Molecular Evolution and Functionally Important Structures of Molluscan Dermatopontin: Implications for the Origins of Molluscan Shell Matrix Proteins

Sarashina, Isao; Yamaguchi, Haruyo; Haga, Takuma; Iijima, Mayumi; Chiba, Satoshi; Endo, Kazuhiko

doi:10.1007/s00239-005-0095-2

Cited by 41 publications

(33 citation statements)

References 47 publications

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“…Dermatopontin was also reported from the shells of other gastropods [42], and bivalves, where it is thought to play a role in nacre formation [43], and can also be found in taxa ranging from bacteria to humans. Interestingly, we did not detect Dermatopontin in the shell of C. nemoralis .…”

Section: Resultsmentioning

confidence: 99%

Characterization of the pigmented shell-forming proteome of the common grove snail Cepaea nemoralis

2014

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BackgroundWith a diversity of pigmented shell morphotypes governed by Mendelian patterns of inheritance, the common grove snail, Cepaea nemoralis, has served as a model for evolutionary biologists and population geneticists for decades. Surprisingly, the molecular mechanisms by which C. nemoralis generates this pigmented shelled diversity, and the degree of evolutionary conservation present between molluscan shell-forming proteomes, remain unknown.ResultsHere, using next generation sequencing and high throughput proteomics, we identify and characterize the major proteinaceous components of the C. nemoralis shell, the first shell-proteome for a pulmonate mollusc. The recent availability of several marine molluscan shell-proteomes, and the dataset we report here, allow us to identify 59 evolutionarily conserved and novel shell-forming proteins. While the C. nemoralis dataset is dominated by proteins that share little to no similarity with proteins in public databases, almost half of it shares similarity with proteins present in other molluscan shells. In addition, we could not find any indication that a protein (or class of proteins) is directly associated with shell pigmentation in C. nemoralis. This is in contrast to the only other partially characterized molluscan-shell pigmentation mechanism employed by the tropical abalone Haliotis asinina.ConclusionsThe unique pulmonate shell-forming proteome that we report here reveals an abundance of both mollusc-specific and pulmonate-specific proteins, suggesting that novel coding sequences, and/or the extensive divergence of these sequences from ancestral sequences, supported the innovation of new shell types within the Conchifera. In addition, we report here the first evidence that molluscs use independently evolved mechanisms to pigment their shells. This proteome provides a solid foundation from which further studies aimed at the functional characterization of these shell-forming proteins can be conducted.

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Section: Resultsmentioning

confidence: 99%

Characterization of the pigmented shell-forming proteome of the common grove snail Cepaea nemoralis

2014

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“…Since then several molluscan dermatopontin-encoding genes have been identified and some of them were transcribed in mantle cells, implying the shell matrix as final destination [17,54,55]. A protein very similar to dermatopontin, Lotgi1|133595 (Figure 7), was identified at moderate abundance in the acid-insoluble matrix consensus proteome and in the soluble fraction of A and C ( Additional file 1 and Additional file 2).…”

Section: Resultsmentioning

confidence: 99%

“…A protein very similar to dermatopontin, Lotgi1|133595 (Figure 7), was identified at moderate abundance in the acid-insoluble matrix consensus proteome and in the soluble fraction of A and C ( Additional file 1 and Additional file 2). The function of this protein remains unknown at present [55]. …”

Section: Resultsmentioning

confidence: 99%

In-depth proteomic analysis of a mollusc shell: acid-soluble and acid-insoluble matrix of the limpet Lottia gigantea

2012

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BackgroundInvertebrate biominerals are characterized by their extraordinary functionality and physical properties, such as strength, stiffness and toughness that by far exceed those of the pure mineral component of such composites. This is attributed to the organic matrix, secreted by specialized cells, which pervades and envelops the mineral crystals. Despite the obvious importance of the protein fraction of the organic matrix, only few in-depth proteomic studies have been performed due to the lack of comprehensive protein sequence databases. The recent public release of the gastropod Lottia gigantea genome sequence and the associated protein sequence database provides for the first time the opportunity to do a state-of-the-art proteomic in-depth analysis of the organic matrix of a mollusc shell.ResultsUsing three different sodium hypochlorite washing protocols before shell demineralization, a total of 569 proteins were identified in Lottia gigantea shell matrix. Of these, 311 were assembled in a consensus proteome comprising identifications contained in all proteomes irrespective of shell cleaning procedure. Some of these proteins were similar in amino acid sequence, amino acid composition, or domain structure to proteins identified previously in different bivalve or gastropod shells, such as BMSP, dermatopontin, nacrein, perlustrin, perlucin, or Pif. In addition there were dozens of previously uncharacterized proteins, many containing repeated short linear motifs or homorepeats. Such proteins may play a role in shell matrix construction or control of mineralization processes.ConclusionsThe organic matrix of Lottia gigantea shells is a complex mixture of proteins comprising possible homologs of some previously characterized mollusc shell proteins, but also many novel proteins with a possible function in biomineralization as framework building blocks or as regulatory components. We hope that this data set, the most comprehensive available at present, will provide a platform for the further exploration of biomineralization processes in molluscs.

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“…Cadherin is involved in cell adhesion [87], and legumain is a cysteine protease associated with response to bacteria [88], antigen processing [89], and ECM remodeling [90] in mammals. Transcripts annotating as dermatopontin-2, a shell matrix protein involved in cell adhesion and shell formation [91], [92] may be involved in bacterial encapsulation and conchiolin production (a hallmark clinical sign of ROD). Dermatopontin is strongly induced in amphioxus following bacterial challenge by gram-positive and gram-negative bacteria [93].…”

Section: Discussionmentioning

confidence: 99%

Transcriptome of American Oysters, Crassostrea virginica, in Response to Bacterial Challenge: Insights into Potential Mechanisms of Disease Resistance

et al. 2014

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The American oyster Crassostrea virginica, an ecologically and economically important estuarine organism, can suffer high mortalities in areas in the Northeast United States due to Roseovarius Oyster Disease (ROD), caused by the gram-negative bacterial pathogen Roseovarius crassostreae. The goals of this research were to provide insights into: 1) the responses of American oysters to R. crassostreae, and 2) potential mechanisms of resistance or susceptibility to ROD. The responses of oysters to bacterial challenge were characterized by exposing oysters from ROD-resistant and susceptible families to R. crassostreae, followed by high-throughput sequencing of cDNA samples from various timepoints after disease challenge. Sequence data was assembled into a reference transcriptome and analyzed through differential gene expression and functional enrichment to uncover genes and processes potentially involved in responses to ROD in the American oyster. While susceptible oysters experienced constant levels of mortality when challenged with R. crassostreae, resistant oysters showed levels of mortality similar to non-challenged oysters. Oysters exposed to R. crassostreae showed differential expression of transcripts involved in immune recognition, signaling, protease inhibition, detoxification, and apoptosis. Transcripts involved in metabolism were enriched in susceptible oysters, suggesting that bacterial infection places a large metabolic demand on these oysters. Transcripts differentially expressed in resistant oysters in response to infection included the immune modulators IL-17 and arginase, as well as several genes involved in extracellular matrix remodeling. The identification of potential genes and processes responsible for defense against R. crassostreae in the American oyster provides insights into potential mechanisms of disease resistance.

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Molecular Evolution and Functionally Important Structures of Molluscan Dermatopontin: Implications for the Origins of Molluscan Shell Matrix Proteins

Cited by 41 publications

References 47 publications

Characterization of the pigmented shell-forming proteome of the common grove snail Cepaea nemoralis

Characterization of the pigmented shell-forming proteome of the common grove snail Cepaea nemoralis

In-depth proteomic analysis of a mollusc shell: acid-soluble and acid-insoluble matrix of the limpet Lottia gigantea

Transcriptome of American Oysters, Crassostrea virginica, in Response to Bacterial Challenge: Insights into Potential Mechanisms of Disease Resistance

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