Open Access version : https://archimer.ifremer.fr/doc/00031/14177/