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The ubiquilin gene family: evolutionary patterns and functional insights.

Marín I - BMC Evol. Biol. (2014)

Bottom Line: This exceptional mammalian-specific expansion is the result of the recent emergence of four new genes, three of them (UBQLN3, UBQLN5 and UBQLNL) with precise testis-specific expression patterns that indicate roles in the postmeiotic stages of spermatogenesis.The ubiquilin gene family is highly conserved in eukaryotes.The infrequent lineage-specific amplifications observed may be linked to the emergence of novel functions in particular tissues.

View Article: PubMed Central - HTML - PubMed

Affiliation: Instituto de Biomedicina de Valencia, Consejo Superior de Investigaciones Científicas (IBV-CSIC), Valencia, Spain. imarin@ibv.csic.es.

ABSTRACT

Background: Ubiquilins are proteins that function as ubiquitin receptors in eukaryotes. Mutations in two ubiquilin-encoding genes have been linked to the genesis of neurodegenerative diseases. However, ubiquilin functions are still poorly understood.

Results: In this study, evolutionary and functional data are combined to determine the origin and diversification of the ubiquilin gene family and to characterize novel potential roles of ubiquilins in mammalian species, including humans. The analysis of more than six hundred sequences allowed characterizing ubiquilin diversity in all the main eukaryotic groups. Many organisms (e. g. fungi, many animals) have single ubiquilin genes, but duplications in animal, plant, alveolate and excavate species are described. Seven different ubiquilins have been detected in vertebrates. Two of them, here called UBQLN5 and UBQLN6, had not been hitherto described. Significantly, marsupial and eutherian mammals have the most complex ubiquilin gene families, composed of up to 6 genes. This exceptional mammalian-specific expansion is the result of the recent emergence of four new genes, three of them (UBQLN3, UBQLN5 and UBQLNL) with precise testis-specific expression patterns that indicate roles in the postmeiotic stages of spermatogenesis. A gene with related features has independently arisen in species of the Drosophila genus. Positive selection acting on some mammalian ubiquilins has been detected.

Conclusions: The ubiquilin gene family is highly conserved in eukaryotes. The infrequent lineage-specific amplifications observed may be linked to the emergence of novel functions in particular tissues.

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Related in: MedlinePlus

Ubiquilin gene expression in different organs, tissues or cell types of wild-type mice. Data, in arbitrary expression units, obtained from the BioGPS database [57]. The key names of the samples used in BioGPS are indicated. Although most names are autoexplicative, additional details of these samples can be found at http://www.biogps.org. Notice the qualitative difference found for testis respect to the other samples. In testis, most of the expression observed derives from UBQLNL group genes (UBQLN3, UBQLN5, UBQLNL) which are not expressed, or at very low levels, in all other tissues.
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Figure 6: Ubiquilin gene expression in different organs, tissues or cell types of wild-type mice. Data, in arbitrary expression units, obtained from the BioGPS database [57]. The key names of the samples used in BioGPS are indicated. Although most names are autoexplicative, additional details of these samples can be found at http://www.biogps.org. Notice the qualitative difference found for testis respect to the other samples. In testis, most of the expression observed derives from UBQLNL group genes (UBQLN3, UBQLN5, UBQLNL) which are not expressed, or at very low levels, in all other tissues.

Mentions: The results in the previous two sections established that the rapid amplification of the ubiquilin gene family detected in mammals is the largest observed in any eukaryotic lineage. We may now ask for the potential roles of this novel ubiquilins that may contribute to explain such amplification. I decided to explore the available human and mouse expression data to obtain information about the potential functional roles of each ubiquilin in vertebrates. Tables 1 and Figures 6 and 7 summarize the expression data for multiple organs, tissues or cell types in, respectively, normal mice and humans. They were obtained from the last version of the Gene Atlas database available at BioGPS [57]. In Table 1 (left), I have included the details of the five mouse samples (tissues, organs or cell types) that had either the highest or the lowest levels of expression for UBQLN1, UBQLN2 and UBLQN4. For the other three ubiquilin genes present in mouse (UBQLN3, UBQLN5 and UBQLNL), only the five samples with the highest levels of expression are indicated, given that the values in most other samples are effectively not different from zero. The same is done for human ubiquilin genes on the right panels of Table 1. No data are indicated for UBQLN5 given that it is absent in our species.


The ubiquilin gene family: evolutionary patterns and functional insights.

Marín I - BMC Evol. Biol. (2014)

Ubiquilin gene expression in different organs, tissues or cell types of wild-type mice. Data, in arbitrary expression units, obtained from the BioGPS database [57]. The key names of the samples used in BioGPS are indicated. Although most names are autoexplicative, additional details of these samples can be found at http://www.biogps.org. Notice the qualitative difference found for testis respect to the other samples. In testis, most of the expression observed derives from UBQLNL group genes (UBQLN3, UBQLN5, UBQLNL) which are not expressed, or at very low levels, in all other tissues.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4230246&req=5

Figure 6: Ubiquilin gene expression in different organs, tissues or cell types of wild-type mice. Data, in arbitrary expression units, obtained from the BioGPS database [57]. The key names of the samples used in BioGPS are indicated. Although most names are autoexplicative, additional details of these samples can be found at http://www.biogps.org. Notice the qualitative difference found for testis respect to the other samples. In testis, most of the expression observed derives from UBQLNL group genes (UBQLN3, UBQLN5, UBQLNL) which are not expressed, or at very low levels, in all other tissues.
Mentions: The results in the previous two sections established that the rapid amplification of the ubiquilin gene family detected in mammals is the largest observed in any eukaryotic lineage. We may now ask for the potential roles of this novel ubiquilins that may contribute to explain such amplification. I decided to explore the available human and mouse expression data to obtain information about the potential functional roles of each ubiquilin in vertebrates. Tables 1 and Figures 6 and 7 summarize the expression data for multiple organs, tissues or cell types in, respectively, normal mice and humans. They were obtained from the last version of the Gene Atlas database available at BioGPS [57]. In Table 1 (left), I have included the details of the five mouse samples (tissues, organs or cell types) that had either the highest or the lowest levels of expression for UBQLN1, UBQLN2 and UBLQN4. For the other three ubiquilin genes present in mouse (UBQLN3, UBQLN5 and UBQLNL), only the five samples with the highest levels of expression are indicated, given that the values in most other samples are effectively not different from zero. The same is done for human ubiquilin genes on the right panels of Table 1. No data are indicated for UBQLN5 given that it is absent in our species.

Bottom Line: This exceptional mammalian-specific expansion is the result of the recent emergence of four new genes, three of them (UBQLN3, UBQLN5 and UBQLNL) with precise testis-specific expression patterns that indicate roles in the postmeiotic stages of spermatogenesis.The ubiquilin gene family is highly conserved in eukaryotes.The infrequent lineage-specific amplifications observed may be linked to the emergence of novel functions in particular tissues.

View Article: PubMed Central - HTML - PubMed

Affiliation: Instituto de Biomedicina de Valencia, Consejo Superior de Investigaciones Científicas (IBV-CSIC), Valencia, Spain. imarin@ibv.csic.es.

ABSTRACT

Background: Ubiquilins are proteins that function as ubiquitin receptors in eukaryotes. Mutations in two ubiquilin-encoding genes have been linked to the genesis of neurodegenerative diseases. However, ubiquilin functions are still poorly understood.

Results: In this study, evolutionary and functional data are combined to determine the origin and diversification of the ubiquilin gene family and to characterize novel potential roles of ubiquilins in mammalian species, including humans. The analysis of more than six hundred sequences allowed characterizing ubiquilin diversity in all the main eukaryotic groups. Many organisms (e. g. fungi, many animals) have single ubiquilin genes, but duplications in animal, plant, alveolate and excavate species are described. Seven different ubiquilins have been detected in vertebrates. Two of them, here called UBQLN5 and UBQLN6, had not been hitherto described. Significantly, marsupial and eutherian mammals have the most complex ubiquilin gene families, composed of up to 6 genes. This exceptional mammalian-specific expansion is the result of the recent emergence of four new genes, three of them (UBQLN3, UBQLN5 and UBQLNL) with precise testis-specific expression patterns that indicate roles in the postmeiotic stages of spermatogenesis. A gene with related features has independently arisen in species of the Drosophila genus. Positive selection acting on some mammalian ubiquilins has been detected.

Conclusions: The ubiquilin gene family is highly conserved in eukaryotes. The infrequent lineage-specific amplifications observed may be linked to the emergence of novel functions in particular tissues.

Show MeSH
Related in: MedlinePlus