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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-5 is a housekeeping gene. The 5' end of the tat-5 locus and structure of the two tat-5 expression cassettes (A). Expression of tat-5b::nls::gfp in the lcIs481.4 line in embryos (B and C) and a head region of an adult (D), and in the lcEx481.2 isolate at the head-intestine junction (E) and in a developing somatic gonad (F). Necrotic death of tat-5(RNAi) embryos (G). Abbreviations: DTC – distal tip cell; in – intestinal nucleus; sg – somatic gonad.
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Figure 3: tat-5 is a housekeeping gene. The 5' end of the tat-5 locus and structure of the two tat-5 expression cassettes (A). Expression of tat-5b::nls::gfp in the lcIs481.4 line in embryos (B and C) and a head region of an adult (D), and in the lcEx481.2 isolate at the head-intestine junction (E) and in a developing somatic gonad (F). Necrotic death of tat-5(RNAi) embryos (G). Abbreviations: DTC – distal tip cell; in – intestinal nucleus; sg – somatic gonad.

Mentions: Three alternative transcripts of tat-5 were detected. tat-5b begins with the sequence from the two short exons located in a close proximity to the upstream ORF and undergoes trans-splicing to SL2 (Figure 3A). tat-5a and tat-5c are almost identical to each other, start with the third exon located over 3 kilobases downstream from the first two tat-5b exons and are spliced to SL1 and SL2. In addition to trans-splicing to SL2, subordinate cistrons in an operon also usually reside close to the previous ORF [19]. By these two criteria, tat-5b is a subordinate cistron in an operon. The status of tat-5a/c is less certain. The long sequence from the end of the previous ORF to the start of tat-5a/c transcripts could conceivably hold another (in addition to the operon promoter) cis-acting regulatory element that drives transcription of these two isoforms.


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-5 is a housekeeping gene. The 5' end of the tat-5 locus and structure of the two tat-5 expression cassettes (A). Expression of tat-5b::nls::gfp in the lcIs481.4 line in embryos (B and C) and a head region of an adult (D), and in the lcEx481.2 isolate at the head-intestine junction (E) and in a developing somatic gonad (F). Necrotic death of tat-5(RNAi) embryos (G). Abbreviations: DTC – distal tip cell; in – intestinal nucleus; sg – somatic gonad.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: tat-5 is a housekeeping gene. The 5' end of the tat-5 locus and structure of the two tat-5 expression cassettes (A). Expression of tat-5b::nls::gfp in the lcIs481.4 line in embryos (B and C) and a head region of an adult (D), and in the lcEx481.2 isolate at the head-intestine junction (E) and in a developing somatic gonad (F). Necrotic death of tat-5(RNAi) embryos (G). Abbreviations: DTC – distal tip cell; in – intestinal nucleus; sg – somatic gonad.
Mentions: Three alternative transcripts of tat-5 were detected. tat-5b begins with the sequence from the two short exons located in a close proximity to the upstream ORF and undergoes trans-splicing to SL2 (Figure 3A). tat-5a and tat-5c are almost identical to each other, start with the third exon located over 3 kilobases downstream from the first two tat-5b exons and are spliced to SL1 and SL2. In addition to trans-splicing to SL2, subordinate cistrons in an operon also usually reside close to the previous ORF [19]. By these two criteria, tat-5b is a subordinate cistron in an operon. The status of tat-5a/c is less certain. The long sequence from the end of the previous ORF to the start of tat-5a/c transcripts could conceivably hold another (in addition to the operon promoter) cis-acting regulatory element that drives transcription of these two isoforms.

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