title: Sphingomyelinase activity in mother's milk is essential for juvenile development: a case from lactating tsetse flies.
abstract: Sphingosine is a structural component of sphingolipids. The metabolism of phosphoethanolamine ceramide (sphingomyelin) by sphingomyelinase (SMase), followed by the breakdown of ceramide by ceramidase (CDase) yields sphingosine. Female tsetse fly is viviparous and generates a single progeny within her uterus during each gonotrophic cycle. The mother provides her offspring with nutrients required for development solely via intrauterine lactation. Quantitative PCR showed that acid smase1 (asmase1) increases in mother's milk gland during lactation. aSMase1 was detected in the milk gland and larval gut, indicating this protein is generated during lactation and consumed by the larva. The higher levels of SMase activity in larval gut contents indicate that this enzyme is activated by the low gut pH. In addition, cdase is expressed at high levels in the larval gut. Breakdown of the resulting ceramide is likely accomplished by the larval gut-secreted CDase, which allows absorption of sphingosine. We used the tsetse system to understand the critical role(s) of SMase and CDase during pregnancy and lactation and their downstream effects on adult progeny fitness. Reduction of asmase1 by short interfering RNA negatively impacted pregnancy and progeny performance, resulting in a 4-5-day extension in pregnancy, 10%-15% reduction in pupal mass, lower pupal hatch rates, impaired heat tolerance, reduced symbiont levels, and reduced fecundity of adult progeny. This study suggests that the SMase activity associated with tsetse lactation and larval digestion is similar in function to that of mammalian lactation and represents a critical process for juvenile development, with important effects on the health of progeny during their adulthood.
authors.affiliation: Division of Epidemiology and Public Health, Yale School of Public Health, Yale University, New Haven, Connecticut 06520, USA. joshua.benoit@yale.edu
authors.forename: Joshua B
authors.initials: JB
authors.lastname: Benoit
authors.forename: Geoffrey M
authors.initials: GM
authors.lastname: Attardo
authors.forename: Veronika
authors.initials: V
authors.lastname: Michalkova
authors.forename: Peter
authors.initials: P
authors.lastname: Takác
authors.forename: Jana
authors.initials: J
authors.lastname: Bohova
authors.forename: Serap
authors.initials: S
authors.lastname: Aksoy
mesh_terms: D000818:Animals; D001483:Base Sequence; D055572:Ceramidases / Q000037:antagonists & inhibitors / Q000235:genetics / Q000378:metabolism; D004330:Drosophila / Q000235:genetics; D005260:Female; D055785:Gene Knockdown Techniques; D017344:Genes, Insect; D006863:Hydrogen-Ion Concentration; D019476:Insect Proteins / Q000037:antagonists & inhibitors / Q000235:genetics / Q000378:metabolism*; D007774:Lactation / Q000235:genetics / Q000378:metabolism; D007814:Larva / Q000254:growth & development; D008892:Milk / Q000201:enzymology*; D008954:Models, Biological; D010802:Phylogeny; D011247:Pregnancy; D034741:RNA, Small Interfering / Q000235:genetics; D013045:Species Specificity; D013108:Sphingomyelin Phosphodiesterase / Q000037:antagonists & inhibitors / Q000235:genetics / Q000378:metabolism*; D013559:Symbiosis; D014370:Tsetse Flies / Q000201:enzymology* / Q000235:genetics / Q000254:growth & development* / Q000382:microbiology; D044106:Wigglesworthia / Q000302:isolation & purification
chemical_list: D019476:Insect Proteins; D034741:RNA, Small Interfering; C112980:acid sphingomyelinase-1; D013108:Sphingomyelin Phosphodiesterase; D055572:Ceramidases