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BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior.

Corrigan L, Redhai S, Leiblich A, Fan SJ, Perera SM, Patel R, Gandy C, Wainwright SM, Morris JF, Hamdy F, Goberdhan DC, Wilson C - J. Cell Biol. (2014)

Bottom Line: Male reproductive glands secrete signals into seminal fluid to facilitate reproductive success.Exosome release was required to inhibit female remating behavior, suggesting that exosomes are downstream effectors of BMP signaling.These results demonstrate a new function for the MVB-exosome pathway in the reproductive tract that appears to be conserved across evolution.

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Affiliation: Department of Physiology, Anatomy and Genetics and Nuffield Department of Surgical Sciences, University of Oxford, Oxford OX1 3QX, England, UK.

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Knockdown of ALiX in SCs selectively affects female postmating receptivity to other males. (A) Proportion of premated 4-d-old males of different genotypes unable to prevent all females it subsequently mates with from remating (*, P < 0.05; **, P < 0.01, Fisher’s exact test). (B and C) Egg counts (B) and progeny counts (C) from mated females before remating experiments were performed (analyzed by unpaired two-tailed Student’s t test after a Shapiro–Wilk test to confirm normality). (D–F) Mating times (D; **, P < 0.01, Student’s t test), proportion of males that mate within the first 40 min of exposure to females (E) or remate within 40 min of the end of previous mating (F), were also analyzed (using Fisher’s exact test for E and F). Values inside bars show the number of males tested (n). Error bars indicate ±SE. Data shown are from a single representative experiment out of two repeats. DN, dominant negative.
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fig8: Knockdown of ALiX in SCs selectively affects female postmating receptivity to other males. (A) Proportion of premated 4-d-old males of different genotypes unable to prevent all females it subsequently mates with from remating (*, P < 0.05; **, P < 0.01, Fisher’s exact test). (B and C) Egg counts (B) and progeny counts (C) from mated females before remating experiments were performed (analyzed by unpaired two-tailed Student’s t test after a Shapiro–Wilk test to confirm normality). (D–F) Mating times (D; **, P < 0.01, Student’s t test), proportion of males that mate within the first 40 min of exposure to females (E) or remate within 40 min of the end of previous mating (F), were also analyzed (using Fisher’s exact test for E and F). Values inside bars show the number of males tested (n). Error bars indicate ±SE. Data shown are from a single representative experiment out of two repeats. DN, dominant negative.

Mentions: In contrast to virgin females, recently mated Drosophila females will reject a courting male (Wolfner, 1997). We have previously shown that BMP signaling in SCs is required for full induction of this female postmating behavior (Leiblich et al., 2012). We hypothesized that SC-derived exosomes might be involved in this function. Remarkably, blocking exosome production, using SC-specific expression of either ALiX-RNAi or dominant-negative Rab11, reduced the ability of males to prevent female remating (Fig. 8 A). Importantly, and similar to our observations when BMP signaling is blocked in SCs (Leiblich et al., 2012), we did not see any significant effect on egg laying, fecundity, or mating behavior for SC>ALiX-RNAi males (mating times, but not egg laying or fecundity, were reduced for Rab11DN; Fig. 8, B–F). Therefore, exosome secretion from SCs appears to be required to fully induce long-term postmating reprogramming of female behavior.


BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior.

Corrigan L, Redhai S, Leiblich A, Fan SJ, Perera SM, Patel R, Gandy C, Wainwright SM, Morris JF, Hamdy F, Goberdhan DC, Wilson C - J. Cell Biol. (2014)

Knockdown of ALiX in SCs selectively affects female postmating receptivity to other males. (A) Proportion of premated 4-d-old males of different genotypes unable to prevent all females it subsequently mates with from remating (*, P < 0.05; **, P < 0.01, Fisher’s exact test). (B and C) Egg counts (B) and progeny counts (C) from mated females before remating experiments were performed (analyzed by unpaired two-tailed Student’s t test after a Shapiro–Wilk test to confirm normality). (D–F) Mating times (D; **, P < 0.01, Student’s t test), proportion of males that mate within the first 40 min of exposure to females (E) or remate within 40 min of the end of previous mating (F), were also analyzed (using Fisher’s exact test for E and F). Values inside bars show the number of males tested (n). Error bars indicate ±SE. Data shown are from a single representative experiment out of two repeats. DN, dominant negative.
© Copyright Policy - openaccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4151142&req=5

fig8: Knockdown of ALiX in SCs selectively affects female postmating receptivity to other males. (A) Proportion of premated 4-d-old males of different genotypes unable to prevent all females it subsequently mates with from remating (*, P < 0.05; **, P < 0.01, Fisher’s exact test). (B and C) Egg counts (B) and progeny counts (C) from mated females before remating experiments were performed (analyzed by unpaired two-tailed Student’s t test after a Shapiro–Wilk test to confirm normality). (D–F) Mating times (D; **, P < 0.01, Student’s t test), proportion of males that mate within the first 40 min of exposure to females (E) or remate within 40 min of the end of previous mating (F), were also analyzed (using Fisher’s exact test for E and F). Values inside bars show the number of males tested (n). Error bars indicate ±SE. Data shown are from a single representative experiment out of two repeats. DN, dominant negative.
Mentions: In contrast to virgin females, recently mated Drosophila females will reject a courting male (Wolfner, 1997). We have previously shown that BMP signaling in SCs is required for full induction of this female postmating behavior (Leiblich et al., 2012). We hypothesized that SC-derived exosomes might be involved in this function. Remarkably, blocking exosome production, using SC-specific expression of either ALiX-RNAi or dominant-negative Rab11, reduced the ability of males to prevent female remating (Fig. 8 A). Importantly, and similar to our observations when BMP signaling is blocked in SCs (Leiblich et al., 2012), we did not see any significant effect on egg laying, fecundity, or mating behavior for SC>ALiX-RNAi males (mating times, but not egg laying or fecundity, were reduced for Rab11DN; Fig. 8, B–F). Therefore, exosome secretion from SCs appears to be required to fully induce long-term postmating reprogramming of female behavior.

Bottom Line: Male reproductive glands secrete signals into seminal fluid to facilitate reproductive success.Exosome release was required to inhibit female remating behavior, suggesting that exosomes are downstream effectors of BMP signaling.These results demonstrate a new function for the MVB-exosome pathway in the reproductive tract that appears to be conserved across evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Physiology, Anatomy and Genetics and Nuffield Department of Surgical Sciences, University of Oxford, Oxford OX1 3QX, England, UK.

Show MeSH
Related in: MedlinePlus