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Examination of the genetic basis for sexual dimorphism in the Aedes aegypti (dengue vector mosquito) pupal brain.

Tomchaney M, Mysore K, Sun L, Li P, Emrich SJ, Severson DW, Duman-Scheel M - Biol Sex Differ (2014)

Bottom Line: Transcripts (2,527), many of which were linked to proteolysis, the proteasome, metabolism, catabolic, and biosynthetic processes, ion transport, cell growth, and proliferation, were found to be differentially expressed in A. aegypti female vs. male pupal heads.Sex-specific differences in gene expression were also detected in the antennal lobe and mushroom body. siRNA-mediated gene targeting experiments demonstrated that Doublesex, a transcription factor with consensus binding sites located adjacent to many dimorphically expressed transcripts that function in neural development, is required for regulation of sex-specific gene expression in the developing A. aegypti brain.These studies revealed sex-specific gene expression profiles in the developing A. aegypti pupal head and identified Doublesex as a key regulator of sexually dimorphic gene expression during mosquito neural development.

View Article: PubMed Central - HTML - PubMed

Affiliation: Eck Institute for Global Health, Galvin Life Sciences, University of Notre Dame, Notre Dame 46556, IN, USA ; Department of Biological Sciences, Galvin Life Sciences, University of Notre Dame, Notre Dame 46556, IN, USA.

ABSTRACT

Background: Most animal species exhibit sexually dimorphic behaviors, many of which are linked to reproduction. A number of these behaviors, including blood feeding in female mosquitoes, contribute to the global spread of vector-borne illnesses. However, knowledge concerning the genetic basis of sexually dimorphic traits is limited in any organism, including mosquitoes, especially with respect to differences in the developing nervous system.

Methods: Custom microarrays were used to examine global differences in female vs. male gene expression in the developing pupal head of the dengue vector mosquito, Aedes aegypti. The spatial expression patterns of a subset of differentially expressed transcripts were examined in the developing female vs. male pupal brain through in situ hybridization experiments. Small interfering RNA (siRNA)-mediated knockdown studies were used to assess the putative role of Doublesex, a terminal component of the sex determination pathway, in the regulation of sex-specific gene expression observed in the developing pupal brain.

Results: Transcripts (2,527), many of which were linked to proteolysis, the proteasome, metabolism, catabolic, and biosynthetic processes, ion transport, cell growth, and proliferation, were found to be differentially expressed in A. aegypti female vs. male pupal heads. Analysis of the spatial expression patterns for a subset of dimorphically expressed genes in the pupal brain validated the data set and also facilitated the identification of brain regions with dimorphic gene expression. In many cases, dimorphic gene expression localized to the optic lobe. Sex-specific differences in gene expression were also detected in the antennal lobe and mushroom body. siRNA-mediated gene targeting experiments demonstrated that Doublesex, a transcription factor with consensus binding sites located adjacent to many dimorphically expressed transcripts that function in neural development, is required for regulation of sex-specific gene expression in the developing A. aegypti brain.

Conclusions: These studies revealed sex-specific gene expression profiles in the developing A. aegypti pupal head and identified Doublesex as a key regulator of sexually dimorphic gene expression during mosquito neural development.

No MeSH data available.


Related in: MedlinePlus

Sex-specific expression patterns of DETs in sectionedA. aegyptipupal brains. Differential expression of cdk4/6(A, E), geko(B, F), synj(C, G), and p53(D, H) was detected in 12 μ sections through 24 hr female (A-D) and male (E-H) pupal brains. Hemisegments oriented dorsal upward are shown. Hybridizations with a sense control probe detected no signal in comparable brain sections (not shown). cdk4/6 is commonly expressed in the optic lobe (blue arrowheads in A, E), but males have an additional cdk4/6 expression domain in the ventral suboesophageal ganglion (red arrowhead in E). geko, which is commonly expressed in the female and male optic lobe (blue arrowheads in B, F), is expressed in additional large cell bodies near the female midbrain and antennal lobe (red arrowheads in B). synj expression is detected in the optic lobe (blue arrowheads in C, G) and in a subset of midbrain neurons (red arrowheads in C, G). The red arrowhead in G marks sex-specific synj optic lobe expression in males, and midbrain synj levels are generally higher in males (compare expression adjacent to red arrowheads in C, G). p53 is expressed in the optic lobe and suboesophageal ganglion of females (blue and red arrowheads, respectively in D). p53 is also expressed in the male optic lobe (blue arrowheads in H), but not in the male subesophageal ganglion (H). Male-specific p53 expression is detected in neurons adjacent to the antennal lobe (red arrowheads in H). These data are consistent with the results presented in Figure 7. al antennal lobe, la lamina, me medulla, SuEG, supraesophageal ganglion.
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Figure 6: Sex-specific expression patterns of DETs in sectionedA. aegyptipupal brains. Differential expression of cdk4/6(A, E), geko(B, F), synj(C, G), and p53(D, H) was detected in 12 μ sections through 24 hr female (A-D) and male (E-H) pupal brains. Hemisegments oriented dorsal upward are shown. Hybridizations with a sense control probe detected no signal in comparable brain sections (not shown). cdk4/6 is commonly expressed in the optic lobe (blue arrowheads in A, E), but males have an additional cdk4/6 expression domain in the ventral suboesophageal ganglion (red arrowhead in E). geko, which is commonly expressed in the female and male optic lobe (blue arrowheads in B, F), is expressed in additional large cell bodies near the female midbrain and antennal lobe (red arrowheads in B). synj expression is detected in the optic lobe (blue arrowheads in C, G) and in a subset of midbrain neurons (red arrowheads in C, G). The red arrowhead in G marks sex-specific synj optic lobe expression in males, and midbrain synj levels are generally higher in males (compare expression adjacent to red arrowheads in C, G). p53 is expressed in the optic lobe and suboesophageal ganglion of females (blue and red arrowheads, respectively in D). p53 is also expressed in the male optic lobe (blue arrowheads in H), but not in the male subesophageal ganglion (H). Male-specific p53 expression is detected in neurons adjacent to the antennal lobe (red arrowheads in H). These data are consistent with the results presented in Figure 7. al antennal lobe, la lamina, me medulla, SuEG, supraesophageal ganglion.

Mentions: For many of the genes analyzed, dimorphic expression localized to the optic lobe of the brain. For example, takeout, ci, obp10, arrow, and caspase 7 (Figure 4A,B,D,E,F, respectively) are upregulated in the female optic lobes with respect to males in which little if any transcripts were detected through in situ hybridization. Expression of obp13 is upregulated in the male optic lobe with respect to females (Figure 4J). To be certain that this intense optic lobe staining was not an artifact of the tissue preparation or whole mount in situ hybridization process, we confirmed that negative sense control probes gave little background staining in the optic lobes or in other regions of the brain (Figure 4K). We also confirmed optic lobe expression for a number of DETs by performing in situ hybridization experiments on sectioned brain tissues (Figure 6).


Examination of the genetic basis for sexual dimorphism in the Aedes aegypti (dengue vector mosquito) pupal brain.

Tomchaney M, Mysore K, Sun L, Li P, Emrich SJ, Severson DW, Duman-Scheel M - Biol Sex Differ (2014)

Sex-specific expression patterns of DETs in sectionedA. aegyptipupal brains. Differential expression of cdk4/6(A, E), geko(B, F), synj(C, G), and p53(D, H) was detected in 12 μ sections through 24 hr female (A-D) and male (E-H) pupal brains. Hemisegments oriented dorsal upward are shown. Hybridizations with a sense control probe detected no signal in comparable brain sections (not shown). cdk4/6 is commonly expressed in the optic lobe (blue arrowheads in A, E), but males have an additional cdk4/6 expression domain in the ventral suboesophageal ganglion (red arrowhead in E). geko, which is commonly expressed in the female and male optic lobe (blue arrowheads in B, F), is expressed in additional large cell bodies near the female midbrain and antennal lobe (red arrowheads in B). synj expression is detected in the optic lobe (blue arrowheads in C, G) and in a subset of midbrain neurons (red arrowheads in C, G). The red arrowhead in G marks sex-specific synj optic lobe expression in males, and midbrain synj levels are generally higher in males (compare expression adjacent to red arrowheads in C, G). p53 is expressed in the optic lobe and suboesophageal ganglion of females (blue and red arrowheads, respectively in D). p53 is also expressed in the male optic lobe (blue arrowheads in H), but not in the male subesophageal ganglion (H). Male-specific p53 expression is detected in neurons adjacent to the antennal lobe (red arrowheads in H). These data are consistent with the results presented in Figure 7. al antennal lobe, la lamina, me medulla, SuEG, supraesophageal ganglion.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4342991&req=5

Figure 6: Sex-specific expression patterns of DETs in sectionedA. aegyptipupal brains. Differential expression of cdk4/6(A, E), geko(B, F), synj(C, G), and p53(D, H) was detected in 12 μ sections through 24 hr female (A-D) and male (E-H) pupal brains. Hemisegments oriented dorsal upward are shown. Hybridizations with a sense control probe detected no signal in comparable brain sections (not shown). cdk4/6 is commonly expressed in the optic lobe (blue arrowheads in A, E), but males have an additional cdk4/6 expression domain in the ventral suboesophageal ganglion (red arrowhead in E). geko, which is commonly expressed in the female and male optic lobe (blue arrowheads in B, F), is expressed in additional large cell bodies near the female midbrain and antennal lobe (red arrowheads in B). synj expression is detected in the optic lobe (blue arrowheads in C, G) and in a subset of midbrain neurons (red arrowheads in C, G). The red arrowhead in G marks sex-specific synj optic lobe expression in males, and midbrain synj levels are generally higher in males (compare expression adjacent to red arrowheads in C, G). p53 is expressed in the optic lobe and suboesophageal ganglion of females (blue and red arrowheads, respectively in D). p53 is also expressed in the male optic lobe (blue arrowheads in H), but not in the male subesophageal ganglion (H). Male-specific p53 expression is detected in neurons adjacent to the antennal lobe (red arrowheads in H). These data are consistent with the results presented in Figure 7. al antennal lobe, la lamina, me medulla, SuEG, supraesophageal ganglion.
Mentions: For many of the genes analyzed, dimorphic expression localized to the optic lobe of the brain. For example, takeout, ci, obp10, arrow, and caspase 7 (Figure 4A,B,D,E,F, respectively) are upregulated in the female optic lobes with respect to males in which little if any transcripts were detected through in situ hybridization. Expression of obp13 is upregulated in the male optic lobe with respect to females (Figure 4J). To be certain that this intense optic lobe staining was not an artifact of the tissue preparation or whole mount in situ hybridization process, we confirmed that negative sense control probes gave little background staining in the optic lobes or in other regions of the brain (Figure 4K). We also confirmed optic lobe expression for a number of DETs by performing in situ hybridization experiments on sectioned brain tissues (Figure 6).

Bottom Line: Transcripts (2,527), many of which were linked to proteolysis, the proteasome, metabolism, catabolic, and biosynthetic processes, ion transport, cell growth, and proliferation, were found to be differentially expressed in A. aegypti female vs. male pupal heads.Sex-specific differences in gene expression were also detected in the antennal lobe and mushroom body. siRNA-mediated gene targeting experiments demonstrated that Doublesex, a transcription factor with consensus binding sites located adjacent to many dimorphically expressed transcripts that function in neural development, is required for regulation of sex-specific gene expression in the developing A. aegypti brain.These studies revealed sex-specific gene expression profiles in the developing A. aegypti pupal head and identified Doublesex as a key regulator of sexually dimorphic gene expression during mosquito neural development.

View Article: PubMed Central - HTML - PubMed

Affiliation: Eck Institute for Global Health, Galvin Life Sciences, University of Notre Dame, Notre Dame 46556, IN, USA ; Department of Biological Sciences, Galvin Life Sciences, University of Notre Dame, Notre Dame 46556, IN, USA.

ABSTRACT

Background: Most animal species exhibit sexually dimorphic behaviors, many of which are linked to reproduction. A number of these behaviors, including blood feeding in female mosquitoes, contribute to the global spread of vector-borne illnesses. However, knowledge concerning the genetic basis of sexually dimorphic traits is limited in any organism, including mosquitoes, especially with respect to differences in the developing nervous system.

Methods: Custom microarrays were used to examine global differences in female vs. male gene expression in the developing pupal head of the dengue vector mosquito, Aedes aegypti. The spatial expression patterns of a subset of differentially expressed transcripts were examined in the developing female vs. male pupal brain through in situ hybridization experiments. Small interfering RNA (siRNA)-mediated knockdown studies were used to assess the putative role of Doublesex, a terminal component of the sex determination pathway, in the regulation of sex-specific gene expression observed in the developing pupal brain.

Results: Transcripts (2,527), many of which were linked to proteolysis, the proteasome, metabolism, catabolic, and biosynthetic processes, ion transport, cell growth, and proliferation, were found to be differentially expressed in A. aegypti female vs. male pupal heads. Analysis of the spatial expression patterns for a subset of dimorphically expressed genes in the pupal brain validated the data set and also facilitated the identification of brain regions with dimorphic gene expression. In many cases, dimorphic gene expression localized to the optic lobe. Sex-specific differences in gene expression were also detected in the antennal lobe and mushroom body. siRNA-mediated gene targeting experiments demonstrated that Doublesex, a transcription factor with consensus binding sites located adjacent to many dimorphically expressed transcripts that function in neural development, is required for regulation of sex-specific gene expression in the developing A. aegypti brain.

Conclusions: These studies revealed sex-specific gene expression profiles in the developing A. aegypti pupal head and identified Doublesex as a key regulator of sexually dimorphic gene expression during mosquito neural development.

No MeSH data available.


Related in: MedlinePlus