Journal of Biological Chemistry
Volume 289, Issue 17, 25 April 2014, Pages 11779-11790
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Immunology
A Shrimp C-type Lectin Inhibits Proliferation of the Hemolymph Microbiota by Maintaining the Expression of Antimicrobial Peptides*

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Some aquatic invertebrates such as shrimp contain low albeit stable numbers of bacteria in the circulating hemolymph. The proliferation of this hemolymph microbiota in such a nutrient-rich environment is tightly controlled in healthy animals, but the mechanisms responsible had remained elusive. In the present study, we report a C-type lectin (MjHeCL) from the kuruma shrimp (Marsupenaeus japonicus) that participates in restraining the hemolymph microbiota. Although the expression of MjHeCL did not seem to be modulated by bacterial challenge, the down-regulation of its expression by RNA interference led to proliferation of the hemolymph microbiota, ultimately resulting in shrimp death. This phenotype was rescued by the injection of recombinant MjHeCL, which restored the healthy status of the knockdown shrimp. A mechanistic analysis revealed that MjHeCL inhibited bacterial proliferation by modulating the expression of antimicrobial peptides. The key function of MjHeCL in the shrimp immune homeostasis might be related to its broader recognition spectrum of the hemolymph microbiota components than other lectins. Our study demonstrates the role of MjHeCL in maintaining the healthy status of shrimp and provides new insight into the biological significance of C-type lectins, a diversified and abundant lectin family in invertebrate species.

Antimicrobial Peptides
Invertebrates
Lectin
Pattern Recognition Receptor
RNA Interference (RNAi)
C-type Lectin
Hemolymph Microbiota
Shrimp

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This work was supported by the National Natural Science Foundation of China (Grants 31130056 and 31302217), the Provincial Natural Science Foundation of Shandong, China (Grant ZR2011CM014), the Ph.D. Program Foundation of the Ministry of Education of China (Grant 20110131130003), and the China Postdoctoral Science Foundation (Grant 2013M540553) (to J.-X. W. and X.-W. W.) and by National Science Foundation Grants IOS-1050518, IOB-0618409, and IOS-0822257 (to G. R. V.). This work was supported, in whole or in part, by National Institutes of Health Grant 5R01GM070589-06 (to G. R. V.).

The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EBI Data Bank with accession number(s) KJ175168.

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X.-W. Wang, J.-D. Xu, X.-F. Zhao, G. R. Vasta, and J.-X. Wang, unpublished data.