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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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Reproduction of mutant and N2 nematodes under regular growth conditions (n = 10 to 12 animals; statistical analysis performed using ANOVA; error bars are standard deviations).
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Figure 7: Reproduction of mutant and N2 nematodes under regular growth conditions (n = 10 to 12 animals; statistical analysis performed using ANOVA; error bars are standard deviations).

Mentions: To determine whether deletion of tat-2 through 4 exerts a negative effect on nematode growth and reproduction, synchronized mutant and N2 larvae were followed through developmental stages, and the viable progeny of the adult hermaphrodites were counted. Wild-type, tat-3(tm1275), tat-4(tm1801) and tat-4(tm1801); tat-3(tm1275) animals were essentially indistinguishable from one another in both the timing of progression through the developmental stages and the number of viable progeny produced by hermaphrodites (Figure 7). tat-2(tm1634) mutants passed through development slightly slower than un-mutated larvae. This is evident in the lower and higher number of tat-2(tm1634) offspring produced during, respectively, the first and the last sampling period, in comparison with the numbers of N2 progeny. Around 20% (n = 10) of tat-2(tm1773) hermaphrodites had notably fewer progeny than the rest of animals of the same genotype. This is reflected in the large standard deviation value for this mutant. However, pair-wise statistical analysis (ANOVA) shows that the total number of viable hatchlings for neither tat-2(tm1634) nor tat-2(tm1773) mutants was significantly different from the corresponding number for N2 animals (P = 0.22 and P = 0.30, respectively). Overall, deletion of tat-1, tat-2, tat-3 or tat-4 individually and tat-3 and tat-4 together does not seem to impair nematode development or reproduction to a significant degree under regular growth conditions.


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)

Reproduction of mutant and N2 nematodes under regular growth conditions (n = 10 to 12 animals; statistical analysis performed using ANOVA; error bars are standard deviations).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 7: Reproduction of mutant and N2 nematodes under regular growth conditions (n = 10 to 12 animals; statistical analysis performed using ANOVA; error bars are standard deviations).
Mentions: To determine whether deletion of tat-2 through 4 exerts a negative effect on nematode growth and reproduction, synchronized mutant and N2 larvae were followed through developmental stages, and the viable progeny of the adult hermaphrodites were counted. Wild-type, tat-3(tm1275), tat-4(tm1801) and tat-4(tm1801); tat-3(tm1275) animals were essentially indistinguishable from one another in both the timing of progression through the developmental stages and the number of viable progeny produced by hermaphrodites (Figure 7). tat-2(tm1634) mutants passed through development slightly slower than un-mutated larvae. This is evident in the lower and higher number of tat-2(tm1634) offspring produced during, respectively, the first and the last sampling period, in comparison with the numbers of N2 progeny. Around 20% (n = 10) of tat-2(tm1773) hermaphrodites had notably fewer progeny than the rest of animals of the same genotype. This is reflected in the large standard deviation value for this mutant. However, pair-wise statistical analysis (ANOVA) shows that the total number of viable hatchlings for neither tat-2(tm1634) nor tat-2(tm1773) mutants was significantly different from the corresponding number for N2 animals (P = 0.22 and P = 0.30, respectively). Overall, deletion of tat-1, tat-2, tat-3 or tat-4 individually and tat-3 and tat-4 together does not seem to impair nematode development or reproduction to a significant degree under regular growth conditions.

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