title: Juvenile hormone and insulin suppress lipolysis between periods of lactation during tsetse fly pregnancy.
abstract: Tsetse flies are viviparous insects that nurture a single intrauterine progeny per gonotrophic cycle. The developing larva is nourished by the lipid-rich, milk-like secretions from a modified female accessory gland (milk gland). An essential feature of the lactation process involves lipid mobilization for incorporation into the milk. In this study, we examined roles for juvenile hormone (JH) and insulin/IGF-like (IIS) signaling pathways during tsetse pregnancy. In particular, we examined the roles for these pathways in regulating lipid homeostasis during transitions between non-lactating (dry) and lactating periods. The dry period occurs over the course of oogenesis and embryogenesis, while the lactation period spans intrauterine larvigenesis. Genes involved in the JH and IIS pathways were upregulated during dry periods, correlating with lipid accumulation between bouts of lactation. RNAi suppression of Forkhead Box Sub Group O (FOXO) expression impaired lipolysis during tsetse lactation and reduced fecundity. Similar reduction of the JH receptor Methoprene tolerant (Met), but not its paralog germ cell expressed (gce), reduced lipid accumulation during dry periods, indicating functional divergence between Met and gce during tsetse reproduction. Reduced lipid levels following Met knockdown led to impaired fecundity due to inadequate fat reserves at the initiation of milk production. Both the application of the JH analog (JHA) methoprene and injection of insulin into lactating females increased stored lipids by suppressing lipolysis and reduced transcripts of lactation-specific genes, leading to elevated rates of larval abortion. To our knowledge, this study is the first to address the molecular physiology of JH and IIS in a viviparous insect, and specifically to provide a role for JH signaling through Met in the regulation of lipid metabolism during insect lactation.
authors.affiliation: Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, VA.
authors.forename: Aaron A
authors.initials: AA
authors.lastname: Baumann
authors.affiliation: Department of Epidemiology of Microbial Diseases, School of Public Health, Yale University, New Haven, CT 06520.
authors.forename: Joshua B
authors.initials: JB
authors.lastname: Benoit
authors.affiliation: Department of Epidemiology of Microbial Diseases, School of Public Health, Yale University, New Haven, CT 06520.|Section of Molecular and Applied Zoology, Institute of Zoology, Slovak Academy of Sciences, Bratislava, Slovakia.
authors.forename: Veronika
authors.initials: V
authors.lastname: Michalkova
authors.affiliation: Department of Biochemistry and Molecular Biology, Egerton University, Njoro, Kenya.
authors.forename: Paul
authors.initials: P
authors.lastname: Mireji
authors.affiliation: Department of Epidemiology of Microbial Diseases, School of Public Health, Yale University, New Haven, CT 06520.
authors.forename: Geoffrey M
authors.initials: GM
authors.lastname: Attardo
authors.affiliation: Department of Entomology and Plant Pathology, University of Tennessee, Knoxville TN.
authors.forename: John K
authors.initials: JK
authors.lastname: Moulton
authors.affiliation: Department of Evolution, Ecology, and Organismal Biology, Ohio State University, Columbus, OH.
authors.forename: Thomas G
authors.initials: TG
authors.lastname: Wilson
authors.affiliation: Department of Epidemiology of Microbial Diseases, School of Public Health, Yale University, New Haven, CT 06520.
authors.forename: Serap
authors.initials: S
authors.lastname: Aksoy
mesh_terms: D000818:Animals; D005260:Female; D051858:Forkhead Transcription Factors / Q000235:genetics / Q000378:metabolism; D015870:Gene Expression; D017344:Genes, Insect; D019476:Insect Proteins / Q000235:genetics / Q000378:metabolism; D007328:Insulin / Q000494:pharmacology / Q000502:physiology*; D007605:Juvenile Hormones / Q000494:pharmacology / Q000502:physiology; D008049:Lipase / Q000235:genetics / Q000378:metabolism; D050356:Lipid Metabolism; D008066:Lipolysis; D008726:Methoprene / Q000494:pharmacology*; D055703:Reproductive Physiological Phenomena; D015398:Signal Transduction; D014370:Tsetse Flies / Q000378:metabolism*; D052286:Viviparity, Nonmammalian
chemical_list: D051858:Forkhead Transcription Factors; D019476:Insect Proteins; D007328:Insulin; D007605:Juvenile Hormones; D008726:Methoprene; D008049:Lipase