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Genomic view of the evolution of the complement system.

Nonaka M, Kimura A - Immunogenetics (2006)

Bottom Line: Genome information from a few mammals, chicken, clawed frog, a few bony fish, sea squirt, fruit fly, nematoda and sea anemone indicate that bony fish and higher vertebrates share practically the same set of complement genes.Members of most complement gene families are also present in ascidians, although they do not show a one-to-one correspondence to their counterparts in higher vertebrates, indicating that the gene duplications of each gene family occurred independently in vertebrates and ascidians.The C3 and factor B genes, but probably not the other complement genes, are present in the genome of the cnidaria and some protostomes, indicating that the origin of the central part of the complement system was established more than 1,000 MYA.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Tokyo, Japan. mnonaka@biol.s.u-tokyo.ac.jp

ABSTRACT
The recent accumulation of genomic information of many representative animals has made it possible to trace the evolution of the complement system based on the presence or absence of each complement gene in the analyzed genomes. Genome information from a few mammals, chicken, clawed frog, a few bony fish, sea squirt, fruit fly, nematoda and sea anemone indicate that bony fish and higher vertebrates share practically the same set of complement genes. This suggests that most of the gene duplications that played an essential role in establishing the mammalian complement system had occurred by the time of the teleost/mammalian divergence around 500 million years ago (MYA). Members of most complement gene families are also present in ascidians, although they do not show a one-to-one correspondence to their counterparts in higher vertebrates, indicating that the gene duplications of each gene family occurred independently in vertebrates and ascidians. The C3 and factor B genes, but probably not the other complement genes, are present in the genome of the cnidaria and some protostomes, indicating that the origin of the central part of the complement system was established more than 1,000 MYA.

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Evolutionary processes of the complement system. Evolutionary origins of the three complement activation pathways are shown by the gray arrows. The origin and evolution of the major gene families of the complement system are shown by the colored arrows. Timings of the gene duplications that possibly contributed to the establishment of the classical pathway are shown by the double-headed arrows. Because the presence of the classical pathway was functionally demonstrated in sharks, it is likely that the Bf/C2 and MASP/C1r,s gene duplication occurred before the emergence of cartilaginous fish
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Fig4: Evolutionary processes of the complement system. Evolutionary origins of the three complement activation pathways are shown by the gray arrows. The origin and evolution of the major gene families of the complement system are shown by the colored arrows. Timings of the gene duplications that possibly contributed to the establishment of the classical pathway are shown by the double-headed arrows. Because the presence of the classical pathway was functionally demonstrated in sharks, it is likely that the Bf/C2 and MASP/C1r,s gene duplication occurred before the emergence of cartilaginous fish

Mentions: The current view of the complement system evolutionary processes is summarized in Fig. 4. First, the primitive complement system, most likely composed of C3 and Bf and thus similar to the mammalian alternative pathway, emerged in the common ancestor of Cnidaria and Bilateralia more than 1,300 MYA. Structural features of these Cnidaria genes suggest that the ancestral C3 was proteolytically activated by Bf, and that it formed a covalent bond with nonself molecules using its intramolecular thioester bond. Whereas the C3 and Bf genes were retained by deuterostomes, they were lost many times independently in the protostome lineages. Second, with the emergence of chordates (900 MYA), the MASP, MBL, and ficolin genes were recruited to the complement system, establishing the lectin pathway. Finally, vertebrate-specific complement gene duplications, such as those among C3/C4/C5 and between Bf/C2 and MASP/C1r/s, occurred before the emergence of cartilaginous fish about 600 MYA, most probably contributing to the establishment of the third activation pathway, the classical pathway. Thus, the complement classical pathway seems to have been established simultaneously with the appearance of the lymphocyte-MHC-based adaptive immune system. Ancestral TCC genes appear to have been recruited by the complement system and duplicated to C6/C7/C8A/C8B/C9 before the appearance of the jawed vertebrates, although its timing still needs to be clarified in detail. The linkages between certain complement genes played a certain role in establishing the modern complement system by facilitating the coevolution of the linked genes.Fig. 4


Genomic view of the evolution of the complement system.

Nonaka M, Kimura A - Immunogenetics (2006)

Evolutionary processes of the complement system. Evolutionary origins of the three complement activation pathways are shown by the gray arrows. The origin and evolution of the major gene families of the complement system are shown by the colored arrows. Timings of the gene duplications that possibly contributed to the establishment of the classical pathway are shown by the double-headed arrows. Because the presence of the classical pathway was functionally demonstrated in sharks, it is likely that the Bf/C2 and MASP/C1r,s gene duplication occurred before the emergence of cartilaginous fish
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2480602&req=5

Fig4: Evolutionary processes of the complement system. Evolutionary origins of the three complement activation pathways are shown by the gray arrows. The origin and evolution of the major gene families of the complement system are shown by the colored arrows. Timings of the gene duplications that possibly contributed to the establishment of the classical pathway are shown by the double-headed arrows. Because the presence of the classical pathway was functionally demonstrated in sharks, it is likely that the Bf/C2 and MASP/C1r,s gene duplication occurred before the emergence of cartilaginous fish
Mentions: The current view of the complement system evolutionary processes is summarized in Fig. 4. First, the primitive complement system, most likely composed of C3 and Bf and thus similar to the mammalian alternative pathway, emerged in the common ancestor of Cnidaria and Bilateralia more than 1,300 MYA. Structural features of these Cnidaria genes suggest that the ancestral C3 was proteolytically activated by Bf, and that it formed a covalent bond with nonself molecules using its intramolecular thioester bond. Whereas the C3 and Bf genes were retained by deuterostomes, they were lost many times independently in the protostome lineages. Second, with the emergence of chordates (900 MYA), the MASP, MBL, and ficolin genes were recruited to the complement system, establishing the lectin pathway. Finally, vertebrate-specific complement gene duplications, such as those among C3/C4/C5 and between Bf/C2 and MASP/C1r/s, occurred before the emergence of cartilaginous fish about 600 MYA, most probably contributing to the establishment of the third activation pathway, the classical pathway. Thus, the complement classical pathway seems to have been established simultaneously with the appearance of the lymphocyte-MHC-based adaptive immune system. Ancestral TCC genes appear to have been recruited by the complement system and duplicated to C6/C7/C8A/C8B/C9 before the appearance of the jawed vertebrates, although its timing still needs to be clarified in detail. The linkages between certain complement genes played a certain role in establishing the modern complement system by facilitating the coevolution of the linked genes.Fig. 4

Bottom Line: Genome information from a few mammals, chicken, clawed frog, a few bony fish, sea squirt, fruit fly, nematoda and sea anemone indicate that bony fish and higher vertebrates share practically the same set of complement genes.Members of most complement gene families are also present in ascidians, although they do not show a one-to-one correspondence to their counterparts in higher vertebrates, indicating that the gene duplications of each gene family occurred independently in vertebrates and ascidians.The C3 and factor B genes, but probably not the other complement genes, are present in the genome of the cnidaria and some protostomes, indicating that the origin of the central part of the complement system was established more than 1,000 MYA.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Tokyo, Japan. mnonaka@biol.s.u-tokyo.ac.jp

ABSTRACT
The recent accumulation of genomic information of many representative animals has made it possible to trace the evolution of the complement system based on the presence or absence of each complement gene in the analyzed genomes. Genome information from a few mammals, chicken, clawed frog, a few bony fish, sea squirt, fruit fly, nematoda and sea anemone indicate that bony fish and higher vertebrates share practically the same set of complement genes. This suggests that most of the gene duplications that played an essential role in establishing the mammalian complement system had occurred by the time of the teleost/mammalian divergence around 500 million years ago (MYA). Members of most complement gene families are also present in ascidians, although they do not show a one-to-one correspondence to their counterparts in higher vertebrates, indicating that the gene duplications of each gene family occurred independently in vertebrates and ascidians. The C3 and factor B genes, but probably not the other complement genes, are present in the genome of the cnidaria and some protostomes, indicating that the origin of the central part of the complement system was established more than 1,000 MYA.

Show MeSH
Related in: MedlinePlus