Hydractinia Allodeterminant alr1 Resides in an Immunoglobulin Superfamily-like Gene Complex

Rosa, Sabrina; Powell, Anahid A.E.; Rosengarten, Rafael R.D.; Nicotra, Matthew L.; Moreno, Marlene Aparecida; Grimwood, Jane; Lakkis, Fadi F.G.; Dellaporta, Stephen S.L.; Buss, Leo L.W.

doi:10.1016/j.cub.2010.04.050

Cited by 66 publications

(132 citation statements)

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“…symbiolongicarpus population (Gloria-Soria et al 2012). The rich allelic nature of these genes facilitates only low rates of colony fusion -experimental manipulations of H. symbiolongicarpus have demonstrated fusion rates at less than 5% (Rosa et al 2010). Similarly, fusibility assays in three Israeli (Rinkevich et al 1995).…”

Section: B Phase Two: Recognitionmentioning

confidence: 99%

“…Sequence polymorphism in alr1 and alr2 is largely restricted to particular hypervariable regions (Nicotra et al 2009;Rosa et al 2010) (Figure 1.2a). Within the FuHC locus, variation in the new candidate allorecognition gene BHF (Voskoboynik et al 2013) and in sFuHC and mFuHC (De Tomaso et al 2005;Nydam et al 2013b;Voskoboynik et al 2013) is distributed across each protein's length; in BHF, polymorphism is somewhat more prominent within the first 300 nucleotides and is absolutely predictive of fusibility outcomes (Voskoboynik et al 2013).…”

Section: B Phase Two: Recognitionmentioning

confidence: 99%

“…The H. symbiolongicarpus alr1 and alr2 genes have been mapped to a single genomic interval, the allorecognition complex (ARC) (Cadavid et al 2004). A 700 kb sub-complex resides within the ARC, in which alr1 is clustered amongst an additional ten Ig-like domain-encoding genes; at least four of these genes are polymorphic (Rosa et al 2010). Although the precise role of these genes is unknown, the variable members remain plausible candidates for other currently unidentified allodeterminants within this species.…”

Section: A Clustering Of Allorecognition Genesmentioning

confidence: 99%

“…Allorecognition genes are often richly allelic. For example, fusion-rejection decisions in H. symbiolongicarpus are largely under the control of two tightly-linked, highly polymorphic genes, alr1 and alr2 (Rosa et al 2010); two contacting colonies require at least one shared allele at both alr1 and alr2 for recognition as self and subsequent successful fusion. Complementary DNA (cDNA) sequencing has identified around 200 unique alr2 alleles within a single Connecticut, USA.…”

Section: B Phase Two: Recognitionmentioning

confidence: 99%

“…Shown are the Amphimedon queenslandica AFs (Gauthier 2009), various reported FuHC locus genes from Botryllus schlosseri (De Tomaso et al 2005;Nyholm et al 2006;Nydam et al 2013a;2013b;Voskoboynik et al 2013), the peptidoglycan recognition protein genes (PGRPs) from Drosophila melanogaster (Werner et al 2000), the Hydractinia symbiolongicarpus ARC, including the uncharacterised IgSF-like genes present in the region (Nicotra et al 2009;Rosa et al 2010), and the Sp185/333 gene cluster from Strongylocentrotus purpuratus (Miller et al 2010). The D. melanogaster PGRP genes sit in three separate genomic regions, corresponding left to right to the X, 2R and 3L chromosomes, respectively.…”

Section: Figure 13 Genomic Clustering Of Invertebrate Self-nonself Rmentioning

confidence: 99%

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Self-nonself recognition: genomic and transcriptomic insights from the sponge aggregation factors

Grice¹

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The multicellular condition cannot be maintained without safeguards protecting the integrity of the individual. Tissue contact and fusion with other conspecific individuals may threaten this integrity, as genetically non-identical cells may shirk their somatic duties and gain disproportionate access to the germ line. As sessile invertebrates that commonly inhabit crowded benthic environments, sponges are particularly reliant on a molecular self-nonself defense system in order to resist loss of habitat space, chimerism and possible germ line parasitism by neighbouring conspecific sponges. Sponge allorecognition appears to be, at least in part, under the control of extracellular proteoglycans called aggregation factors (AFs), which were first discovered based on their role in the species-specific reaggregation of dissociated sponge cells. Although the AFs have been extensively studied for over fifty years, the majority of this work has involved biochemical, rather than genetic approaches, and has focussed on the role of the glycan subunits associated with the AFs. In the present work, I investigate the genetic properties underlying the AF protein backbone, to better understand the functions and evolution of these putative allorecognition molecules.Using newly-available genomic and transcriptomic data, I surveyed the phylum Porifera for novel putative AF sequences, to explore the evolutionary origins of this gene family. I conclude that the AFs are a demosponge and hexactinellid-specific innovation. I then performed an in-depth characterisation of the six AF genes from the model demosponge species, Amphimedon queenslandica. The six genes display a highly modular intron/exon organisation. However, as expected of putative allorecognition genes, the AFs are greatly diversified between individuals, with nucleotide polymorphism (and possible positive selection) and intron retention events distributed across the six genes. The AFs are very highly expressed across sponge development and in response to alloimmune challenge, and undergo a particular spike in gene expression levels after the onset of sponge metamorphosis. The AF genes also exhibit expression patterns across development that are significantly correlated with those of other, developmentally important genes with roles in various cell signalling pathways. I conclude that the AFs play a novel developmental role, in addition to their putative allorecognition capabilities.iii S e l f -N o N S e l f R e c o g N i t i o N : S p o N g e ag g R e g at i o N f a c t o R S Declaration by authorThis thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis.I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial ...

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Section: B Phase Two: Recognitionmentioning

confidence: 99%

Section: B Phase Two: Recognitionmentioning

confidence: 99%

Section: A Clustering Of Allorecognition Genesmentioning

confidence: 99%

Section: B Phase Two: Recognitionmentioning

confidence: 99%

Section: Figure 13 Genomic Clustering Of Invertebrate Self-nonself Rmentioning

confidence: 99%

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Self-nonself recognition: genomic and transcriptomic insights from the sponge aggregation factors

Grice¹

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Contagious cancer: Lessons from the devil and the dog

Belov

2012

BioEssays

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Cancer is generally defined as uncontrollable growth of cells caused by genetic aberrations and/or environmental factors. Yet contagious cancers also occur. The recent emergence of a contagious cancer in Tasmanian devils has reignited interest in transmissible cancers. Two naturally occurring transmissible cancers are known: devil facial tumour disease and canine transmissible venereal tumour. Both cancers evolved once and have then been transmitted from one individual to another as clonal cell lines. The dog cancer is ancient; having evolved more than 6,000 years ago, while the devil disease was first seen in 1996. In this review I will compare and contrast the two diseases focusing on the life histories of the clonal cell lines, their evolutionary trajectories and the mechanisms by which they have achieved immune tolerance. A greater understanding of these contagious cancers will provide unique insights into the role of the immune system in shaping tumour evolution and may uncover novel approaches for treating human cancer.

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A single gene determines allorecognition in hydrozoan jellyfish Cladonema radiatum inbred lines

Tang,

Tamura‐Nakano,

Kobayakawa

et al. 2024

J Exp Zool Pt A

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Allorecognition—the ability of an organism to discriminate between self and nonself—is crucial to colonial marine animals to avoid invasion by other individuals in the same habitat. The cnidarian hydroid Hydractinia has long been a major research model in studying invertebrate allorecognition, establishing a rich knowledge foundation. In this study, we introduce a new cnidarian model Cladonema radiatum (C. radiatum). C. radiatum is a hydroid jellyfish which also forms polyp colonies interconnected with stolons. Allorecognition responses—fusion or regression of stolons—are observed when stolons encounter each other. By transmission electron microscopy, we observe rapid tissue remodeling contributing to gastrovascular system connection in fusion. Meanwhile, rejection responses are regulated by reconstruction of the chitinous exoskeleton perisarc, and induction of necrotic and autophagic cellular responses at cells in contact with the opponent. Genetic analysis identifies allorecognition genes: six Alr genes located on the putative allorecognition complex and four immunoglobulin superfamily genes on a separate genome region. C. radiatum allorecognition genes show notable conservation with the Hydractinia Alr family. Remarkedly, stolon encounter assays of inbred lines reveal that genotypes of Alr1 solely determine allorecognition outcomes in C. radiatum.

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Hydractinia Allodeterminant alr1 Resides in an Immunoglobulin Superfamily-like Gene Complex

Cited by 66 publications

References 33 publications

Self-nonself recognition: genomic and transcriptomic insights from the sponge aggregation factors

Self-nonself recognition: genomic and transcriptomic insights from the sponge aggregation factors

Contagious cancer: Lessons from the devil and the dog

A single gene determines allorecognition in hydrozoan jellyfish Cladonema radiatum inbred lines

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