TY - JOUR
T1 - AMP-activated protein kinase has diet-dependent and -independent roles in Drosophila oogenesis
AU - Laws, Kaitlin M.
AU - Drummond-Barbosa, Daniela
N1 - Funding Information:
K.M.L. and D.D.-B. designed experiments, analyzed and interpreted data, and wrote the manuscript; K.M.L. performed all experiments. We thank the Developmental Studies Hybridoma Bank for antibodies and the Bloomington Stock Center (supported by National Institutes of Health P40 OD018537 ), D. St. Johnston, and J. Chung for Drosophila stocks. We are grateful to members of the Drummond-Barbosa lab for critical reading of the manuscript. This work was supported by National Institutes of Health R01 GM069875 (D.D.-B.). K.M.L. was supported by National Institutes of Health T32 CA009110 and the Elsa Orent Keiles Fellowship .
Publisher Copyright:
© 2016 Elsevier Inc.
PY - 2016/12/1
Y1 - 2016/12/1
N2 - Multiple aspects of organismal physiology influence the number and activity of stem cells and their progeny, including nutritional status. Previous studies demonstrated that Drosophila germline stem cells (GSCs), follicle stem cells (FSCs), and their progeny sense and respond to diet via complex mechanisms involving many systemic and local signals. AMP-activated protein kinase, or AMPK, is a highly conserved regulator of energy homeostasis known to be activated under low cellular energy conditions; however, its role in the ovarian response to diet has not been investigated. Here, we describe nutrient-dependent and -independent requirements for AMPK in Drosophila oogenesis. We found that AMPK is cell autonomously required for the slow down in GSC and follicle cell proliferation that occurs on a poor diet. Similarly, AMPK activity is necessary in the germline for the degeneration of vitellogenic stages in response to nutrient deprivation. In contrast, AMPK activity is not required within the germline to modulate its growth. Instead, AMPK acts in follicle cells to negatively regulate their growth and proliferation, thereby indirectly limiting the size of the underlying germline cyst within developing follicles. Paradoxically, AMPK is required for GSC maintenance in well-fed flies (when AMPK activity is presumably at its lowest), suggesting potentially important roles for basal AMPK activity in specific cell types. Finally, we identified a nutrient-independent, developmental role for AMPK in cyst encapsulation by follicle cells. These results uncover specific AMPK requirements in multiple cell types in the ovary and suggest that AMPK can function outside of its canonical nutrient-sensing role in specific developmental contexts.
AB - Multiple aspects of organismal physiology influence the number and activity of stem cells and their progeny, including nutritional status. Previous studies demonstrated that Drosophila germline stem cells (GSCs), follicle stem cells (FSCs), and their progeny sense and respond to diet via complex mechanisms involving many systemic and local signals. AMP-activated protein kinase, or AMPK, is a highly conserved regulator of energy homeostasis known to be activated under low cellular energy conditions; however, its role in the ovarian response to diet has not been investigated. Here, we describe nutrient-dependent and -independent requirements for AMPK in Drosophila oogenesis. We found that AMPK is cell autonomously required for the slow down in GSC and follicle cell proliferation that occurs on a poor diet. Similarly, AMPK activity is necessary in the germline for the degeneration of vitellogenic stages in response to nutrient deprivation. In contrast, AMPK activity is not required within the germline to modulate its growth. Instead, AMPK acts in follicle cells to negatively regulate their growth and proliferation, thereby indirectly limiting the size of the underlying germline cyst within developing follicles. Paradoxically, AMPK is required for GSC maintenance in well-fed flies (when AMPK activity is presumably at its lowest), suggesting potentially important roles for basal AMPK activity in specific cell types. Finally, we identified a nutrient-independent, developmental role for AMPK in cyst encapsulation by follicle cells. These results uncover specific AMPK requirements in multiple cell types in the ovary and suggest that AMPK can function outside of its canonical nutrient-sensing role in specific developmental contexts.
KW - AMPK
KW - Diet
KW - Drosophila
KW - Follicle growth
KW - Germline stem cell
KW - LKB1
KW - Oogenesis
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U2 - 10.1016/j.ydbio.2016.10.006
DO - 10.1016/j.ydbio.2016.10.006
M3 - Article
C2 - 27729213
AN - SCOPUS:84996790680
SN - 0012-1606
VL - 420
SP - 90
EP - 99
JO - Developmental biology
JF - Developmental biology
IS - 1
ER -