Characterization of immune genes from the schistosome host snail Biomphalaria glabrata that encode peptidoglycan recognition proteins and gram-negative bacteria binding protein

Zhang, Si-Ming; Zeng, Yong; Loker, Eric S.

doi:10.1007/s00251-007-0245-3

Cited by 62 publications

(46 citation statements)

References 66 publications

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“…For Southern blotting, genomic DNA was extracted from an M line snail, which was inbred for 20-generations [31], using CTAB method [32]. The concentration and purity of total RNA and genomic DNA were determined spectrophotometrically.…”

Section: Extraction Of Total Rna and Genomic Dnamentioning

confidence: 99%

Fibrinogen-bearing protein genes in the snail Biomphalaria glabrata: Characterization of two novel genes and expression studies during ontogenesis and trematode infection

Zhang

Nian

Zeng

et al. 2008

Developmental & Comparative Immunology

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All fibrinogen (FBG)-bearing proteins documented to date in the freshwater snail Biomphalaria glabrata, the intermediate host of the human blood fluke Schistosoma mansoni, possess the same molecular structure; one or two immunoglobin superfamily (IgSF) domains at the N-terminus and a FBG domain at the C-terminus (named as FBG-related protein (FREP)). Here we report two novel genes that encode FBG-bearing proteins from B. glabrata. Different from all known FREPs, the first gene encodes a protein (657 amino acids (aa)) composed of a long N-terminal region with no sequence homology to any known protein, a middle epidermal growth factor (EGF) repeat region and a Cterminal FBG domain, designated FBG-related molecule (FReM). A differential expression at 2 days post exposure (dpe) to the trematode S. mansoni or Echinostoma paraensei has been found in the S. mansoni susceptible M line and resistant BS-90 snail strains. The second gene is a new member of the FREP family, designated FREP14, which encodes a 399 aa putative secreted protein. FREP14 is different from known FREPs in that it is encoded by a single locus and is not upregulated in early or late stage S. mansoni exposure, but is upregulated in late stage E. paraensei infection. Furthermore, gene expression during the snail's ontogenesis and at a late stage of trematode-infection (52 dpe) has been investigated in the two newly-identified genes (FReM and FREP14) described in this paper and five representative members of known FREPs (FREPs 2,3,4,12,and 13). A variety of expression patterns were observed, suggestive of functional diversity among the members of FBG-bearing proteins. Our findings further broaden our understanding of the diversity and function of the FBGbearing protein encoded genes in B. glabrata.

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Section: Extraction Of Total Rna and Genomic Dnamentioning

confidence: 99%

Fibrinogen-bearing protein genes in the snail Biomphalaria glabrata: Characterization of two novel genes and expression studies during ontogenesis and trematode infection

Zhang

Nian

Zeng

et al. 2008

Developmental & Comparative Immunology

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“…GNBPs can be divided into two groups. Group A is restricted to Drosophila and has lost the key residues for glucanase activity (44), whereas group B is present in various invertebrates and has predicted glucanase activity. Notably, Drosophila GNBP1 and GNBP3 act as sensor PRRs and work with PGRPs in the Toll pathway (9).…”

Section: Gnbpsmentioning

confidence: 99%

The Evolution and Regulation of the Mucosal Immune Complexity in the Basal Chordate Amphioxus

Huang

Wang

Yan

et al. 2011

The Journal of Immunology

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Both amphioxus and the sea urchin encode a complex innate immune gene repertoire in their genomes, but the composition and mechanisms of their innate immune systems, as well as the fundamental differences between two systems, remain largely unexplored. In this study, we dissect the mucosal immune complexity of amphioxus into different evolutionary-functional modes and regulatory patterns by integrating information from phylogenetic inferences, genome-wide digital expression profiles, time course expression dynamics, and functional analyses. With these rich data, we reconstruct several major immune subsystems in amphioxus and analyze their regulation during mucosal infection. These include the TNF/IL-1R network, TLR and NLR networks, complement system, apoptosis network, oxidative pathways, and other effector genes (e.g., peptidoglycan recognition proteins, Gram-negative binding proteins, and chitin-binding proteins). We show that beneath the superficial similarity to that of the sea urchin, the amphioxus innate system, despite preserving critical invertebrate components, is more similar to that of the vertebrates in terms of composition, expression regulation, and functional strategies. For example, major effectors in amphioxus gut mucous tissue are the well-developed complement and oxidative-burst systems, and the signaling network in amphioxus seems to emphasize signal transduction/modulation more than initiation. In conclusion, we suggest that the innate immune systems of amphioxus and the sea urchin are strategically different, possibly representing two successful cases among many expanded immune systems that arose at the age of the Cambrian explosion. We further suggest that the vertebrate innate immune system should be derived from one of these expanded systems, most likely from the same one that was shared by amphioxus.

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“…The Drosophila PGRP-LB has a catalytic amidase activity that can degrade PGN and prevent host immune activation (16,17). The ability of PGRP-LB to control host immune activation provides protection to beneficial microbes in several insects (18)(19)(20). In tsetse, pgrp-lb is expressed in Wigglesworthia harboring tissues (bacteriome and milk gland), and there is a positive correlation between Wigglesworthia density and pgrp-lb expression levels.…”

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confidence: 99%

PGRP-LB is a maternally transmitted immune milk protein that influences symbiosis and parasitism in tsetse’s offspring

Wang

Aksoy

2012

Proc. Natl. Acad. Sci. U.S.A.

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Beneficial microbe functions range from host dietary supplementation to development and maintenance of host immune system. In mammals, newborn progeny are quickly colonized with a symbiotic fauna that is provisioned in mother's milk and that closely resembles that of the parent. Tsetse fly (Diptera: Glossinidae) also depends on the obligate symbiont Wigglesworthia for nutritional supplementation, optimal fecundity, and immune system development. Tsetse progeny develop one at a time in an intrauterine environment and receive nourishment and symbionts in mother's milk. We show that the host Peptidoglycan Recognition Protein (PGRP-LB) is expressed only in adults and is a major component of the milk that nourishes the developing progeny. The amidase activity associated with PGRP-LB may scavenge the symbiotic peptidoglycan and prevent the induction of tsetse's Immune Deficiency pathway that otherwise can damage the symbionts. Reduction of PGRP-LB experimentally diminishes female fecundity and damages Wigglesworthia in the milk through induction of antimicrobial peptides, including Attacin. Larvae that receive less maternal PGRP-LB give rise to adults with fewer Wigglesworthia and hyperimmune responses. Such adults also suffer dysregulated immunity, as indicated by the presence of higher trypanosome densities in parasitized adults. We show that recPGRP-LB has antimicrobial and antitrypanosomal activities that may regulate symbiosis and impact immunity. Thus, PGRP-LB plays a pivotal role in tsetse's fitness by protecting symbiosis against host-inflicted damage during development and by controlling parasite infections in adults that can otherwise reduce host fecundity. maternal transfer | transgenerational immune effects | antimicrobial activity | antitrypanosomal activity

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Characterization of immune genes from the schistosome host snail Biomphalaria glabrata that encode peptidoglycan recognition proteins and gram-negative bacteria binding protein

Cited by 62 publications

References 66 publications

Fibrinogen-bearing protein genes in the snail Biomphalaria glabrata: Characterization of two novel genes and expression studies during ontogenesis and trematode infection

Fibrinogen-bearing protein genes in the snail Biomphalaria glabrata: Characterization of two novel genes and expression studies during ontogenesis and trematode infection

The Evolution and Regulation of the Mucosal Immune Complexity in the Basal Chordate Amphioxus

PGRP-LB is a maternally transmitted immune milk protein that influences symbiosis and parasitism in tsetse’s offspring

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