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

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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.

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Acknowledgments

We thank Dr. Hideyuki Inui of the Research Center for Environmental Genomics, Kobe University for facilities and useful discussions and Dr. Susumu Hiragaki for critical reading of the manuscript.

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Authors and Affiliations

  1. Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, P O Box 14115-336, Tehran, Iran

    Azam Mikani

  2. Laboratory of Biotechnology, Faculty of Education, Ashiya University, Rokurokusocho, 13-22, Ashiya, Hyogo, 659-8511, Japan

    Yasuhiko Watari

  3. Graduate School of Agricultural Science, Kobe University, 1-1 Rokkodai-cho, Nada-ku, Kobe, 657-8501, Japan

    Makio Takeda

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  1. Azam Mikani
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  2. Yasuhiko Watari
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  3. Makio Takeda
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Correspondence to Makio Takeda.

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Mikani, A., Watari, Y. & Takeda, M. Brain-midgut cross-talk and autocrine metabolastat via the sNPF/CCAP negative feed-back loop in the American cockroach, Periplaneta americana . Cell Tissue Res 362, 481–496 (2015). https://doi.org/10.1007/s00441-015-2242-4

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  • DOI: https://doi.org/10.1007/s00441-015-2242-4

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