Identification, molecular characterization, and gene expression analysis of a CD109 molecule in the Hawaiian bobtail squid Euprymna scolopes

Yazzie, Natasha; Salazar, Karla A.; Castillo, Maria G.

doi:10.1016/j.fsi.2015.02.036

Cited by 21 publications

(21 citation statements)

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“…Only BgTEP3 possesses a point mutation in the thioester site, changing the key cysteine into a serine residue ( Figure S3). In addition, N-and C-terminal transmembrane domains were also predicted for BgCD109 molecule, which is consistent with the predicted GPI-anchor site, as CD109 are known to be cell surface-membrane bound molecules [25,61].…”

Section: Bgtep Protein Features Analysissupporting

confidence: 70%

“…In mosquito, AgTEP1 was shown to be able to directly bind malaria parasite and to promote their elimination [21,22], while Aedes aegypti iTEP have been shown to regulate Flavivirus infection [23,24]. Finally, the Mollusca phylum has been seldom explored, CD109 molecule was characterized in the cephalopod Euprymna scolopes [25], two bivalve species were reported to contain A2M, iTEP, and C3-like complement factor [26][27][28], and more recently five TEP members belonging to C3-like complement factors, A2M, and CD109 classes have been identified in the gastropod Littorina littorea [29]. However, only few data are available concerning the functional role of such TEP proteins in mollusc phylum.…”

Section: Introductionmentioning

confidence: 99%

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A New Assessment of Thioester-Containing Proteins Diversity of the Freshwater Snail Biomphalaria glabrata

Duval

Pichon

Lassalle

et al. 2020

Genes

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Thioester-containing proteins (TEPs) superfamily is known to play important innate immune functions in a wide range of animal phyla. TEPs are involved in recognition, and in the direct or mediated killing of several invading organisms or pathogens. While several TEPs have been identified in many invertebrates, only one TEP (named BgTEP) has been previously characterized in the freshwater snail, Biomphalaria glabrata. As the presence of a single member of that family is particularly intriguing, transcriptomic data and the recently published genome were used to explore the presence of other BgTEP related genes in B. glabrata. Ten other TEP members have been reported and classified into different subfamilies: Three complement-like factors (BgC3-1 to BgC3-3), one α-2-macroblobulin (BgA2M), two macroglobulin complement-related proteins (BgMCR1, BgMCR2), one CD109 (BgCD109), and three insect TEP (BgTEP2 to BgTEP4) in addition to the previously characterized BgTEP that we renamed BgTEP1. This is the first report on such a level of TEP diversity and of the presence of macroglobulin complement-related proteins (MCR) in mollusks. Gene structure analysis revealed alternative splicing in the highly variable region of three members (BgA2M, BgCD109, and BgTEP2) with a particularly unexpected diversity for BgTEP2. Finally, different gene expression profiles tend to indicate specific functions for such novel family members.

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Section: Bgtep Protein Features Analysissupporting

confidence: 70%

Section: Introductionmentioning

confidence: 99%

A New Assessment of Thioester-Containing Proteins Diversity of the Freshwater Snail Biomphalaria glabrata

Duval

Pichon

Lassalle

et al. 2020

Genes

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“…This may be related to the primary sequence similarities between mollusk iTEPs, or may be due to a functional specificity. Among this mollusk subgroup, many proteins are predicted from automatic genome annotations, which means that they were not previously characterised, with the exception of clam TEP (Zhang et al, 2007) and bobtail squid CD109 (Yazzie et al, 2015). A unique sequence from this subgroup carries a predicted C-terminal transmembrane domain while most of them were automatically annotated as CD109 proteins.…”

Section: Discussionmentioning

confidence: 99%

“…TEPs seem to appear early in animal evolution: members of this family are present in a wide variety of invertebrate species: in arthropods (Levashina et al, 2001;Blandin and Levashina, 2004;Buresova et al, 2011;Sekiguchi et al, 2012;Urbanová et al, 2015); crustaceans (Wu et al, 2012;Li et al, 2017); cnidarians (Fujito et al, 2010) and mollusks (Zhang et al, 2007;Yazzie et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

BgTEP: an antiprotease involved in innate immune sensing in Biomphalaria glabrata

Portet

Galinier

Pinaud

et al. 2018

Preprint

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Insect Thioester-containing protein (iTEP) is the most recently defined group among the TEP superfamily. TEPs are key components of the immune system, and iTEPs from flies and mosquitoes were shown to be major immune weapons. Initially characterised from insects, TEP genes homologous to iTEP were further described from several other invertebrates including arthropods, cniderians and mollusks albeit with few functional characterisations. In the freshwater snail Biomphalaria glabrata, a vector of the schistosomiasis disease, the presence of a TEP protein (BgTEP) was previously described in a well-defined immune complex involving snail lectins (FREP) and schistosome parasite mucins (SmPoMuc).To investigate the potential role of BgTEP in the immune response of the snail, we first characterised its genomic organisation and its predicted protein structure. A phylogenetic analysis clustered BgTEP in a well-conserved subgroup of mollusk TEP. We then investigated the BgTEP expression profile in different snail tissues, and followed immune challenges using different kinds of intruders during infection kinetics. Results revealed that BgTEP is particularly expressed in hemocytes, the immune-specialised cells in invertebrates, and is secreted into the hemolymph. Transcriptomic results further evidenced an intruder-dependent differential expression pattern of BgTEP whilst interactome experiments showed that BgTEP is capable of binding to the surface of different microbes and parasite either in its full length form or in processed forms.Through this work, we report the first characterisation of a snail TEP. Our study also reveals that BgTEP may display an unexpected functional dual-role. In addition to its previously characterised anti-protease activity, we demonstrate that BgTEP can bind to the intruder surface membrane, which supports a likely opsonin role.

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“…In some systems they have been shown to influence phagocytosis and/or contribute to innate immune system specificity toward bacteria (Yu et al, 2007; Shi et al, 2014; Stowell et al, 2014). Members of the complement cascade in hemocytes and the light organ were also found to be differentially expressed depending on colonization state (Collins et al, 2012a; Schleicher et al, 2014; Yazzie et al, 2015). Combined, these “omics” data provide evidence that colonization by V. fischeri influences hemocyte gene expression and protein abundance.…”

Section: Light Organ Colonization Influences Hemocyte Gene Expressionmentioning

confidence: 99%

The Role of Hemocytes in the Hawaiian Bobtail Squid, Euprymna scolopes: A Model Organism for Studying Beneficial Host–Microbe Interactions

McAnulty

Nyholm

2017

Front. Microbiol.

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Most, if not all, animals engage in associations with bacterial symbionts. Understanding the mechanisms by which host immune systems and beneficial bacteria communicate is a fundamental question in the fields of immunology and symbiosis. The Hawaiian bobtail squid (Euprymna scolopes) engages in two known symbioses; a binary relationship with the light organ symbiont Vibrio fischeri, and a bacterial consortium within a specialized organ of the female reproductive system, the accessory nidamental gland (ANG). E. scolopes has a well-developed circulatory system that allows immune cells (hemocytes) to migrate into tissues, including the light organ and ANG. In the association with V. fischeri, hemocytes are thought to have a number of roles in the management of symbiosis, including the recognition of non-symbiotic bacteria and the contribution of chitin as a nutrient source for V. fischeri. Hemocytes are hypothesized to recognize bacteria through interactions between pattern recognition receptors and microbe-associated molecular patterns. Colonization by V. fischeri has been shown to affect the bacteria-binding behavior, gene expression, and proteome of hemocytes, indicating that the symbiont can modulate host immune function. In the ANG, hemocytes have also been observed interacting with the residing bacterial community. As a model host, E. scolopes offers a unique opportunity to study how the innate immune system interacts with both a binary and consortial symbiosis. This mini review will recapitulate what is known about the role of hemocytes in the light organ association and offer future directions for understanding how these immune cells interact with multiple types of symbioses.

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Identification, molecular characterization, and gene expression analysis of a CD109 molecule in the Hawaiian bobtail squid Euprymna scolopes

Cited by 21 publications

References 83 publications

A New Assessment of Thioester-Containing Proteins Diversity of the Freshwater Snail Biomphalaria glabrata

A New Assessment of Thioester-Containing Proteins Diversity of the Freshwater Snail Biomphalaria glabrata

BgTEP: an antiprotease involved in innate immune sensing in Biomphalaria glabrata

The Role of Hemocytes in the Hawaiian Bobtail Squid, Euprymna scolopes: A Model Organism for Studying Beneficial Host–Microbe Interactions

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