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An unexpectedly high degree of specialization and a widespread involvement in sterol metabolism among the C. elegans putative aminophospholipid translocases.

Lyssenko NN, Miteva Y, Gilroy S, Hanna-Rose W, Schlegel RA - BMC Dev. Biol. (2008)

Bottom Line: Strong expression of both tat-2 and tat-4 occurs in the intestine and certain other cells of the alimentary system.Although individually dispensable, tat-1 through 4 seem to be at most only partly redundant.These findings uncover an unexpectedly high degree of specialization and a widespread involvement in sterol metabolism among the genes encoding the putative aminophospholipid translocases.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania 16802, USA. lyssenn@ccf.org

ABSTRACT

Background: P-type ATPases in subfamily IV are exclusively eukaryotic transmembrane proteins that have been proposed to directly translocate the aminophospholipids phosphatidylserine and phosphatidylethanolamine from the exofacial to the cytofacial monolayer of the plasma membrane. Eukaryotic genomes contain many genes encoding members of this subfamily. At present it is unclear why there are so many genes of this kind per organism or what individual roles these genes perform in organism development.

Results: We have systematically investigated expression and developmental function of the six, tat-1 through 6, subfamily IV P-type ATPase genes encoded in the Caenorhabditis elegans genome. tat-5 is the only ubiquitously-expressed essential gene in the group. tat-6 is a poorly-transcribed recent duplicate of tat-5. tat-2 through 4 exhibit tissue-specific developmentally-regulated expression patterns. Strong expression of both tat-2 and tat-4 occurs in the intestine and certain other cells of the alimentary system. The two are also expressed in the uterus, during spermatogenesis and in the fully-formed spermatheca. tat-2 alone is expressed in the pharyngeal gland cells, the excretory system and a few cells of the developing vulva. The expression pattern of tat-3 is almost completely different from those of tat-2 and tat-4. tat-3 expression is detectable in the steroidogenic tissues: the hypodermis and the XXX cells, as well as in most cells of the pharynx (except gland), various tissues of the reproductive system (except uterus and spermatheca) and seam cells. Deletion of tat-1 through 4 individually interferes little or not at all with the regular progression of organism growth and development under normal conditions. However, tat-2 through 4 become essential for reproductive growth during sterol starvation.

Conclusion: tat-5 likely encodes a housekeeping protein that performs the proposed aminophospholipid translocase function routinely. Although individually dispensable, tat-1 through 4 seem to be at most only partly redundant. Expression patterns and the sterol deprivation hypersensitivity deletion phenotype of tat-2 through 4 suggest that these genes carry out subtle metabolic functions, such as fine-tuning sterol metabolism in digestive or steroidogenic tissues. These findings uncover an unexpectedly high degree of specialization and a widespread involvement in sterol metabolism among the genes encoding the putative aminophospholipid translocases.

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A phylogenetic tree of S. cerevisiae, C. elegans and human P-type ATPases in subfamily IV. The tree was assembled using ClustalW2 [48]. The outgroup is a Drosophila melanogaster calcium-transporting P-type ATPase.
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Figure 2: A phylogenetic tree of S. cerevisiae, C. elegans and human P-type ATPases in subfamily IV. The tree was assembled using ClustalW2 [48]. The outgroup is a Drosophila melanogaster calcium-transporting P-type ATPase.

Mentions: P-type ATPases in subfamily IV are customarily divided into six classes [13]. A phylogenetic analysis of these ATPases expressed in S. cerevisiae, C. elegans and humans reveals a substantial evolutionary dissimilarity between class 2 and the other classes (Figure 2). After the early split between the branch leading to class 2 and the branch leading to the rest of the classes, class 2 genes have not duplicated significantly. Thus, yeast express a single gene in this class (NEO1), while C. elegans and humans express two class 2 genes each (tat-5 and tat-6 in the nematode). The other branch of the subfamily, in contrast, has quickly undergone multiplication and diversification. This difference in the extent of evolutionary expansion may indicate that the strictly preserved class 2 proteins perform some essential function conserved throughout evolution in all eukaryotes, while the frequently duplicating ATPases in the other classes rapidly evolve to fill new roles.


An unexpectedly high degree of specialization and a widespread involvement in sterol metabolism among the C. elegans putative aminophospholipid translocases.

Lyssenko NN, Miteva Y, Gilroy S, Hanna-Rose W, Schlegel RA - BMC Dev. Biol. (2008)

A phylogenetic tree of S. cerevisiae, C. elegans and human P-type ATPases in subfamily IV. The tree was assembled using ClustalW2 [48]. The outgroup is a Drosophila melanogaster calcium-transporting P-type ATPase.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2572054&req=5

Figure 2: A phylogenetic tree of S. cerevisiae, C. elegans and human P-type ATPases in subfamily IV. The tree was assembled using ClustalW2 [48]. The outgroup is a Drosophila melanogaster calcium-transporting P-type ATPase.
Mentions: P-type ATPases in subfamily IV are customarily divided into six classes [13]. A phylogenetic analysis of these ATPases expressed in S. cerevisiae, C. elegans and humans reveals a substantial evolutionary dissimilarity between class 2 and the other classes (Figure 2). After the early split between the branch leading to class 2 and the branch leading to the rest of the classes, class 2 genes have not duplicated significantly. Thus, yeast express a single gene in this class (NEO1), while C. elegans and humans express two class 2 genes each (tat-5 and tat-6 in the nematode). The other branch of the subfamily, in contrast, has quickly undergone multiplication and diversification. This difference in the extent of evolutionary expansion may indicate that the strictly preserved class 2 proteins perform some essential function conserved throughout evolution in all eukaryotes, while the frequently duplicating ATPases in the other classes rapidly evolve to fill new roles.

Bottom Line: Strong expression of both tat-2 and tat-4 occurs in the intestine and certain other cells of the alimentary system.Although individually dispensable, tat-1 through 4 seem to be at most only partly redundant.These findings uncover an unexpectedly high degree of specialization and a widespread involvement in sterol metabolism among the genes encoding the putative aminophospholipid translocases.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania 16802, USA. lyssenn@ccf.org

ABSTRACT

Background: P-type ATPases in subfamily IV are exclusively eukaryotic transmembrane proteins that have been proposed to directly translocate the aminophospholipids phosphatidylserine and phosphatidylethanolamine from the exofacial to the cytofacial monolayer of the plasma membrane. Eukaryotic genomes contain many genes encoding members of this subfamily. At present it is unclear why there are so many genes of this kind per organism or what individual roles these genes perform in organism development.

Results: We have systematically investigated expression and developmental function of the six, tat-1 through 6, subfamily IV P-type ATPase genes encoded in the Caenorhabditis elegans genome. tat-5 is the only ubiquitously-expressed essential gene in the group. tat-6 is a poorly-transcribed recent duplicate of tat-5. tat-2 through 4 exhibit tissue-specific developmentally-regulated expression patterns. Strong expression of both tat-2 and tat-4 occurs in the intestine and certain other cells of the alimentary system. The two are also expressed in the uterus, during spermatogenesis and in the fully-formed spermatheca. tat-2 alone is expressed in the pharyngeal gland cells, the excretory system and a few cells of the developing vulva. The expression pattern of tat-3 is almost completely different from those of tat-2 and tat-4. tat-3 expression is detectable in the steroidogenic tissues: the hypodermis and the XXX cells, as well as in most cells of the pharynx (except gland), various tissues of the reproductive system (except uterus and spermatheca) and seam cells. Deletion of tat-1 through 4 individually interferes little or not at all with the regular progression of organism growth and development under normal conditions. However, tat-2 through 4 become essential for reproductive growth during sterol starvation.

Conclusion: tat-5 likely encodes a housekeeping protein that performs the proposed aminophospholipid translocase function routinely. Although individually dispensable, tat-1 through 4 seem to be at most only partly redundant. Expression patterns and the sterol deprivation hypersensitivity deletion phenotype of tat-2 through 4 suggest that these genes carry out subtle metabolic functions, such as fine-tuning sterol metabolism in digestive or steroidogenic tissues. These findings uncover an unexpectedly high degree of specialization and a widespread involvement in sterol metabolism among the genes encoding the putative aminophospholipid translocases.

Show MeSH
Related in: MedlinePlus