Drosophila Sex Peptide controls the assembly of lipid microcarriers in seminal fluid.
Drosophila Sex Peptide controls the assembly of lipid microcarriers in seminal fluid.
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DOI:
10.1073/pnas.2019622118
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发表时间:
2021-02-02
影响因子:
11.1
通讯作者:
Wilson C
中科院分区:
文献类型:
--
作者:
Wainwright SM;Hopkins BR;Mendes CC;Sekar A;Kroeger B;Hellberg JEEU;Fan SJ;Pavey A;Marie PP;Leiblich A;Sepil I;Charles PD;Thézénas ML;Fischer R;Kessler BM;Gandy C;Corrigan L;Patel R;Wigby S;Morris JF;Goberdhan DCI;Wilson C
Seminal fluid plays a critical role in reprogramming female physiology and behavior to promote male reproductive success. We show, in the fruit fly, that specific seminal proteins, including the archetypal “female-reprogramming” molecule Sex Peptide, are stored in male seminal secretions in association with large neutral lipid-containing microcarriers, which rapidly disperse in females. Related structures are also observed in other Sex Peptide-expressing Drosophila species. Males lacking Sex Peptide have structurally defective microcarriers and exhibit abnormal transfer of many seminal proteins to females. Our data reveal that this key signaling molecule in Drosophila seminal fluid is also a microcarrier assembly factor that modulates transfer of other seminal factors and that this may be a more evolutionarily ancient role of this protein. Seminal fluid plays an essential role in promoting male reproductive success and modulating female physiology and behavior. In the fruit fly, Drosophila melanogaster, Sex Peptide (SP) is the best-characterized protein mediator of these effects. It is secreted from the paired male accessory glands (AGs), which, like the mammalian prostate and seminal vesicles, generate most of the seminal fluid contents. After mating, SP binds to spermatozoa and is retained in the female sperm storage organs. It is gradually released by proteolytic cleavage and induces several long-term postmating responses, including increased ovulation, elevated feeding, and reduced receptivity to remating, primarily signaling through the SP receptor (SPR). Here, we demonstrate a previously unsuspected SPR-independent function for SP. We show that, in the AG lumen, SP and secreted proteins with membrane-binding anchors are carried on abundant, large neutral lipid-containing microcarriers, also found in other SP-expressing Drosophila species. These microcarriers are transferred to females during mating where they rapidly disassemble. Remarkably, SP is a key microcarrier assembly and disassembly factor. Its absence leads to major changes in the seminal proteome transferred to females upon mating. Males expressing nonfunctional SP mutant proteins that affect SP’s binding to and release from sperm in females also do not produce normal microcarriers, suggesting that this male-specific defect contributes to the resulting widespread abnormalities in ejaculate function. Our data therefore reveal a role for SP in formation of seminal macromolecular assemblies, which may explain the presence of SP in Drosophila species that lack the signaling functions seen in D. melanogaster.
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DOI:
10.1083/jcb.201401072
发表时间:
2014-09-01
期刊:
The Journal of cell biology
影响因子:
--
作者:
Corrigan L;Redhai S;Leiblich A;Fan SJ;Perera SM;Patel R;Gandy C;Wainwright SM;Morris JF;Hamdy F;Goberdhan DC;Wilson C
通讯作者:
Wilson C
DOI:
10.1073/pnas.1906149116
发表时间:
2019-09-03
影响因子:
11.1
作者:
Hopkins, Ben R.;Sepil, Irem;Wigby, Stuart
通讯作者:
Wigby, Stuart
影响因子:
9.2
作者:
Carvalho, GB;Kapahi, P;Benzer, S
通讯作者:
Benzer, S
影响因子:
1.9
作者:
Juyena, N. S.;Vencato, J.;Stelletta, C.
通讯作者:
Stelletta, C.
影响因子:
1.5
作者:
Hayashi, S;Ito, K;Goto, S
通讯作者:
Goto, S