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Evolution and functional divergence of NLRP genes in mammalian reproductive systems.

Tian X, Pascal G, Monget P - BMC Evol. Biol. (2009)

Bottom Line: The aim of the present work was to study how these genes evolved and diverged after their duplication, as well as whether natural selection played a role during their evolution.In conclusion, this study brings us novel information on the evolution of mammalian reproduction-related NLRPs.On the one hand, NLRP genes duplicated and functionally diversified in mammalian reproductive systems (such as NLRP4, 5, 9 and 14).

View Article: PubMed Central - HTML - PubMed

Affiliation: Physiologie de la Reproduction et des Comportements, UMR 6175 INRA-CNRS-Université François Rabelais de Tours-Haras Nationaux, 37380 Nouzilly, France. xin.savois@tours.inra.fr

ABSTRACT

Background: NLRPs (Nucleotide-binding oligomerization domain, Leucine rich Repeat and Pyrin domain containing Proteins) are members of NLR (Nod-like receptors) protein family. Recent researches have shown that NLRP genes play important roles in both mammalian innate immune system and reproductive system. Several of NLRP genes were shown to be specifically expressed in the oocyte in mammals. The aim of the present work was to study how these genes evolved and diverged after their duplication, as well as whether natural selection played a role during their evolution.

Results: By using in silico methods, we have evaluated the evolution and functional divergence of NLRP genes, in particular of mouse reproduction-related Nlrp genes. We found that (1) major NLRP genes have been duplicated before the divergence of mammals, with certain lineage-specific duplications in primates (NLRP7 and 11) and in rodents (Nlrp1, 4 and 9 duplicates); (2) tandem duplication events gave rise to a mammalian reproduction-related NLRP cluster including NLRP2, 4, 5, 7, 8, 9, 11, 13 and 14 genes; (3) the function of mammalian oocyte-specific NLRP genes (NLRP4, 5, 9 and 14) might have diverged during gene evolution; (4) recent segmental duplications concerning Nlrp4 copies and vomeronasal 1 receptor encoding genes (V1r) have been undertaken in the mouse; and (5) duplicates of Nlrp4 and 9 in the mouse might have been subjected to adaptive evolution.

Conclusion: In conclusion, this study brings us novel information on the evolution of mammalian reproduction-related NLRPs. On the one hand, NLRP genes duplicated and functionally diversified in mammalian reproductive systems (such as NLRP4, 5, 9 and 14). On the other hand, during evolution, different lineages adapted to develop their own NLRP genes, particularly in reproductive function (such as the specific expansion of Nlrp4 and Nlrp9 in the mouse).

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Syntenic comparison of NLRP genes among the cattle, the dog, the human and the mouse. The NLRP genes are marked in red, the orthologues are indicated by discontinuous lines. The order of NLRPs in each genome is listed as following: The cattle: NLRP3 (chr 7); NLRP1 (chr 19); NLRP9, 13, 8 and 5 (chr 18); NLRP6 (Un.004.137); NLRP14 (chr 15). The dog: NLRP3 (chr 8); NLRP1 (chr 5); NLRP12, 2, 9, 13, 8 and 5 (chr 1); NLRP6 (chr 18); NLRP14 and 10 (chr 21). The human: NLRP3 (chr 1); NLRP1 (chr 17); NLRP12, 2, 9, 13, 8 and 5 (chr 19); NLRP6, NLRP14 and 10 (chr 11). The mouse: Nlrp3, 1a, 1b and 1c (chr 11); Nlrp12, 2, 4c, 4d, 4b, 9b, 4e, 5, 9c, 4a, 9a, 14, 10 and 6 (chr 7).
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Figure 2: Syntenic comparison of NLRP genes among the cattle, the dog, the human and the mouse. The NLRP genes are marked in red, the orthologues are indicated by discontinuous lines. The order of NLRPs in each genome is listed as following: The cattle: NLRP3 (chr 7); NLRP1 (chr 19); NLRP9, 13, 8 and 5 (chr 18); NLRP6 (Un.004.137); NLRP14 (chr 15). The dog: NLRP3 (chr 8); NLRP1 (chr 5); NLRP12, 2, 9, 13, 8 and 5 (chr 1); NLRP6 (chr 18); NLRP14 and 10 (chr 21). The human: NLRP3 (chr 1); NLRP1 (chr 17); NLRP12, 2, 9, 13, 8 and 5 (chr 19); NLRP6, NLRP14 and 10 (chr 11). The mouse: Nlrp3, 1a, 1b and 1c (chr 11); Nlrp12, 2, 4c, 4d, 4b, 9b, 4e, 5, 9c, 4a, 9a, 14, 10 and 6 (chr 7).

Mentions: Moreover, this reproduction-related clade is also supported by the syntenic analysis (Figure 2). In the human genome, all the reproduction-related NLRP genes, except for NLRP14, are tandemly located on the chromosome 19q13.42, suggesting that multiple tandem duplication events might have given birth to these genes. The similar arrangements of the reproduction-related NLRPs are also found in cattle and dog genomes (Figure 2). In the mouse genome, the reproduction-related Nlrps (except for Nlrp14) are not located side by side, but interrupted by some other types of genes, especially and mainly by certain V1r genes (discussed below) on chromosome 7A1 and 7A3. Although NLRP14 is not located in the syntenic region encompassing other reproduction-related NLRPs in all the studied mammalian genomes (involving cattle, dog, human, chimpanzee, mouse and rat), our phylogenetic result and the published expression profile show that this gene is close to other reproduction-related NLRPs. This suggests that early (before the divergence of mammals) genomic rearrangements might have resulted in the separation of NLRP14 from its relatives.


Evolution and functional divergence of NLRP genes in mammalian reproductive systems.

Tian X, Pascal G, Monget P - BMC Evol. Biol. (2009)

Syntenic comparison of NLRP genes among the cattle, the dog, the human and the mouse. The NLRP genes are marked in red, the orthologues are indicated by discontinuous lines. The order of NLRPs in each genome is listed as following: The cattle: NLRP3 (chr 7); NLRP1 (chr 19); NLRP9, 13, 8 and 5 (chr 18); NLRP6 (Un.004.137); NLRP14 (chr 15). The dog: NLRP3 (chr 8); NLRP1 (chr 5); NLRP12, 2, 9, 13, 8 and 5 (chr 1); NLRP6 (chr 18); NLRP14 and 10 (chr 21). The human: NLRP3 (chr 1); NLRP1 (chr 17); NLRP12, 2, 9, 13, 8 and 5 (chr 19); NLRP6, NLRP14 and 10 (chr 11). The mouse: Nlrp3, 1a, 1b and 1c (chr 11); Nlrp12, 2, 4c, 4d, 4b, 9b, 4e, 5, 9c, 4a, 9a, 14, 10 and 6 (chr 7).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2735741&req=5

Figure 2: Syntenic comparison of NLRP genes among the cattle, the dog, the human and the mouse. The NLRP genes are marked in red, the orthologues are indicated by discontinuous lines. The order of NLRPs in each genome is listed as following: The cattle: NLRP3 (chr 7); NLRP1 (chr 19); NLRP9, 13, 8 and 5 (chr 18); NLRP6 (Un.004.137); NLRP14 (chr 15). The dog: NLRP3 (chr 8); NLRP1 (chr 5); NLRP12, 2, 9, 13, 8 and 5 (chr 1); NLRP6 (chr 18); NLRP14 and 10 (chr 21). The human: NLRP3 (chr 1); NLRP1 (chr 17); NLRP12, 2, 9, 13, 8 and 5 (chr 19); NLRP6, NLRP14 and 10 (chr 11). The mouse: Nlrp3, 1a, 1b and 1c (chr 11); Nlrp12, 2, 4c, 4d, 4b, 9b, 4e, 5, 9c, 4a, 9a, 14, 10 and 6 (chr 7).
Mentions: Moreover, this reproduction-related clade is also supported by the syntenic analysis (Figure 2). In the human genome, all the reproduction-related NLRP genes, except for NLRP14, are tandemly located on the chromosome 19q13.42, suggesting that multiple tandem duplication events might have given birth to these genes. The similar arrangements of the reproduction-related NLRPs are also found in cattle and dog genomes (Figure 2). In the mouse genome, the reproduction-related Nlrps (except for Nlrp14) are not located side by side, but interrupted by some other types of genes, especially and mainly by certain V1r genes (discussed below) on chromosome 7A1 and 7A3. Although NLRP14 is not located in the syntenic region encompassing other reproduction-related NLRPs in all the studied mammalian genomes (involving cattle, dog, human, chimpanzee, mouse and rat), our phylogenetic result and the published expression profile show that this gene is close to other reproduction-related NLRPs. This suggests that early (before the divergence of mammals) genomic rearrangements might have resulted in the separation of NLRP14 from its relatives.

Bottom Line: The aim of the present work was to study how these genes evolved and diverged after their duplication, as well as whether natural selection played a role during their evolution.In conclusion, this study brings us novel information on the evolution of mammalian reproduction-related NLRPs.On the one hand, NLRP genes duplicated and functionally diversified in mammalian reproductive systems (such as NLRP4, 5, 9 and 14).

View Article: PubMed Central - HTML - PubMed

Affiliation: Physiologie de la Reproduction et des Comportements, UMR 6175 INRA-CNRS-Université François Rabelais de Tours-Haras Nationaux, 37380 Nouzilly, France. xin.savois@tours.inra.fr

ABSTRACT

Background: NLRPs (Nucleotide-binding oligomerization domain, Leucine rich Repeat and Pyrin domain containing Proteins) are members of NLR (Nod-like receptors) protein family. Recent researches have shown that NLRP genes play important roles in both mammalian innate immune system and reproductive system. Several of NLRP genes were shown to be specifically expressed in the oocyte in mammals. The aim of the present work was to study how these genes evolved and diverged after their duplication, as well as whether natural selection played a role during their evolution.

Results: By using in silico methods, we have evaluated the evolution and functional divergence of NLRP genes, in particular of mouse reproduction-related Nlrp genes. We found that (1) major NLRP genes have been duplicated before the divergence of mammals, with certain lineage-specific duplications in primates (NLRP7 and 11) and in rodents (Nlrp1, 4 and 9 duplicates); (2) tandem duplication events gave rise to a mammalian reproduction-related NLRP cluster including NLRP2, 4, 5, 7, 8, 9, 11, 13 and 14 genes; (3) the function of mammalian oocyte-specific NLRP genes (NLRP4, 5, 9 and 14) might have diverged during gene evolution; (4) recent segmental duplications concerning Nlrp4 copies and vomeronasal 1 receptor encoding genes (V1r) have been undertaken in the mouse; and (5) duplicates of Nlrp4 and 9 in the mouse might have been subjected to adaptive evolution.

Conclusion: In conclusion, this study brings us novel information on the evolution of mammalian reproduction-related NLRPs. On the one hand, NLRP genes duplicated and functionally diversified in mammalian reproductive systems (such as NLRP4, 5, 9 and 14). On the other hand, during evolution, different lineages adapted to develop their own NLRP genes, particularly in reproductive function (such as the specific expansion of Nlrp4 and Nlrp9 in the mouse).

Show MeSH