Highly Variable Immune-Response Proteins (185/333) from the Sea Urchin,<i>Strongylocentrotus purpuratus</i>: Proteomic Analysis Identifies Diversity within and between Individuals

Dheilly, Nolwenn M.; Nair, Sham V.; Smith, L. Courtney; Raftos, David A.

doi:10.4049/jimmunol.07012766

Cited by 51 publications

(142 citation statements)

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“…Integrin gene models are present in the sea urchin genome (Sodergren et al, 2006;Whittaker et al, 2006), and some integrins are expressed by the immune cells . The diversity of the Sp185/333 protein repertoire in coelomocytes results in patterns of bands or spots on one-and two-dimensional western blots that are not shared among individual sea urchins (Brockton et al, 2008;Dheilly et al, 2009). The number of Sp185/333-positive spots on two-dimensional western blots suggests that individual sea urchins may produce significantly more protein variants, which includes truncated and missense forms, than the estimated number of genes (Dheilly et al, 2009).…”

Section: Protein Diversitymentioning

confidence: 99%

“…The diversity of the Sp185/333 protein repertoire in coelomocytes results in patterns of bands or spots on one-and two-dimensional western blots that are not shared among individual sea urchins (Brockton et al, 2008;Dheilly et al, 2009). The number of Sp185/333-positive spots on two-dimensional western blots suggests that individual sea urchins may produce significantly more protein variants, which includes truncated and missense forms, than the estimated number of genes (Dheilly et al, 2009). The combination of Sp185/333 gene diversification (Buckley et al, 2008b) plus message editing (Buckley et al, 2008a) results in an extraordinarily diverse set of expressed proteins.…”

Section: Protein Diversitymentioning

confidence: 99%

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Diversification of innate immune genes: lessons from the purple sea urchin

Smith

2010

Disease Models &Amp; Mechanisms

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Pathogen diversification can alter infection virulence, which in turn drives the evolution of host immune diversification, resulting in countermeasures for survival in this arms race. Somatic recombination of the immunoglobulin gene family members is a very effective mechanism to diversify antibodies and T-cell receptors that function in the adaptive immune system. Although mechanisms to diversify innate immune genes are not clearly understood, a seemingly unlikely source for insight into innate immune diversification may be derived from the purple sea urchin, which has recently had its genome sequenced and annotated. Although there are many differences, some characteristics of the sea urchin make for a useful tool to understand the human immune system. The sea urchin is phylogenetically related to humans although, as a group, sea urchins are evolutionarily much older than mammals. Humans require both adaptive and innate immune responses to survive immune challenges, whereas sea urchins only require innate immune functions. Genes that function in immunity tend to be members of families, and the sea urchin has several innate immune gene families. One of these is the Sp185/333 gene family with about 50 clustered members that encode a diverse array of putative immune response proteins. Understanding gene diversification in the Sp185/333 family in the sea urchin may illuminate new mechanisms of diversification that could apply to gene families that function in innate immunity in humans, such as the killer immunoglobulin-like receptor genes.

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Section: Protein Diversitymentioning

confidence: 99%

Section: Protein Diversitymentioning

confidence: 99%

Diversification of innate immune genes: lessons from the purple sea urchin

Smith

2010

Disease Models &Amp; Mechanisms

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“…Although all but 1 of the 171 sequenced genes have perfect full-length open reading frames (15), half of the mRNAs encode truncated proteins due to single nucleotide polymorphisms and small (1-2 nt) indels that result in early stop codons or nonsense sequence leading to stop codons (20), which are likely the result of RNA editing (21). Overall, there appears to be multiple levels of immune diversification based on gene sequence diversity and RNA editing, in addition to putative posttranslational modifications and multimerization of the encoded proteins (22) with possible synergistic activities among the Sp185/333 proteins. The extraordinary diversity of the Sp185/333 system produces a very broad array of both full-length and truncated Sp185/333 proteins in response to immune challenge (22,23).…”

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confidence: 99%

“…Overall, there appears to be multiple levels of immune diversification based on gene sequence diversity and RNA editing, in addition to putative posttranslational modifications and multimerization of the encoded proteins (22) with possible synergistic activities among the Sp185/333 proteins. The extraordinary diversity of the Sp185/333 system produces a very broad array of both full-length and truncated Sp185/333 proteins in response to immune challenge (22,23).…”

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confidence: 99%

Single Sea Urchin Phagocytes Express Messages of a Single Sequence from the DiverseSp185/333Gene Family in Response to Bacterial Challenge

Majeske

Oren

Sacchi

et al. 2014

The Journal of Immunology

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Immune systems in animals rely on fast and efficient responses to a wide variety of pathogens. The Sp185/333 gene family in the purple sea urchin, Strongylocentrotus purpuratus, consists of an estimated 50 (±10) members per genome that share a basic gene structure but show high sequence diversity, primarily due to the mosaic appearance of short blocks of sequence called elements. The genes show significantly elevated expression in three subpopulations of phagocytes responding to marine bacteria. The encoded Sp185/333 proteins are highly diverse and have central effector functions in the immune system. In this study we report the Sp185/333 gene expression in single sea urchin phagocytes. Sea urchins challenged with heat-killed marine bacteria resulted in a typical increase in coelomocyte concentration within 24 h, which included an increased proportion of phagocytes expressing Sp185/333 proteins. Phagocyte fractions enriched from coelomocytes were used in limiting dilutions to obtain samples of single cells that were evaluated for Sp185/333 gene expression by nested RT-PCR. Amplicon sequences showed identical or nearly identical Sp185/333 amplicon sequences in single phagocytes with matches to six known Sp185/333 element patterns, including both common and rare element patterns. This suggested that single phagocytes show restricted expression from the Sp185/333 gene family and infers a diverse, flexible, and efficient response to pathogens. This type of expression pattern from a family of immune response genes in single cells has not been identified previously in other invertebrates.

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“…In response to challenge with various pathogen-associated molecular patterns (PAMPs) and sham-injected injury controls that received artificial coelomic fluid, there is a change in the dominant element patterns of the messages and an increase in the number of minor patterns (28). Furthermore, different suites of 185/333 proteins have been observed by two-dimensional electrophoresis following challenge with LPS vs peptidoglycan (50). These data suggest that the sea urchin may be able to discriminate among different PAMPs by modulating the specific 185/333 genes expressed, although the mechanisms are unknown.…”

mentioning

confidence: 99%

Sequence Variations in 185/333 Messages from the Purple Sea Urchin Suggest Posttranscriptional Modifications to Increase Immune Diversity

Buckley

Terwilliger

Smith

2008

The Journal of Immunology

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The 185/333 gene family is highly expressed in two subsets of immune cells in the purple sea urchin in response to immune challenges. The genes encode a surprisingly diverse set of transcripts, which is a function of the variable presence or absence of blocks of shared sequences, known as elements that generate element patterns. Diversity is also the result of a significant level of point mutations. Together, variable element patterns and single nucleotide polymorphisms result in many unique transcripts. The 185/333 genes only have two exons, with the variable element patterns encoded entirely within the second exon. The diversity of the gene family may be the result of frequent recombination among the 185/333 genes that generates a mosaic distribution of element sequences among the genes. A comparative analysis of the sequences for the genes and messages from individual sea urchins indicates that these two sequence sets have largely different nucleotide sequences and appear to use different element patterns. Furthermore, the nucleotide substitution patterns between genes and messages reveal a strong bias toward transitions, particularly cytidine to uridine conversions. These data are consistent with cytidine deaminase activity and may represent a novel form of immunological diversification in an invertebrate immune response system.

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Highly Variable Immune-Response Proteins (185/333) from the Sea Urchin,Strongylocentrotus purpuratus: Proteomic Analysis Identifies Diversity within and between Individuals

Cited by 51 publications

References 43 publications

Diversification of innate immune genes: lessons from the purple sea urchin

Diversification of innate immune genes: lessons from the purple sea urchin

Single Sea Urchin Phagocytes Express Messages of a Single Sequence from the DiverseSp185/333Gene Family in Response to Bacterial Challenge

Sequence Variations in 185/333 Messages from the Purple Sea Urchin Suggest Posttranscriptional Modifications to Increase Immune Diversity

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