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Genomic analysis of the TRIM family reveals two groups of genes with distinct evolutionary properties.

Sardiello M, Cairo S, Fontanella B, Ballabio A, Meroni G - BMC Evol. Biol. (2008)

Bottom Line: By means of comparative analyses we found that, after assembly of the tripartite motif in an early metazoan ancestor, few types of C-terminal domains have been associated with this module during evolution and that an important increase in TRIM number occurred in vertebrate species concomitantly with the addition of the SPRY domain.Comparing the murine and human TRIM sets, we found that group 1 and 2 genes evolve at different speeds and are subject to different selective pressures.We found that the TRIM family is composed of two groups of genes with distinct evolutionary properties.

View Article: PubMed Central - HTML - PubMed

Affiliation: Telethon Institute of Genetics and Medicine, Via P, Castellino 111, 80131 Naples, Italy. sardiello@tigem.it

ABSTRACT

Background: The TRIM family is composed of multi-domain proteins that display the Tripartite Motif (RING, B-box and Coiled-coil) that can be associated with a C-terminal domain. TRIM genes are involved in ubiquitylation and are implicated in a variety of human pathologies, from Mendelian inherited disorders to cancer, and are also involved in cellular response to viral infection.

Results: Here we defined the entire human TRIM family and also identified the TRIM sets of other vertebrate (mouse, rat, dog, cow, chicken, tetraodon, and zebrafish) and invertebrate species (fruitfly, worm, and ciona). By means of comparative analyses we found that, after assembly of the tripartite motif in an early metazoan ancestor, few types of C-terminal domains have been associated with this module during evolution and that an important increase in TRIM number occurred in vertebrate species concomitantly with the addition of the SPRY domain. We showed that the human TRIM family is split into two groups that differ in domain structure, genomic organization and evolutionary properties. Group 1 members present a variety of C-terminal domains, are highly conserved among vertebrate species, and are represented in invertebrates. Conversely, group 2 is absent in invertebrates, is characterized by the presence of a C-terminal SPRY domain and presents unique sets of genes in each mammal examined. The generation of independent sets of group 2 genes is also evident in the other vertebrate species. Comparing the murine and human TRIM sets, we found that group 1 and 2 genes evolve at different speeds and are subject to different selective pressures.

Conclusion: We found that the TRIM family is composed of two groups of genes with distinct evolutionary properties. Group 2 is younger, highly dynamic, and might act as a reservoir to develop novel TRIM functions. Since some group 2 genes are implicated in innate immune response, their evolutionary features may account for species-specific battles against viral infection.

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Phylogenetic analysis of TRIM and TRIM-like proteins of representative species of mammals, aves, and fish. Human (Hs, dark blue), chicken (Gg, dark green), tetraodon (Tn, light blue); ciona (Ci, orange), fruitfly (red) and worm (light green) are included. Bootstrap support values based on 1000 replicates are shown. Group 1 TRIM37 sequences are used as outgroups. The scale of amino acid sequence divergence is indicated at the bottom right corner.
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Figure 6: Phylogenetic analysis of TRIM and TRIM-like proteins of representative species of mammals, aves, and fish. Human (Hs, dark blue), chicken (Gg, dark green), tetraodon (Tn, light blue); ciona (Ci, orange), fruitfly (red) and worm (light green) are included. Bootstrap support values based on 1000 replicates are shown. Group 1 TRIM37 sequences are used as outgroups. The scale of amino acid sequence divergence is indicated at the bottom right corner.

Mentions: In all species analyzed, we found clear orthologs for TRIM23 and TRIM37 (Fig. 6A). With respect to subgroup C, there is one representative of this subgroup in ciona, closely related to the fruitfly member. All the known mammalian members of this subgroup are found in chick with recognizable orthologous relationships (Fig. 6B). This is not completely true for tetraodon in which 3 members belonging to this group have been found: one orthologous to TRIM33 and the others representing fish-specific duplications related to the TRIM33-24 clade. Genes strictly related to KIAA0298/TRIM66* and TRIM19 have not been found in tetraodon (Fig. 6B). In ciona there are 5 representative members of subgroup A, 3 representing the ancestors of different subclades (TRIM9-67; TRIM1-18; TRIM54-55-63) and 2 apparently more ancestral genes. DIBP/TRIM44* appears to be uniquely represented in mammals. All the other members are present in chick and fish although orthology is clear only for TRIM9, 67, 1, 18, and 36. TRIM46, if truly absent, may have been lost in chick while of the MURF group (TRIM54, 55, 63) 2 orthologues are present in chick while 4 members with no direct orthologous relationship are present in fish (Fig. 6C). An analogous situation is observed for subgroup D. In fact, ciona has two representative members; orthologous relationship with human is observed for both chick and fish for four members (TRIM2, 3, 45, 71). TRIM32 might have been lost in chick and TRIM56 in both chick and fish (Fig. 6D). For the above group 1 subgroups, we therefore found that most of the mammalian components are present in chick often with clearly recognizable orthologous relationship. Although the number of members within these subgroups is similar also in tetraodon, the TRIM and TRIM-like genes in this species, consistent with a larger evolutionary distance, have duplicated and diverged more extensively, sometimes obscuring orthologies.


Genomic analysis of the TRIM family reveals two groups of genes with distinct evolutionary properties.

Sardiello M, Cairo S, Fontanella B, Ballabio A, Meroni G - BMC Evol. Biol. (2008)

Phylogenetic analysis of TRIM and TRIM-like proteins of representative species of mammals, aves, and fish. Human (Hs, dark blue), chicken (Gg, dark green), tetraodon (Tn, light blue); ciona (Ci, orange), fruitfly (red) and worm (light green) are included. Bootstrap support values based on 1000 replicates are shown. Group 1 TRIM37 sequences are used as outgroups. The scale of amino acid sequence divergence is indicated at the bottom right corner.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2533329&req=5

Figure 6: Phylogenetic analysis of TRIM and TRIM-like proteins of representative species of mammals, aves, and fish. Human (Hs, dark blue), chicken (Gg, dark green), tetraodon (Tn, light blue); ciona (Ci, orange), fruitfly (red) and worm (light green) are included. Bootstrap support values based on 1000 replicates are shown. Group 1 TRIM37 sequences are used as outgroups. The scale of amino acid sequence divergence is indicated at the bottom right corner.
Mentions: In all species analyzed, we found clear orthologs for TRIM23 and TRIM37 (Fig. 6A). With respect to subgroup C, there is one representative of this subgroup in ciona, closely related to the fruitfly member. All the known mammalian members of this subgroup are found in chick with recognizable orthologous relationships (Fig. 6B). This is not completely true for tetraodon in which 3 members belonging to this group have been found: one orthologous to TRIM33 and the others representing fish-specific duplications related to the TRIM33-24 clade. Genes strictly related to KIAA0298/TRIM66* and TRIM19 have not been found in tetraodon (Fig. 6B). In ciona there are 5 representative members of subgroup A, 3 representing the ancestors of different subclades (TRIM9-67; TRIM1-18; TRIM54-55-63) and 2 apparently more ancestral genes. DIBP/TRIM44* appears to be uniquely represented in mammals. All the other members are present in chick and fish although orthology is clear only for TRIM9, 67, 1, 18, and 36. TRIM46, if truly absent, may have been lost in chick while of the MURF group (TRIM54, 55, 63) 2 orthologues are present in chick while 4 members with no direct orthologous relationship are present in fish (Fig. 6C). An analogous situation is observed for subgroup D. In fact, ciona has two representative members; orthologous relationship with human is observed for both chick and fish for four members (TRIM2, 3, 45, 71). TRIM32 might have been lost in chick and TRIM56 in both chick and fish (Fig. 6D). For the above group 1 subgroups, we therefore found that most of the mammalian components are present in chick often with clearly recognizable orthologous relationship. Although the number of members within these subgroups is similar also in tetraodon, the TRIM and TRIM-like genes in this species, consistent with a larger evolutionary distance, have duplicated and diverged more extensively, sometimes obscuring orthologies.

Bottom Line: By means of comparative analyses we found that, after assembly of the tripartite motif in an early metazoan ancestor, few types of C-terminal domains have been associated with this module during evolution and that an important increase in TRIM number occurred in vertebrate species concomitantly with the addition of the SPRY domain.Comparing the murine and human TRIM sets, we found that group 1 and 2 genes evolve at different speeds and are subject to different selective pressures.We found that the TRIM family is composed of two groups of genes with distinct evolutionary properties.

View Article: PubMed Central - HTML - PubMed

Affiliation: Telethon Institute of Genetics and Medicine, Via P, Castellino 111, 80131 Naples, Italy. sardiello@tigem.it

ABSTRACT

Background: The TRIM family is composed of multi-domain proteins that display the Tripartite Motif (RING, B-box and Coiled-coil) that can be associated with a C-terminal domain. TRIM genes are involved in ubiquitylation and are implicated in a variety of human pathologies, from Mendelian inherited disorders to cancer, and are also involved in cellular response to viral infection.

Results: Here we defined the entire human TRIM family and also identified the TRIM sets of other vertebrate (mouse, rat, dog, cow, chicken, tetraodon, and zebrafish) and invertebrate species (fruitfly, worm, and ciona). By means of comparative analyses we found that, after assembly of the tripartite motif in an early metazoan ancestor, few types of C-terminal domains have been associated with this module during evolution and that an important increase in TRIM number occurred in vertebrate species concomitantly with the addition of the SPRY domain. We showed that the human TRIM family is split into two groups that differ in domain structure, genomic organization and evolutionary properties. Group 1 members present a variety of C-terminal domains, are highly conserved among vertebrate species, and are represented in invertebrates. Conversely, group 2 is absent in invertebrates, is characterized by the presence of a C-terminal SPRY domain and presents unique sets of genes in each mammal examined. The generation of independent sets of group 2 genes is also evident in the other vertebrate species. Comparing the murine and human TRIM sets, we found that group 1 and 2 genes evolve at different speeds and are subject to different selective pressures.

Conclusion: We found that the TRIM family is composed of two groups of genes with distinct evolutionary properties. Group 2 is younger, highly dynamic, and might act as a reservoir to develop novel TRIM functions. Since some group 2 genes are implicated in innate immune response, their evolutionary features may account for species-specific battles against viral infection.

Show MeSH
Related in: MedlinePlus