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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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Presence or absence of complement component genes in various animal groups. All complement components and related genes of human, as a representative of Mammalia, are shown, and the presence of the orthologous genes reported from the other animal groups are indicated by the reference numbers. Plus and minus indicate the presence and absence, respectively, of the orthologous genes in the assembled genome sequences of at least one representative species of each group. Genes located outside of the complement gene clusters in the phylogenetic tree, showing an uncertain orthologous relationship with complement genes, are indicated in red. Literatures cited here are: 1 Mavroidis et al. 1995; 2 Fritzinger et al. 1992; 3 Kaufman et al. 1999; 4 Kjalke et al. 1993; 5 Laursen et al. 1998; 6 Lynch et al. 2005; 7 Oshiumi et al. 2005; 8 Mahon et al. 1999; 9 Grossberger et al. 1989; 10 Mo et al. 1996; 11 Kato et al. 1995; 12 Kato et al. 1994; 13 Endo et al. 1998 and Kakinuma et al. 2003; 14 Endo et al. 1998; 15 Kunnath-Muglia et al. 1993; 16 Boshra et al. 2005; 17 Abelseth et al. 2003; 18 Samonte et al. 2002; 19 Zarkadis et al. 2001; 20 Nakao et al. 2000; 21 Kuroda et al. 2000; 22 Sato et al. 1999; 23 Sunyer et al. 1997b; 24 Sunyer et al. 1997a; 25 Sunyer et al. 1996; 26 Lambris et al. 1993; 27 Boshra et al. 2004a; 28 Wang and Secombes 2003; 29 Sambrook et al. 2003; 30 Kato et al. 2003; 31 Franchini et al. 2001; 32 Nakao et al. 2002; 33 Sunyer et al. 1998; 34 Nakao et al. 1998; 35 Gongora et al. 1998; 36 Seeger et al. 1996; 37 Kuroda et al. 1996; 38 Yano and Nakao 1994; 39 Vitved et al. 2000; 40 Nakao et al. 2001; 41 Chondrou et al. 2006; 42 Zarkadis et al. 2005; 43 Papanastasiou and Zarkadis 2005; 44 Uemura et al. 1996; 45 Katagiri et al. 1999; 46 Kazantzi et al. 2003; 47 Yeo et al. 1997; 48 Tomlinson et al. 1993; 49 Nakao et al. 2003a; 50 Kemper et al. 1998; 51 Boshra et al. 2005; 52 Boshra et al. 2004b; 53 Fujiki et al. 2003; 54 Dodds et al. 1998; 55 Terado et al. 2003; 56 Smith 1998; 57 Terado et al. 2002; 58 Ishiguro et al. 1992; 59 Nonaka et al. 1984 and Nonaka and Takahashi 1992; 60 Nonaka et al. 1994; 61 Matsushita et al. 2004; 62 Takahashi et al. 2006; 63 Song et al. 2005; 64 Kimura et al. 2004; 65 dos Remedios et al. 1999; 66 Suzuki et al. 2002; 67 Endo et al. 2003; 68 Raftos et al. 2002; 69 Marino et al. 2002; 70 Nonaka et al. 1999; 71 Yoshizaki et al. 2005; 72 Azumi et al. 2003; 73 Dehal et al. 2002; 74 Kenjo et al. 2001; 75 Sekine et al. 2001; 76 Ji et al. 1997; 77 Miyazawa and Nonaka 2004; 78 Miyazawa et al. 2001; 79 Al-Sharif et al. 1998; 80 Smith et al. 1998; 81 Zhu et al. 2005; 82 Adams et al. 2000; 83 The C. elegans Sequencing Consortium 1998; 84 Dishaw et al. 2005; *1 H. Nagumo et al., unpublished data; and *2 A. Kimura and M. Nonaka, unpublished data
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Fig2: Presence or absence of complement component genes in various animal groups. All complement components and related genes of human, as a representative of Mammalia, are shown, and the presence of the orthologous genes reported from the other animal groups are indicated by the reference numbers. Plus and minus indicate the presence and absence, respectively, of the orthologous genes in the assembled genome sequences of at least one representative species of each group. Genes located outside of the complement gene clusters in the phylogenetic tree, showing an uncertain orthologous relationship with complement genes, are indicated in red. Literatures cited here are: 1 Mavroidis et al. 1995; 2 Fritzinger et al. 1992; 3 Kaufman et al. 1999; 4 Kjalke et al. 1993; 5 Laursen et al. 1998; 6 Lynch et al. 2005; 7 Oshiumi et al. 2005; 8 Mahon et al. 1999; 9 Grossberger et al. 1989; 10 Mo et al. 1996; 11 Kato et al. 1995; 12 Kato et al. 1994; 13 Endo et al. 1998 and Kakinuma et al. 2003; 14 Endo et al. 1998; 15 Kunnath-Muglia et al. 1993; 16 Boshra et al. 2005; 17 Abelseth et al. 2003; 18 Samonte et al. 2002; 19 Zarkadis et al. 2001; 20 Nakao et al. 2000; 21 Kuroda et al. 2000; 22 Sato et al. 1999; 23 Sunyer et al. 1997b; 24 Sunyer et al. 1997a; 25 Sunyer et al. 1996; 26 Lambris et al. 1993; 27 Boshra et al. 2004a; 28 Wang and Secombes 2003; 29 Sambrook et al. 2003; 30 Kato et al. 2003; 31 Franchini et al. 2001; 32 Nakao et al. 2002; 33 Sunyer et al. 1998; 34 Nakao et al. 1998; 35 Gongora et al. 1998; 36 Seeger et al. 1996; 37 Kuroda et al. 1996; 38 Yano and Nakao 1994; 39 Vitved et al. 2000; 40 Nakao et al. 2001; 41 Chondrou et al. 2006; 42 Zarkadis et al. 2005; 43 Papanastasiou and Zarkadis 2005; 44 Uemura et al. 1996; 45 Katagiri et al. 1999; 46 Kazantzi et al. 2003; 47 Yeo et al. 1997; 48 Tomlinson et al. 1993; 49 Nakao et al. 2003a; 50 Kemper et al. 1998; 51 Boshra et al. 2005; 52 Boshra et al. 2004b; 53 Fujiki et al. 2003; 54 Dodds et al. 1998; 55 Terado et al. 2003; 56 Smith 1998; 57 Terado et al. 2002; 58 Ishiguro et al. 1992; 59 Nonaka et al. 1984 and Nonaka and Takahashi 1992; 60 Nonaka et al. 1994; 61 Matsushita et al. 2004; 62 Takahashi et al. 2006; 63 Song et al. 2005; 64 Kimura et al. 2004; 65 dos Remedios et al. 1999; 66 Suzuki et al. 2002; 67 Endo et al. 2003; 68 Raftos et al. 2002; 69 Marino et al. 2002; 70 Nonaka et al. 1999; 71 Yoshizaki et al. 2005; 72 Azumi et al. 2003; 73 Dehal et al. 2002; 74 Kenjo et al. 2001; 75 Sekine et al. 2001; 76 Ji et al. 1997; 77 Miyazawa and Nonaka 2004; 78 Miyazawa et al. 2001; 79 Al-Sharif et al. 1998; 80 Smith et al. 1998; 81 Zhu et al. 2005; 82 Adams et al. 2000; 83 The C. elegans Sequencing Consortium 1998; 84 Dishaw et al. 2005; *1 H. Nagumo et al., unpublished data; and *2 A. Kimura and M. Nonaka, unpublished data

Mentions: To trace the evolution of the complement system, we searched the genome data of chicken (Gallus gallus, http://www.ncbi.nlm.nih.gov/genome/guide/chicken/), clawed frog (Xenopus tropicalis, http://genome.jgi-psf.org/Xentr4/Xentr4.home.html), pufferfish (Takifugu rubripes, http://genome.jgi-psf.org/Takru4/Takru4.home.html), and sea anemone (Nematostella vectensis, http://www.stellabase.org/) for the presence of the complement genes. Because five complement gene families, C3/C4/C5, Bf/C2, MASP/C1r/s, C6/C7/C8A/C8B/C9, and Factor I (I), have a unique domain combination found only among complement genes in the human genome, identification was carried out based merely on the predicted domain structures. For other complement genes, however, the same domain combination is also found in noncomplement genes. In these cases, phylogenetic tree analysis was performed to confirm the orthologous relationship between the possible complement genes of various animals and their mammalian counterparts. Figure 2 summarizes the current status of the presence/absence of the complement genes judged by these searches, the published results, and our unpublished experimental data.Fig. 2


Genomic view of the evolution of the complement system.

Nonaka M, Kimura A - Immunogenetics (2006)

Presence or absence of complement component genes in various animal groups. All complement components and related genes of human, as a representative of Mammalia, are shown, and the presence of the orthologous genes reported from the other animal groups are indicated by the reference numbers. Plus and minus indicate the presence and absence, respectively, of the orthologous genes in the assembled genome sequences of at least one representative species of each group. Genes located outside of the complement gene clusters in the phylogenetic tree, showing an uncertain orthologous relationship with complement genes, are indicated in red. Literatures cited here are: 1 Mavroidis et al. 1995; 2 Fritzinger et al. 1992; 3 Kaufman et al. 1999; 4 Kjalke et al. 1993; 5 Laursen et al. 1998; 6 Lynch et al. 2005; 7 Oshiumi et al. 2005; 8 Mahon et al. 1999; 9 Grossberger et al. 1989; 10 Mo et al. 1996; 11 Kato et al. 1995; 12 Kato et al. 1994; 13 Endo et al. 1998 and Kakinuma et al. 2003; 14 Endo et al. 1998; 15 Kunnath-Muglia et al. 1993; 16 Boshra et al. 2005; 17 Abelseth et al. 2003; 18 Samonte et al. 2002; 19 Zarkadis et al. 2001; 20 Nakao et al. 2000; 21 Kuroda et al. 2000; 22 Sato et al. 1999; 23 Sunyer et al. 1997b; 24 Sunyer et al. 1997a; 25 Sunyer et al. 1996; 26 Lambris et al. 1993; 27 Boshra et al. 2004a; 28 Wang and Secombes 2003; 29 Sambrook et al. 2003; 30 Kato et al. 2003; 31 Franchini et al. 2001; 32 Nakao et al. 2002; 33 Sunyer et al. 1998; 34 Nakao et al. 1998; 35 Gongora et al. 1998; 36 Seeger et al. 1996; 37 Kuroda et al. 1996; 38 Yano and Nakao 1994; 39 Vitved et al. 2000; 40 Nakao et al. 2001; 41 Chondrou et al. 2006; 42 Zarkadis et al. 2005; 43 Papanastasiou and Zarkadis 2005; 44 Uemura et al. 1996; 45 Katagiri et al. 1999; 46 Kazantzi et al. 2003; 47 Yeo et al. 1997; 48 Tomlinson et al. 1993; 49 Nakao et al. 2003a; 50 Kemper et al. 1998; 51 Boshra et al. 2005; 52 Boshra et al. 2004b; 53 Fujiki et al. 2003; 54 Dodds et al. 1998; 55 Terado et al. 2003; 56 Smith 1998; 57 Terado et al. 2002; 58 Ishiguro et al. 1992; 59 Nonaka et al. 1984 and Nonaka and Takahashi 1992; 60 Nonaka et al. 1994; 61 Matsushita et al. 2004; 62 Takahashi et al. 2006; 63 Song et al. 2005; 64 Kimura et al. 2004; 65 dos Remedios et al. 1999; 66 Suzuki et al. 2002; 67 Endo et al. 2003; 68 Raftos et al. 2002; 69 Marino et al. 2002; 70 Nonaka et al. 1999; 71 Yoshizaki et al. 2005; 72 Azumi et al. 2003; 73 Dehal et al. 2002; 74 Kenjo et al. 2001; 75 Sekine et al. 2001; 76 Ji et al. 1997; 77 Miyazawa and Nonaka 2004; 78 Miyazawa et al. 2001; 79 Al-Sharif et al. 1998; 80 Smith et al. 1998; 81 Zhu et al. 2005; 82 Adams et al. 2000; 83 The C. elegans Sequencing Consortium 1998; 84 Dishaw et al. 2005; *1 H. Nagumo et al., unpublished data; and *2 A. Kimura and M. Nonaka, unpublished data
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Fig2: Presence or absence of complement component genes in various animal groups. All complement components and related genes of human, as a representative of Mammalia, are shown, and the presence of the orthologous genes reported from the other animal groups are indicated by the reference numbers. Plus and minus indicate the presence and absence, respectively, of the orthologous genes in the assembled genome sequences of at least one representative species of each group. Genes located outside of the complement gene clusters in the phylogenetic tree, showing an uncertain orthologous relationship with complement genes, are indicated in red. Literatures cited here are: 1 Mavroidis et al. 1995; 2 Fritzinger et al. 1992; 3 Kaufman et al. 1999; 4 Kjalke et al. 1993; 5 Laursen et al. 1998; 6 Lynch et al. 2005; 7 Oshiumi et al. 2005; 8 Mahon et al. 1999; 9 Grossberger et al. 1989; 10 Mo et al. 1996; 11 Kato et al. 1995; 12 Kato et al. 1994; 13 Endo et al. 1998 and Kakinuma et al. 2003; 14 Endo et al. 1998; 15 Kunnath-Muglia et al. 1993; 16 Boshra et al. 2005; 17 Abelseth et al. 2003; 18 Samonte et al. 2002; 19 Zarkadis et al. 2001; 20 Nakao et al. 2000; 21 Kuroda et al. 2000; 22 Sato et al. 1999; 23 Sunyer et al. 1997b; 24 Sunyer et al. 1997a; 25 Sunyer et al. 1996; 26 Lambris et al. 1993; 27 Boshra et al. 2004a; 28 Wang and Secombes 2003; 29 Sambrook et al. 2003; 30 Kato et al. 2003; 31 Franchini et al. 2001; 32 Nakao et al. 2002; 33 Sunyer et al. 1998; 34 Nakao et al. 1998; 35 Gongora et al. 1998; 36 Seeger et al. 1996; 37 Kuroda et al. 1996; 38 Yano and Nakao 1994; 39 Vitved et al. 2000; 40 Nakao et al. 2001; 41 Chondrou et al. 2006; 42 Zarkadis et al. 2005; 43 Papanastasiou and Zarkadis 2005; 44 Uemura et al. 1996; 45 Katagiri et al. 1999; 46 Kazantzi et al. 2003; 47 Yeo et al. 1997; 48 Tomlinson et al. 1993; 49 Nakao et al. 2003a; 50 Kemper et al. 1998; 51 Boshra et al. 2005; 52 Boshra et al. 2004b; 53 Fujiki et al. 2003; 54 Dodds et al. 1998; 55 Terado et al. 2003; 56 Smith 1998; 57 Terado et al. 2002; 58 Ishiguro et al. 1992; 59 Nonaka et al. 1984 and Nonaka and Takahashi 1992; 60 Nonaka et al. 1994; 61 Matsushita et al. 2004; 62 Takahashi et al. 2006; 63 Song et al. 2005; 64 Kimura et al. 2004; 65 dos Remedios et al. 1999; 66 Suzuki et al. 2002; 67 Endo et al. 2003; 68 Raftos et al. 2002; 69 Marino et al. 2002; 70 Nonaka et al. 1999; 71 Yoshizaki et al. 2005; 72 Azumi et al. 2003; 73 Dehal et al. 2002; 74 Kenjo et al. 2001; 75 Sekine et al. 2001; 76 Ji et al. 1997; 77 Miyazawa and Nonaka 2004; 78 Miyazawa et al. 2001; 79 Al-Sharif et al. 1998; 80 Smith et al. 1998; 81 Zhu et al. 2005; 82 Adams et al. 2000; 83 The C. elegans Sequencing Consortium 1998; 84 Dishaw et al. 2005; *1 H. Nagumo et al., unpublished data; and *2 A. Kimura and M. Nonaka, unpublished data
Mentions: To trace the evolution of the complement system, we searched the genome data of chicken (Gallus gallus, http://www.ncbi.nlm.nih.gov/genome/guide/chicken/), clawed frog (Xenopus tropicalis, http://genome.jgi-psf.org/Xentr4/Xentr4.home.html), pufferfish (Takifugu rubripes, http://genome.jgi-psf.org/Takru4/Takru4.home.html), and sea anemone (Nematostella vectensis, http://www.stellabase.org/) for the presence of the complement genes. Because five complement gene families, C3/C4/C5, Bf/C2, MASP/C1r/s, C6/C7/C8A/C8B/C9, and Factor I (I), have a unique domain combination found only among complement genes in the human genome, identification was carried out based merely on the predicted domain structures. For other complement genes, however, the same domain combination is also found in noncomplement genes. In these cases, phylogenetic tree analysis was performed to confirm the orthologous relationship between the possible complement genes of various animals and their mammalian counterparts. Figure 2 summarizes the current status of the presence/absence of the complement genes judged by these searches, the published results, and our unpublished experimental data.Fig. 2

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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Related in: MedlinePlus