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
Wilson C
中科院分区:
综合性期刊1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

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精液在重新编程女性的生理和行为以促进男性生殖成功方面起着至关重要的作用。在果蝇中,我们发现特定的精液蛋白,包括原型的“雌性重编程”分子性肽,储存在雄性精液分泌物中,与大的中性含脂微载体结合,这些微载体在雌性体内迅速分散。在其他表达性肽的果蝇中也观察到了相关的结构。缺乏性肽的男性具有结构缺陷的微载体,并表现出许多精液蛋白向女性的异常转移。我们的数据显示,果蝇精液中的这个关键信号分子也是一个微载体组装因子,它调节其他精液因子的转移,这可能是该蛋白在进化上更古老的作用。精液在促进男性生殖成功和调节女性生理和行为方面起着至关重要的作用。在果蝇中,性肽(SP)是这些作用的最典型的蛋白质介体。它是由成对的男性附腺(AG)分泌的,像哺乳动物的前列腺和精囊一样,这些腺体产生了大部分精液内容物。交配后,SP与精子结合,并保留在雌性精子储存器官中。它通过蛋白水解酶的裂解逐渐释放,并诱导几种长期的交配反应,包括增加排卵,增加摄食量,降低对记忆的接受性,主要通过SP受体(SPR)传递信号。在这里,我们演示了SP的一个先前未被怀疑的SPR独立函数。我们发现,在AG腔内,SP和带有膜结合锚定的分泌蛋白被携带在丰富的、大的中性含脂微载体上,这在其他表达SP的果蝇中也存在。这些微载体在交配过程中被转移到雌性体内,在那里它们迅速分解。值得注意的是,SP是一个关键的微载体组装和拆解因素。它的缺失导致交配时转移给雌性的精液蛋白质组发生了重大变化。男性表达无功能的SP突变蛋白,影响女性精子与SP的结合和释放,也不能产生正常的微载体,这表明这种男性特有的缺陷导致了射精功能的广泛异常。因此,我们的数据揭示了SP在精液大分子组合形成中的作用,这可能解释了为什么在缺乏黑腹果蝇信号功能的果蝇物种中存在SP。
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.
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
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影响因子: 9.2
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发表时间: 2013-01-01
影响因子: 1.9
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期刊: GENESIS
影响因子: 1.5
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