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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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tat-4 reporter expression pattern. The 5' end of the tat-4 locus, location of the deleted region in tm1801 mutants (bar) and structure of the tat-4 expression cassette (A). Reporter expression in the pharyngeal-intestinal valve, intestine and rectal gland cells in 3-fold embryos (B) and in advanced stage larvae (C and D) in the lcIs911.30 line. GFP fluorescence in the uterus (E), during spermatogenesis (F) and in the spermatheca of previously ovulated hermaphrodites (G) in lcIs911.30 animals. Abbreviations: pv – pharyngeal-intestinal valve; r – rectum; rgc – rectal gland cells; sp – spermatheca.
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Figure 6: tat-4 reporter expression pattern. The 5' end of the tat-4 locus, location of the deleted region in tm1801 mutants (bar) and structure of the tat-4 expression cassette (A). Reporter expression in the pharyngeal-intestinal valve, intestine and rectal gland cells in 3-fold embryos (B) and in advanced stage larvae (C and D) in the lcIs911.30 line. GFP fluorescence in the uterus (E), during spermatogenesis (F) and in the spermatheca of previously ovulated hermaphrodites (G) in lcIs911.30 animals. Abbreviations: pv – pharyngeal-intestinal valve; r – rectum; rgc – rectal gland cells; sp – spermatheca.

Mentions: Four integrated and six extrachromosomal tat-4::nls::gfp transgenic lines were derived (Figure 6A). Five of these lines (2 integrated and 3 extrachromosomal) were investigated in detail. Notable tat-4 reporter expression begins in 2–3 fold embryos in the developing pharyngeal-intestinal valve and unidentified cells at the posterior (Figure 6B). In the fully formed alimentary system, GFP fluorescence emanates strongly from the pharyngeal-intestinal valve, rectal gland cells and the intestine (Figure 6C and 6D). tat-4 reporter is also expressed in the uterus, during spermatogenesis in the proximal gonad and in the spermatheca of previously ovulated adults (Figure 6E–6G).


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)

tat-4 reporter expression pattern. The 5' end of the tat-4 locus, location of the deleted region in tm1801 mutants (bar) and structure of the tat-4 expression cassette (A). Reporter expression in the pharyngeal-intestinal valve, intestine and rectal gland cells in 3-fold embryos (B) and in advanced stage larvae (C and D) in the lcIs911.30 line. GFP fluorescence in the uterus (E), during spermatogenesis (F) and in the spermatheca of previously ovulated hermaphrodites (G) in lcIs911.30 animals. Abbreviations: pv – pharyngeal-intestinal valve; r – rectum; rgc – rectal gland cells; sp – spermatheca.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: tat-4 reporter expression pattern. The 5' end of the tat-4 locus, location of the deleted region in tm1801 mutants (bar) and structure of the tat-4 expression cassette (A). Reporter expression in the pharyngeal-intestinal valve, intestine and rectal gland cells in 3-fold embryos (B) and in advanced stage larvae (C and D) in the lcIs911.30 line. GFP fluorescence in the uterus (E), during spermatogenesis (F) and in the spermatheca of previously ovulated hermaphrodites (G) in lcIs911.30 animals. Abbreviations: pv – pharyngeal-intestinal valve; r – rectum; rgc – rectal gland cells; sp – spermatheca.
Mentions: Four integrated and six extrachromosomal tat-4::nls::gfp transgenic lines were derived (Figure 6A). Five of these lines (2 integrated and 3 extrachromosomal) were investigated in detail. Notable tat-4 reporter expression begins in 2–3 fold embryos in the developing pharyngeal-intestinal valve and unidentified cells at the posterior (Figure 6B). In the fully formed alimentary system, GFP fluorescence emanates strongly from the pharyngeal-intestinal valve, rectal gland cells and the intestine (Figure 6C and 6D). tat-4 reporter is also expressed in the uterus, during spermatogenesis in the proximal gonad and in the spermatheca of previously ovulated adults (Figure 6E–6G).

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