Brain-midgut cross-talk and autocrine metabolastat via the sNPF/CCAP negative feed-back loop in the American cockroach, Periplaneta americana

Cell Tissue Res. 2015 Dec;362(3):481-96. doi: 10.1007/s00441-015-2242-4. Epub 2015 Jul 16.

Abstract

Immunohistochemical reactivities against short neuropeptide F (sNPF-ir) and crustacean cardioactive peptide (CCAP-ir) were detected in both the brain-subesophageal ganglion (Br-SOG) and midgut epithelial cells of the male American cockroach, Periplaneta americana. Four weeks of starvation increased the number of sNPF-ir cells and decreased the CCAP-ir cells in the Br-SOG, whereas refeeding reversed these effects. The contents of sNPF in the Br-SOG, midgut and hemolymph titer decreased in response to an injection of CCAP into the hemocoel of normally fed male cockroaches, while CCAP titers/contents decreased in response to an injection of sNPF. The results of a double-labeling experiment demonstrated that sNPF-ir co-existed in CCAP-ir cells in the pars intercerebralis (PI), dorsolateral region of protocerebrum (DL), deutocerebrum (De) and SOG. sNPF-ir and CCAP-ir were also colocalized in the midgut. sNPF and CCAP are neuropeptides and midgut factors that interact with each other. Since the two peptides are known to be secreted by identical cells that affect each other, this constitutes autocrine negative feedback regulation for a quick response to food accessibility/inaccessibility. These peptides not only constitute the switch in the digestive mechanism but also couple digestive adaptation with behavior. A CCAP injection suppressed locomotor activity when cockroaches were starved, whereas sNPF activated it when they were fed.

Keywords: Crustacean cardioactive peptide; Locomotor activity; Metabolastat; Periplaneta americana; Short neuropeptide F.

MeSH terms

  • Animals
  • Autocrine Communication*
  • Brain / metabolism*
  • Cockroaches / metabolism*
  • Digestive System / metabolism*
  • Enzyme-Linked Immunosorbent Assay
  • Esophagus / metabolism
  • Feedback, Physiological*
  • Feeding Behavior
  • Ganglia, Invertebrate / metabolism
  • Male
  • Metabolome*
  • Motor Activity
  • Neuropeptides / metabolism*
  • Starvation

Substances

  • Neuropeptides
  • crustacean cardioactive peptide
  • neuropeptide F