TY - JOUR
T1 - Pronounced Postmating Response in the Drosophila Female Reproductive Tract Fluid Proteome
AU - McDonough-Goldstein, Caitlin E.
AU - Whittington, Emma
AU - McCullough, Erin L.
AU - Buel, Sharleen M.
AU - Erdman, Scott
AU - Pitnick, Scott
AU - Dorus, Steve
N1 - Funding Information:
Funding and additional information—This work was supported by a National Science Foundation Graduate Research Fellowship (to C. E. M.-G.), by grants from the National Science Foundation (DEB-1655840 to S. D. and S. P.) and the Eunice Kennedy Shriver National Institute of Child Health and Human Development (R21-HD088910 to S. D. and S. P.).
Funding Information:
Acknowledgments—The authors thank Yagnesh Umrania, Renata Feret, and Mike Deery at the Cambridge Center for Proteomics for their assistance with proteomics data acquisition and analysis. We also thank Elen Safarian for contributing to developing and testing fluid isolation methods. Finally, we appreciate the analytical support from Kirill Borziak and Yasir Ahmed-Braimah as well as the thoughtful feedback from all the members of the Center for Reproductive Evolution throughout the development of this research. This work was supported by a generous gift by Mike and Jane Weeden to the Syracuse University.
Publisher Copyright:
© 2021 American Society for Biochemistry and Molecular Biology Inc.. All rights reserved.
PY - 2021/9
Y1 - 2021/9
N2 - Fertility depends on the progression of complex and coordinated postmating processes within the extracellular environment of the female reproductive tract (FRT). Molecular interactions between ejaculate and FRT proteins regulate many of these processes, including sperm motility, migration, storage, and modification, along with concurrent changes in the female. Although extensive progress has been made in the proteomic characterization of the male-derived components of sperm and seminal fluid, investigations into the FRT have remained more limited. To achieve a comparable level of knowledge regarding female-derived proteins that comprise the reproductive environment, we utilized semiquantitative MS-based proteomics to study the composition of the FRT tissue and, separately, the luminal fluid, before and after mating in Drosophila melanogaster. Our approach leveraged whole-fly isotopic labeling to delineate female proteins from transferred male ejaculate proteins. Our results revealed several characteristics that distinguish the FRT fluid proteome from the FRT tissue proteome: (1) the fluid proteome is encoded by genes with higher overall levels of FRT gene expression and tissue specificity, including many genes with enriched expression in the fat body, (2) fluid-biased proteins are enriched for metabolic functions, and (3) the fluid exhibits pronounced postmating compositional changes. The dynamic mating-induced proteomic changes in the FRT fluid inform our understanding of secretory mechanisms of the FRT, serve as a foundation for establishing female contributions to the ejaculate–female interactions that regulate fertility, and highlight the importance of applying proteomic approaches to characterize the composition and dynamics of the FRT environment.
AB - Fertility depends on the progression of complex and coordinated postmating processes within the extracellular environment of the female reproductive tract (FRT). Molecular interactions between ejaculate and FRT proteins regulate many of these processes, including sperm motility, migration, storage, and modification, along with concurrent changes in the female. Although extensive progress has been made in the proteomic characterization of the male-derived components of sperm and seminal fluid, investigations into the FRT have remained more limited. To achieve a comparable level of knowledge regarding female-derived proteins that comprise the reproductive environment, we utilized semiquantitative MS-based proteomics to study the composition of the FRT tissue and, separately, the luminal fluid, before and after mating in Drosophila melanogaster. Our approach leveraged whole-fly isotopic labeling to delineate female proteins from transferred male ejaculate proteins. Our results revealed several characteristics that distinguish the FRT fluid proteome from the FRT tissue proteome: (1) the fluid proteome is encoded by genes with higher overall levels of FRT gene expression and tissue specificity, including many genes with enriched expression in the fat body, (2) fluid-biased proteins are enriched for metabolic functions, and (3) the fluid exhibits pronounced postmating compositional changes. The dynamic mating-induced proteomic changes in the FRT fluid inform our understanding of secretory mechanisms of the FRT, serve as a foundation for establishing female contributions to the ejaculate–female interactions that regulate fertility, and highlight the importance of applying proteomic approaches to characterize the composition and dynamics of the FRT environment.
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U2 - 10.1016/j.mcpro.2021.100156
DO - 10.1016/j.mcpro.2021.100156
M3 - Article
C2 - 34597791
AN - SCOPUS:85120848448
SN - 1535-9476
VL - 20
JO - Molecular and Cellular Proteomics
JF - Molecular and Cellular Proteomics
M1 - 100156
ER -