A role for triglyceride lipase brummer in the regulation of sex differences in Drosophila fat storage and breakdown

Triglycerides are the major form of stored fat in all animals. One important determinant of whole-body fat storage is whether an animal is male or female. Here, we use Drosophila , an established model for studies on triglyceride metabolism, to gain insight into the genes and physiological mechanism...

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Veröffentlicht in:	PLoS biology Jg. 18; H. 1; S. e3000595
Hauptverfasser:	Wat, Lianna W., Chao, Charlotte, Bartlett, Rachael, Buchanan, Justin L., Millington, Jason W., Chih, Hui Ju, Chowdhury, Zahid S., Biswas, Puja, Huang, Vivian, Shin, Leah J., Wang, Lin Chuan, Gauthier, Marie-Pierre L., Barone, Maria C., Montooth, Kristi L., Welte, Michael A., Rideout, Elizabeth J.
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	United States Public Library of Science 01.01.2020 Public Library of Science (PLoS)
Schlagworte:	Animals Animals, Genetically Modified Biology and Life Sciences Body fat Breakdown Cell culture Computer and Information Sciences Droplets Drosophila Drosophila - genetics Drosophila - metabolism Drosophila Proteins - physiology Energy Metabolism - genetics Fat body Female Gender aspects Gender differences Homeostasis Insects Lipase Lipase - genetics Lipase - metabolism Lipase - physiology Lipid Metabolism - genetics Lipids Lipolysis - genetics Male Males Medicine and Health Sciences Metabolism Micronutrients - metabolism mRNA Neurons Regulations Research and Analysis Methods Sex Sex Characteristics Sex differences Somatic cells Storage Triglycerides Triglycerides - metabolism
ISSN:	1545-7885, 1544-9173, 1545-7885
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Abstract	Triglycerides are the major form of stored fat in all animals. One important determinant of whole-body fat storage is whether an animal is male or female. Here, we use Drosophila , an established model for studies on triglyceride metabolism, to gain insight into the genes and physiological mechanisms that contribute to sex differences in fat storage. Our analysis of triglyceride storage and breakdown in both sexes identified a role for triglyceride lipase brummer ( bmm ) in the regulation of sex differences in triglyceride homeostasis. Normally, male flies have higher levels of bmm mRNA both under normal culture conditions and in response to starvation, a lipolytic stimulus. We find that loss of bmm largely eliminates the sex difference in triglyceride storage and abolishes the sex difference in triglyceride breakdown via strongly male-biased effects. Although we show that bmm function in the fat body affects whole-body triglyceride levels in both sexes, in males, we identify an additional role for bmm function in the somatic cells of the gonad and in neurons in the regulation of whole-body triglyceride homeostasis. Furthermore, we demonstrate that lipid droplets are normally present in both the somatic cells of the male gonad and in neurons, revealing a previously unrecognized role for bmm function, and possibly lipid droplets, in these cell types in the regulation of whole-body triglyceride homeostasis. Taken together, our data reveal a role for bmm function in the somatic cells of the gonad and in neurons in the regulation of male–female differences in fat storage and breakdown and identify bmm as a link between the regulation of triglyceride homeostasis and biological sex.
AbstractList	Triglycerides are the major form of stored fat in all animals. One important determinant of whole-body fat storage is whether an animal is male or female. Here, we use Drosophila, an established model for studies on triglyceride metabolism, to gain insight into the genes and physiological mechanisms that contribute to sex differences in fat storage. Our analysis of triglyceride storage and breakdown in both sexes identified a role for triglyceride lipase brummer (bmm) in the regulation of sex differences in triglyceride homeostasis. Normally, male flies have higher levels of bmm mRNA both under normal culture conditions and in response to starvation, a lipolytic stimulus. We find that loss of bmm largely eliminates the sex difference in triglyceride storage and abolishes the sex difference in triglyceride breakdown via strongly male-biased effects. Although we show that bmm function in the fat body affects whole-body triglyceride levels in both sexes, in males, we identify an additional role for bmm function in the somatic cells of the gonad and in neurons in the regulation of whole-body triglyceride homeostasis. Furthermore, we demonstrate that lipid droplets are normally present in both the somatic cells of the male gonad and in neurons, revealing a previously unrecognized role for bmm function, and possibly lipid droplets, in these cell types in the regulation of whole-body triglyceride homeostasis. Taken together, our data reveal a role for bmm function in the somatic cells of the gonad and in neurons in the regulation of male–female differences in fat storage and breakdown and identify bmm as a link between the regulation of triglyceride homeostasis and biological sex. An investigation of the genetic and physiological mechanisms underlying sex differences in fat storage and breakdown in the fruit fly Drosophila identifies previously unrecognized sex- and cell type-specific roles for the conserved triglyceride lipase brummer. Triglycerides are the major form of stored fat in all animals. One important determinant of whole-body fat storage is whether an animal is male or female. Here, we use Drosophila, an established model for studies on triglyceride metabolism, to gain insight into the genes and physiological mechanisms that contribute to sex differences in fat storage. Our analysis of triglyceride storage and breakdown in both sexes identified a role for triglyceride lipase brummer (bmm) in the regulation of sex differences in triglyceride homeostasis. Normally, male flies have higher levels of bmm mRNA both under normal culture conditions and in response to starvation, a lipolytic stimulus. We find that loss of bmm largely eliminates the sex difference in triglyceride storage and abolishes the sex difference in triglyceride breakdown via strongly male-biased effects. Although we show that bmm function in the fat body affects whole-body triglyceride levels in both sexes, in males, we identify an additional role for bmm function in the somatic cells of the gonad and in neurons in the regulation of whole-body triglyceride homeostasis. Furthermore, we demonstrate that lipid droplets are normally present in both the somatic cells of the male gonad and in neurons, revealing a previously unrecognized role for bmm function, and possibly lipid droplets, in these cell types in the regulation of whole-body triglyceride homeostasis. Taken together, our data reveal a role for bmm function in the somatic cells of the gonad and in neurons in the regulation of male-female differences in fat storage and breakdown and identify bmm as a link between the regulation of triglyceride homeostasis and biological sex. Triglycerides are the major form of stored fat in all animals. One important determinant of whole-body fat storage is whether an animal is male or female. Here, we use Drosophila, an established model for studies on triglyceride metabolism, to gain insight into the genes and physiological mechanisms that contribute to sex differences in fat storage. Our analysis of triglyceride storage and breakdown in both sexes identified a role for triglyceride lipase brummer (bmm) in the regulation of sex differences in triglyceride homeostasis. Normally, male flies have higher levels of bmm mRNA both under normal culture conditions and in response to starvation, a lipolytic stimulus. We find that loss of bmm largely eliminates the sex difference in triglyceride storage and abolishes the sex difference in triglyceride breakdown via strongly male-biased effects. Although we show that bmm function in the fat body affects whole-body triglyceride levels in both sexes, in males, we identify an additional role for bmm function in the somatic cells of the gonad and in neurons in the regulation of whole-body triglyceride homeostasis. Furthermore, we demonstrate that lipid droplets are normally present in both the somatic cells of the male gonad and in neurons, revealing a previously unrecognized role for bmm function, and possibly lipid droplets, in these cell types in the regulation of whole-body triglyceride homeostasis. Taken together, our data reveal a role for bmm function in the somatic cells of the gonad and in neurons in the regulation of male-female differences in fat storage and breakdown and identify bmm as a link between the regulation of triglyceride homeostasis and biological sex.Triglycerides are the major form of stored fat in all animals. One important determinant of whole-body fat storage is whether an animal is male or female. Here, we use Drosophila, an established model for studies on triglyceride metabolism, to gain insight into the genes and physiological mechanisms that contribute to sex differences in fat storage. Our analysis of triglyceride storage and breakdown in both sexes identified a role for triglyceride lipase brummer (bmm) in the regulation of sex differences in triglyceride homeostasis. Normally, male flies have higher levels of bmm mRNA both under normal culture conditions and in response to starvation, a lipolytic stimulus. We find that loss of bmm largely eliminates the sex difference in triglyceride storage and abolishes the sex difference in triglyceride breakdown via strongly male-biased effects. Although we show that bmm function in the fat body affects whole-body triglyceride levels in both sexes, in males, we identify an additional role for bmm function in the somatic cells of the gonad and in neurons in the regulation of whole-body triglyceride homeostasis. Furthermore, we demonstrate that lipid droplets are normally present in both the somatic cells of the male gonad and in neurons, revealing a previously unrecognized role for bmm function, and possibly lipid droplets, in these cell types in the regulation of whole-body triglyceride homeostasis. Taken together, our data reveal a role for bmm function in the somatic cells of the gonad and in neurons in the regulation of male-female differences in fat storage and breakdown and identify bmm as a link between the regulation of triglyceride homeostasis and biological sex. Triglycerides are the major form of stored fat in all animals. One important determinant of whole-body fat storage is whether an animal is male or female. Here, we use Drosophila , an established model for studies on triglyceride metabolism, to gain insight into the genes and physiological mechanisms that contribute to sex differences in fat storage. Our analysis of triglyceride storage and breakdown in both sexes identified a role for triglyceride lipase brummer ( bmm ) in the regulation of sex differences in triglyceride homeostasis. Normally, male flies have higher levels of bmm mRNA both under normal culture conditions and in response to starvation, a lipolytic stimulus. We find that loss of bmm largely eliminates the sex difference in triglyceride storage and abolishes the sex difference in triglyceride breakdown via strongly male-biased effects. Although we show that bmm function in the fat body affects whole-body triglyceride levels in both sexes, in males, we identify an additional role for bmm function in the somatic cells of the gonad and in neurons in the regulation of whole-body triglyceride homeostasis. Furthermore, we demonstrate that lipid droplets are normally present in both the somatic cells of the male gonad and in neurons, revealing a previously unrecognized role for bmm function, and possibly lipid droplets, in these cell types in the regulation of whole-body triglyceride homeostasis. Taken together, our data reveal a role for bmm function in the somatic cells of the gonad and in neurons in the regulation of male–female differences in fat storage and breakdown and identify bmm as a link between the regulation of triglyceride homeostasis and biological sex.
Author	Wang, Lin Chuan Wat, Lianna W. Chowdhury, Zahid S. Biswas, Puja Chih, Hui Ju Millington, Jason W. Gauthier, Marie-Pierre L. Huang, Vivian Shin, Leah J. Buchanan, Justin L. Montooth, Kristi L. Welte, Michael A. Chao, Charlotte Bartlett, Rachael Rideout, Elizabeth J. Barone, Maria C.
AuthorAffiliation	2 School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, Nebraska, United States of America 1 Department of Cellular and Physiological Sciences, Life Sciences Institute, The University of British Columbia, Vancouver, British Columbia, Canada ICM, FRANCE 3 Department of Biology, University of Rochester, Rochester, New York, United States of America
AuthorAffiliation_xml	– name: 3 Department of Biology, University of Rochester, Rochester, New York, United States of America – name: ICM, FRANCE – name: 2 School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, Nebraska, United States of America – name: 1 Department of Cellular and Physiological Sciences, Life Sciences Institute, The University of British Columbia, Vancouver, British Columbia, Canada
Author_xml	– sequence: 1 givenname: Lianna W. surname: Wat fullname: Wat, Lianna W. – sequence: 2 givenname: Charlotte surname: Chao fullname: Chao, Charlotte – sequence: 3 givenname: Rachael orcidid: 0000-0002-9199-1326 surname: Bartlett fullname: Bartlett, Rachael – sequence: 4 givenname: Justin L. orcidid: 0000-0002-1701-5570 surname: Buchanan fullname: Buchanan, Justin L. – sequence: 5 givenname: Jason W. surname: Millington fullname: Millington, Jason W. – sequence: 6 givenname: Hui Ju surname: Chih fullname: Chih, Hui Ju – sequence: 7 givenname: Zahid S. surname: Chowdhury fullname: Chowdhury, Zahid S. – sequence: 8 givenname: Puja orcidid: 0000-0001-6808-6662 surname: Biswas fullname: Biswas, Puja – sequence: 9 givenname: Vivian orcidid: 0000-0002-6255-5955 surname: Huang fullname: Huang, Vivian – sequence: 10 givenname: Leah J. surname: Shin fullname: Shin, Leah J. – sequence: 11 givenname: Lin Chuan orcidid: 0000-0002-1767-6811 surname: Wang fullname: Wang, Lin Chuan – sequence: 12 givenname: Marie-Pierre L. surname: Gauthier fullname: Gauthier, Marie-Pierre L. – sequence: 13 givenname: Maria C. orcidid: 0000-0002-0528-1898 surname: Barone fullname: Barone, Maria C. – sequence: 14 givenname: Kristi L. orcidid: 0000-0001-9456-6694 surname: Montooth fullname: Montooth, Kristi L. – sequence: 15 givenname: Michael A. orcidid: 0000-0001-5741-4720 surname: Welte fullname: Welte, Michael A. – sequence: 16 givenname: Elizabeth J. orcidid: 0000-0003-0012-2828 surname: Rideout fullname: Rideout, Elizabeth J.
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/31961851$$D View this record in MEDLINE/PubMed
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ContentType	Journal Article
Copyright	2020 Wat et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2020 Wat et al 2020 Wat et al
Copyright_xml	– notice: 2020 Wat et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2020 Wat et al 2020 Wat et al
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Snippet	Triglycerides are the major form of stored fat in all animals. One important determinant of whole-body fat storage is whether an animal is male or female....
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SubjectTerms	Animals Animals, Genetically Modified Biology and Life Sciences Body fat Breakdown Cell culture Computer and Information Sciences Droplets Drosophila Drosophila - genetics Drosophila - metabolism Drosophila Proteins - physiology Energy Metabolism - genetics Fat body Female Gender aspects Gender differences Homeostasis Insects Lipase Lipase - genetics Lipase - metabolism Lipase - physiology Lipid Metabolism - genetics Lipids Lipolysis - genetics Male Males Medicine and Health Sciences Metabolism Micronutrients - metabolism mRNA Neurons Regulations Research and Analysis Methods Sex Sex Characteristics Sex differences Somatic cells Storage Triglycerides Triglycerides - metabolism
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Title	A role for triglyceride lipase brummer in the regulation of sex differences in Drosophila fat storage and breakdown
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Volume	18
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