Identification of a homologue of CD59 in a cyclostome: implications for the evolutionary development of the complement system

Remedios, Nick dos; Ramsland, Paul A.; Hook, Jeffrey W.; Raison, Robert L.

doi:10.1016/s0145-305x(98)00049-4

Cited by 16 publications

(4 citation statements)

References 40 publications

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“…Factor H-like clones have been isolated from trout and sequence analysis has shown high homology with the SBP1 protein from the barred sand bass [61]. A molecule similar to 408 mammalian CD59 has been cloned from hagfish, Eptatretus stouti, a jawless fish, and from the brook trout [62,63].…”

Section: The Complement System In Teleostsmentioning

confidence: 99%

The complement system in teleosts

Holland

Lambris

2002

Fish & Shellfish Immunology

531

251

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Section: The Complement System In Teleostsmentioning

confidence: 99%

The complement system in teleosts

Holland

Lambris

2002

Fish & Shellfish Immunology

531

251

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“…In contrast, alignments with human exon 5, which codes for the majority of the mature protein sequence, identified putative regions of homology comprised of two adjacent, truncated regions (together, approximately 60% the size of its human counterpart) that did not contain a complete ORF but contained both non-sense mutations and deletions. In humans, this region encodes for a Cysteine-Asparagine combination that appears to be highly conserved across vertebrate Ly6 family proteins (30). The loss of this highly conserved region and the presence of nonsense and deletion mutations support the assertion that this segment of chromosomal DNA is no longer under functional constraint, but instead represents an inactive pseudogene prone to genetic drift.…”

Section: Discussionmentioning

confidence: 99%

Absence of CD59 in Guinea Pigs: Analysis of the Cavia porcellus Genome Suggests the Evolution of a CD59 Pseudogene

Boshra

Zelek

Hughes

et al. 2018

The Journal of Immunology

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CD59 is a membrane-bound regulatory protein that inhibits the assembly of the terminal membrane attack complex (C5b-9) of complement. From its original discovery in humans almost 30 years ago, CD59 has been characterized in a variety of species, from primates to early vertebrates, such as teleost fish. CD59 is ubiquitous in mammals; however, we have described circumstantial evidence suggesting that guinea pigs () lack CD59, at least on erythrocytes. In this study, we have used a combination of phylogenetic analyses with syntenic alignment of mammalian genes to identify the only span of genomic DNA in that is homologous to a portion of mammalian and show that this segment of DNA is not transcribed. We describe a pseudogene sharing homology to exons 2 through 5 of human present in the genome. This pseudogene was flanked by homologs of two genes, and, a relationship and orientation that were consistent with other known mammalian genes. Analysis using RNA sequencing confirmed that this segment of chromosomal DNA was not transcribed. We conclude that guinea pigs lack an intact gene encoding CD59; to our knowledge, this is the first report of a mammalian species that does not express a functional CD59. The pseudogene we describe is likely the product of a genomic deletion event during its evolutionary divergence from other members of the rodent order.

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“…A gene encoding a CD59-like molecule has also been cloned from the hagfish. The presence of CD59 in the hagfish, together with the observation of a C5a-like activity in hagfish plasma, suggests that an ancient form of the lytic pathway is present in these primitive vertebrates (dos Remedios et al, 1999).…”

Section: Complement Regulatory Proteinsmentioning

confidence: 96%

“…There is no evidence for the presence of the membrane attack complex (MAC) in lamprey (Fujii et al, 1992), although a single component with lytic activity has been described in lamprey serum. However, a gene with sequence similarity to the mammalian complement membrane attack regulatory molecule CD59 (protectin) has been reported in the hagfish (dos Remedios et al, 1999). The presence of this gene suggests that the terminal lytic complement pathway (C5b-9) could operate in these primitive vertebrates.…”

Section: Ancestry Of the Complement Systemmentioning

confidence: 99%

The ancestry and cumulative evolution of immune reactions.

Dzik

2010

Acta Biochim Pol

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The last two decades of study enriched greatly our knowledge of how the immune system originated and the sophisticated immune mechanisms of today's vertebrates and invertebrates developed. Even unicellular organisms possess mechanisms for pathogen destruction and self recognition. The ability to distinguish self from non-self is a prerequisite for recognition of sexual compatibility and ensuring survival. Molecules involved in these processes resemble those found in the phagocytic cells of higher organisms. Recognition of bacteria by scavenger receptors induces phagocytosis or endocytosis. The phagocytic mechanisms characterizing the amoeboid protozoans developed further during the evolution towards innate immunity. The scavenger receptor cysteine-rich domain SRCR is encoded in the genomes from the most primitive sponges to mammals. The immune system of sponges comprises signal transduction molecules which occur in higher metazoans as well. Sponges already possess recognition systems for pathogenic bacteria and fungi, based on membrane receptors (a lipopolysaccharide-interacting protein, a cell surface receptor recognizing β(1 → 3)-d-glucans of fungi). Perforin-like molecules and lysozymes are involved, among others, in defense in sponges. Reactive oxygen and nitrogen species function in the immunity of early metazoan. Genes encoding the family of reactive oxygen-generating NADPH oxidases (Noxes) are found in a variety of protists and plants. The NO synthases of cnidarians, mollusks, and chordates are conserved with respect to the mammalian NOS. The antimicrobial peptides of protozoans, amoebapores, are structural and functional analogs of the natural killer cell peptide, NK-lysin, of vertebrates. An ancestral S-type lectin has been found in sponges. Opsonizing properties of lectins and the ability to agglutinate cells justify their classification as primitive recognition molecules. Invertebrate cytokines are not homologous to those of vertebrate, and their functional convergence was presumably enabled by the general similarity of the lectin-like recognition domain three-dimensional structure. Sponges contain molecules with SCR/CCP domains that show high homology to the mammalian regulators of complement activation (RCA family). A multi-component complement system comprising at least the central molecule of the complement system, C3, Factor B, and MASP developed in the cnidarians and evolved into the multilevel cascade engaged in innate and acquired immunity of vertebrates. The adaptive immune system of mammals is also deeply rooted in the metazoan evolution. Some its precursors have been traced as deep as in sponges, namely, two classes of receptors that comprise Ig-like domains, the receptor tyrosine kinases (RTK), and the non-enzymic sponge adhesion molecules (SAM). The antibody-based immune system defined by the presence of the major histocompatibility complex (MHC), T-cell receptor (TCR), B-cell receptor (BCR) or recombination activating genes (RAGs) is known beginning from jawed fishes. However, genes closely resembling RAG1 and RAG2 have been uncovered in the genome of a see urchin. The ancestry of MHC gene remains unknown. Similarly, no homologue of the protein binding domain (PBD) in MHC molecules has been found in invertebrates. The pathway by which endogenous peptides are degraded for presentation with class I MHC molecules utilizes mechanisms similar to those involved in the normal turnover of intracellular proteins, apparently recruited to work also for the immune system. Several cDNAs coding for lysosomal enzymes, e.g., cathepsin, have been isolated from sponges. All chromosomal duplication events in the MHC region occurred after the origin of the agnathans but before the gnathostomes split from them. The V-domains of the subtype found in the receptors of T and B-cells are known from both agnathans and cephalochordates, although they do not rearrange. The rearrangement mechanism of the lymphocyte V-domains suggests its origin from a common ancestral domain existing before the divergence of the extant gnathostome classes. Activation-induced deaminase (AID) - homologous proteins have been found only in the gnathostomes. It appears thus that the adaptive immunity of vertebrates is a result of stepwise accumulation of small changes in molecules, cells and organs over almost half a billion years.

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Identification of a homologue of CD59 in a cyclostome: implications for the evolutionary development of the complement system

Cited by 16 publications

References 40 publications

The complement system in teleosts

The complement system in teleosts

Absence of CD59 in Guinea Pigs: Analysis of the Cavia porcellus Genome Suggests the Evolution of a CD59 Pseudogene

The ancestry and cumulative evolution of immune reactions.

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