Neurochemical fine tuning of a peripheral tissue: peptidergic and aminergic regulation of fluid secretion by Malpighian tubules in the tobacco hawkmoth M. sexta

Author:

Skaer N. J. V.1,Nässel D. R.2,Maddrell S. H. P.1,Tublitz N. J.3

Affiliation:

1. Department of Zoology, Downing Street, University of Cambridge, Cambridge CB2 3EJ, UK

2. Department of Zoology, Stockholm University, Svante Arrhenius väg 16,SE-106 91 Stockholm, Sweden

3. Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403 USA

Abstract

SUMMARY The actions of various peptides and other compounds on fluid secretion by Malpighian tubules in the tobacco hawkmoth Manduca sexta sexta are investigated in this study. Using a newly developed pharate adult Malpighian tubule bioassay, we show that three tachykinin-related peptides (TRPs),leucokinin I, serotonin (5-HT), octopamine, the cardioacceleratory peptides 1a, 1b and 2c, cGMP and cAMP each cause an increase in the rate of fluid secretion in pharate adult tubules. Whereas the possible hormonal sources of biogenic amines and some of the peptides are known, the distribution of TRPs has not been investigated previously in M. sexta. Thus we performed immunocytochemistry using an anti-TRP antiserum. We show the presence of TRP-like material in a small subset of cells in the M. sexta central nervous system (CNS). The larval brain contains approximately 60 TRP-immunopositive cells and there are approximately 100 such cells in the adult brain including the optic lobes. Every ganglion of the ventral nerve cord also contains TRP-like immunoreactive cells. No TRP-containing neurosecretory cells were seen in the CNS, but endocrine cells of the midgut reacted with the antiserum. We propose the hypothesis that the control in insects of physiological systems by hormones may not always involve tissue-specific hormones that force stereotypical responses in their target systems. Instead, there may exist in the extracellular fluid a continuous broadcast of information in the form of a chemical language to which some or all parts of the body continuously respond on a moment-to-moment basis, and which ensures a more effective and efficient coordination of function than could be achieved otherwise.

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

Reference52 articles.

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2. Chamberlin, M. E. and Phillips, J. E. (1982). Regulation of hemolymph amino acid levels and active secretion of proline by Malpighian tubules of locusts. Can. J. Zool.60,2745-2752.

3. Chen, Y., Veenstra, J. A., Davis, N. T. and Hagedorn, H. H.(1994). Leucokinin and diuretic hormone immunoreactivity in the tobacco hornworm, M. sexta, and co-localization of this immunoreactivity in lateral neurosecretory cells of the abdominal ganglia. Cell Tissue Res.278,493-507.

4. Cheung, C. C., Loi, P. K., Sylwester, A. W., Lee, T. D. and Tublitz, N. J. (1992). Primary structure of a cardioactive neuropeptide from the tobacco hawkmoth, M. sexta.FEBS Lett.313,165-168.

5. Christie, A. C., Lundquist, C. T., Nässel, D. R. and Nusbaum, M. P. (1997). Two novel tachykinin-related peptides from the nervous system of the crab Cancer borealis.J. Exp. Biol.200,2279-2294.

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