Genes “Waiting” for Recruitment by the Adaptive Immune System: The Insights from Amphioxus

Yu, Cuiling; Dong, Meiling; Wu, Xiaokun; Li, Shengguo; Huang, Shengfeng; Su, Jing; Wei, Jianwen; Shen, Yang; Mou, Chunyan; Xie, Xiaojin; Lin, Jianghai; Yuan, Shaochun; Yu, Xuesong; Yu, Ye; Du, Jingchun; Zhang, Shicui; Peng, Xuan‐xian; Xiang, Mengqing; Xu, Anlong

doi:10.4049/jimmunol.174.6.3493

Cited by 57 publications

(39 citation statements)

References 59 publications

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“…Immunocytes (coelomocytes) of amphioxus were first discovered in the gut region 25 yr ago (Rhodes et al 1982). Our studies have further confirmed that gill and gut represent the major immune region in amphioxus Yu et al 2005Yu et al , 2007bHuang et al 2007a,b;Yuan et al 2007). Unfortunately, since the year 1982, only a few studies address the amphioxus immunity.…”

supporting

confidence: 75%

Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity

Huang¹,

Yuan²,

Guo³

et al. 2008

Genome Res.

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348

284

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It has been speculated that before vertebrates evolved somatic diversity-based adaptive immunity, the germline-encoded diversity of innate immunity may have been more developed. Amphioxus occupies the basal position of the chordate phylum and hence is an important reference to the evolution of vertebrate immunity. Here we report the first comprehensive genomic survey of the immune gene repertoire of the amphioxus Branchiostoma floridae. It has been reported that the purple sea urchin has a vastly expanded innate receptor repertoire not previously seen in other species, which includes 222 toll-like receptors (TLRs), 203 NOD/NALP-like receptors (NLRs), and 218 scavenger receptors (SRs). We discovered that the amphioxus genome contains comparable expansion with 71 TLR gene models, 118 NLR models, and 270 SR models. Amphioxus also expands other receptor-like families, including 1215 C-type lectin models, 240 LRR and IGcam-containing models, 1363 other LRR-containing models, 75 C1q-like models, 98 ficolin-like models, and hundreds of models containing complement-related domains. The expansion is not restricted to receptors but is likely to extend to intermediate signal transducers because there are 58 TIR adapter-like models, 36 TRAF models, 44 initiator caspase models, and 541 death-fold domain-containing models in the genome. Amphioxus also has a sophisticated TNF system and a complicated complement system not previously seen in other invertebrates. Besides the increase of gene number, domain combinations of immune proteins are also increased. Altogether, this survey suggests that the amphioxus, a species without vertebrate-type adaptive immunity, holds extraordinary innate complexity and diversity.

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supporting

confidence: 75%

Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity

Huang¹,

Yuan²,

Guo³

et al. 2008

Genome Res.

Self Cite

348

284

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“…The earliest forms of secondary lymphoid tissue were diffuse aggregations and infiltrations in the intestinal wall [60].The implication is that many of the functions which we associate with organised lymphoid tissues in mammals (collections of B-cell follicles and associated T-cell zones) originally took place in more diffuse aggregations of leucocytes in mucosal tissues. Consistent with this idea, immunologically-related genes appear to be expressed preferentially in the intestine in the protochordate amphioxus and in the jawless lampreys [50,59]. Since mucosal tissues are permanently exposed to both harmless as well as harmful antigens, mechanisms must exist which activate appropriate, but different responses to different types of antigens.…”

Section: Structure Of the Mucosal Immune Systemmentioning

confidence: 87%

The postnatal development of the mucosal immune system and mucosal tolerance in domestic animals

Bailey

Haverson²

2006

Vet. Res.

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-The mucosal immune system is exposed to a range of antigens associated with pathogens, to which it must mount active immune responses. However, it is also exposed to a large number of harmless antigens associated with food and with commensal microbial flora, to which expression of active, inflammatory immune responses to these antigens is undesirable. The mucosal immune system must contain machinery capable of evaluating the antigens to which it is exposed and mounting appropriate effector or regulatory responses. Since the immune system is likely to have evolved initially in mucosal tissues, the requirement to prevent damaging allergic responses must be at least as old as the adaptive immune system, and studies of the mechanisms should include a range of non-mammalian species. Despite the importance for rational design of vaccines and for control of allergic reactions, the mechanisms involved are still largely unclear. It is not clear that the classical experimental protocol of "oral tolerance" is, in fact, measuring a biologically important phenomenon, nor is it clear whether tolerance is regulated in the evolutionarily recent organised lymphoid tissue (the lymph nodes) or the more ancient, diffuse architecture in the intestine. The capacity of the immune system to discriminate between "dangerous" and "harmless" antigens appears to develop with age and exposure to microbial flora. Thus, the ability of an individual or a group of animals to correctly regulate mucosal immune responses will depend on age, genetics and on their microbial environment and history. Attempts to manipulate the mucosal immune system towards active immune responses by oral vaccines, or towards oral tolerance, are likely to be confounded by environmentally-induced variability between individuals and between groups of animals.

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“…These include the FREP genes in snails that are thought to diversify through alternative splicing and gene conversion (30,51; reviewed in Ref. 24), the VCBP gene family in Amphioxus (6 -8, 22, 23, 51), and the antimicrobial penaeidins in shrimp (10,15,31).…”

Section: Paradigm Shiftmentioning

confidence: 99%

Unexpected diversity displayed in cDNAs expressed by the immune cells of the purple sea urchin,Strongylocentrotus purpuratus

Terwilliger

Buckley

Mehta

et al. 2006

Physiological Genomics

252

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We recently identified a unique family of transcripts, the 185/333 family, that comprise ϳ60% of the mRNAs induced by coelomocytes from the purple sea urchin in response to immunological challenge from lipopolysaccharide. An analysis of 81 full-length cDNAs revealed 67 unique nucleotide sequences encoding 64 different proteins. Diversity of the transcripts was based on 25 sequence blocks, or "elements," which resulted in 22 different element patterns based on their presence or absence. Furthermore, there was a high level of nucleotide variation within elements, including single nucleotide polymorphisms and insertions/deletions, both of which resulted in amino acid sequence variability. The deduced 185/333 proteins contained an NH2-terminal leader, a glycine-rich region with an RGD motif, a histidine-rich region, and a COOH-terminal region. Two 185/333 genes, identified in the partially assembled Strongylocentrotus purpuratus genome, have two exons. The first encoded the leader, and the second encoded the remainder of the predicted protein. Estimates from quantitative PCR indicated that there were ϳ100 alleles in the diploid genome. These results suggested that the purple sea urchin may have mechanisms for generating high levels of diversity in response to immunological challenge that have not been considered previously. coelomocytes; innate immunity; echinoderm INVERTEBRATES WERE ONCE THOUGHT to have simple immune systems; however, recent evidence suggests that both invertebrates and plants express families of immune response genes with high levels of sequence diversity (reviewed in Refs. 13, 22-25). The fresh water snail, Biomphalaria glabrata, expresses fibrinogen-related proteins (FREPs) that contain one or two highly variable immunoglobulin superfamily (IgSF) domains (1,17,21,53,54). The protochordate, Branchiostoma floridae (Amphioxus), expresses a family of chitin-binding genes that also have diversified IgSF variable domains (6 -8).A single copy gene in Drosophila called the Down syndrome cell adhesion molecule (DSCAM), which is expressed in hemocytes, also contains multiple IgSF domains with high levels of sequence diversity generated by alternative splicing of 95 exons (47). The existence of highly variable defense response genes is not restricted to animals. Plant genomes contain large families of disease resistance (R) genes (reviewed in Ref. 25) that are closely linked and undergo both gene duplication and conversion events, which generate new members (20,34,35). Thus, in light of recent evidence and contrary to previous notions that innate immunity was invariant, both invertebrates and plants may be able to diversify their innate immune responses.The identification of families of variable immune response genes has been facilitated by the characterization of expressed sequence tags (ESTs), which can provide a global picture of transcriptional activity after immune challenge. In the purple sea urchin, Strongylocentrotus purpuratus, EST studies have identified a variety of immune-related genes that ...

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Genes “Waiting” for Recruitment by the Adaptive Immune System: The Insights from Amphioxus

Cited by 57 publications

References 59 publications

Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity

Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity

The postnatal development of the mucosal immune system and mucosal tolerance in domestic animals

Unexpected diversity displayed in cDNAs expressed by the immune cells of the purple sea urchin,Strongylocentrotus purpuratus

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