Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1987 Apr;84(7):1867–1870. doi: 10.1073/pnas.84.7.1867

G protein and diacylglycerol regulate metamorphosis of planktonic molluscan larvae

Gregory Baxter 1, Daniel E Morse 1
PMCID: PMC304542  PMID: 16593819

Abstract

The regulatory guanine nucleotide binding protein (G protein) activators cholera toxin and the GTP analog 5-guanylyl imidophosphate, the second messenger diacylglycerol, and certain diamino acids all facilitate (amplify) the settlement and metamorphic responses of planktonic larvae of Haliotis rufescens (marine mollusc) to morphogenetic chemical stimuli. In contrast, the G protein-inhibiting analog guanosine 5′-O-[β-thio]diphosphate inhibits facilitation by L-α,β-diaminopropionic acid but does not block facilitation by diacylglycerol. Diacylglycerol, cholera toxin, and the guanine nucleotide analogs alone neither induce the settlement and metamorphosis of the larvae nor do they inhibit induction of metamorphosis by γ-aminobutyric acid. These results thus establish the existence of separate regulatory and inductive pathways controlling larval metamorphosis in response to two classes of exogenous chemical signals from the environment. The regulatory pathway, operating independently through a G protein-diacylglycerol cascade apparently controlled by facilitating diamino acids in the water column, can amplify the larval responsiveness to inducers of metamorphosis. This mechanism may have adaptive significance in the recognition and selection of favorable habitats for metamorphosis of the larvae. Similar regulatory pathways, based on exogenous control of a G protein-diacylglycerol cascade, may govern responsiveness to stimuli in other sensory and developmental systems.

Keywords: signal transduction, development, regulation, chemosensory, γ-aminobutyric acid

Full text

PDF
1867

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abood M. E., Hurley J. B., Pappone M. C., Bourne H. R., Stryer L. Functional homology between signal-coupling proteins. Cholera toxin inactivates the GTPase activity of transducin. J Biol Chem. 1982 Sep 25;257(18):10540–10543. [PubMed] [Google Scholar]
  2. Aksamit R. R., Backlund P. S., Jr, Cantoni G. L. Cholera toxin inhibits chemotaxis by a cAMP-independent mechanism. Proc Natl Acad Sci U S A. 1985 Nov;82(22):7475–7479. doi: 10.1073/pnas.82.22.7475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barrowman M. M., Cockcroft S., Gomperts B. D. Two roles for guanine nucleotides in the stimulus-secretion sequence of neutrophils. Nature. 1986 Feb 6;319(6053):504–507. doi: 10.1038/319504a0. [DOI] [PubMed] [Google Scholar]
  4. Breitwieser G. E., Szabo G. Uncoupling of cardiac muscarinic and beta-adrenergic receptors from ion channels by a guanine nucleotide analogue. Nature. 1985 Oct 10;317(6037):538–540. doi: 10.1038/317538a0. [DOI] [PubMed] [Google Scholar]
  5. Cockcroft S., Gomperts B. D. Role of guanine nucleotide binding protein in the activation of polyphosphoinositide phosphodiesterase. Nature. 1985 Apr 11;314(6011):534–536. doi: 10.1038/314534a0. [DOI] [PubMed] [Google Scholar]
  6. Eckstein F., Cassel D., Levkovitz H., Lowe M., Selinger Z. Guanosine 5'-O-(2-thiodiphosphate). An inhibitor of adenylate cyclase stimulation by guanine nucleotides and fluoride ions. J Biol Chem. 1979 Oct 10;254(19):9829–9834. [PubMed] [Google Scholar]
  7. Farley J., Auerbach S. Protein kinase C activation induces conductance changes in Hermissenda photoreceptors like those seen in associative learning. Nature. 1986 Jan 16;319(6050):220–223. doi: 10.1038/319220a0. [DOI] [PubMed] [Google Scholar]
  8. Gilman A. G. G proteins and dual control of adenylate cyclase. Cell. 1984 Mar;36(3):577–579. doi: 10.1016/0092-8674(84)90336-2. [DOI] [PubMed] [Google Scholar]
  9. Hawkins R. D., Abrams T. W., Carew T. J., Kandel E. R. A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. Science. 1983 Jan 28;219(4583):400–405. doi: 10.1126/science.6294833. [DOI] [PubMed] [Google Scholar]
  10. Holz G. G., 4th, Rane S. G., Dunlap K. GTP-binding proteins mediate transmitter inhibition of voltage-dependent calcium channels. Nature. 1986 Feb 20;319(6055):670–672. doi: 10.1038/319670a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hopkins W. F., Johnston D. Frequency-dependent noradrenergic modulation of long-term potentiation in the hippocampus. Science. 1984 Oct 19;226(4672):350–352. doi: 10.1126/science.6091272. [DOI] [PubMed] [Google Scholar]
  12. Hurley J. B., Simon M. I., Teplow D. B., Robishaw J. D., Gilman A. G. Homologies between signal transducing G proteins and ras gene products. Science. 1984 Nov 16;226(4676):860–862. doi: 10.1126/science.6436980. [DOI] [PubMed] [Google Scholar]
  13. KRAVITZ E. A., KUFFLER S. W., POTTER D. D. GAMMA-AMINOBUTYRIC ACID AND OTHER BLOCKING COMPOUNDS IN CRUSTACEA. III. THEIR RELATIVE CONCENTRATIONS IN SEPARATED MOTOR AND INHIBITORY AXONS. J Neurophysiol. 1963 Sep;26:739–751. doi: 10.1152/jn.1963.26.5.739. [DOI] [PubMed] [Google Scholar]
  14. Kopf G. S., Lewis C. A., Vacquier V. D. Regulation of abalone sperm cyclic AMP concentrations and the acrosome reaction by calcium and methylxanthines. Dev Biol. 1983 Jul;98(1):28–36. doi: 10.1016/0012-1606(83)90332-9. [DOI] [PubMed] [Google Scholar]
  15. Manning D. R., Gilman A. G. The regulatory components of adenylate cyclase and transducin. A family of structurally homologous guanine nucleotide-binding proteins. J Biol Chem. 1983 Jun 10;258(11):7059–7063. [PubMed] [Google Scholar]
  16. Merritt J. E., Taylor C. W., Rubin R. P., Putney J. W., Jr Evidence suggesting that a novel guanine nucleotide regulatory protein couples receptors to phospholipase C in exocrine pancreas. Biochem J. 1986 Jun 1;236(2):337–343. doi: 10.1042/bj2360337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Morse D. E., Duncan H., Hooker N., Baloun A., Young G. GABA induces behavioral and developmental metamorphosis in planktonic molluscan larvae. Fed Proc. 1980 Dec;39(14):3237–3241. [PubMed] [Google Scholar]
  18. Morse D. E., Hooker N., Duncan H., Jensen L. ggr-Aminobutyric Acid, a Neurotransmitter, Induces Planktonic Abalone Larvae to Settle and Begin Metamorphosis. Science. 1979 Apr 27;204(4391):407–410. doi: 10.1126/science.204.4391.407. [DOI] [PubMed] [Google Scholar]
  19. Nakamura T., Ui M. Simultaneous inhibitions of inositol phospholipid breakdown, arachidonic acid release, and histamine secretion in mast cells by islet-activating protein, pertussis toxin. A possible involvement of the toxin-specific substrate in the Ca2+-mobilizing receptor-mediated biosignaling system. J Biol Chem. 1985 Mar 25;260(6):3584–3593. [PubMed] [Google Scholar]
  20. Otsuka M., Iversen L. L., Hall Z. W., Kravitz E. A. Release of gamma-aminobutyric acid from inhibitory nerves of lobster. Proc Natl Acad Sci U S A. 1966 Oct;56(4):1110–1115. doi: 10.1073/pnas.56.4.1110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pace U., Lancet D. Olfactory GTP-binding protein: signal-transducing polypeptide of vertebrate chemosensory neurons. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4947–4951. doi: 10.1073/pnas.83.13.4947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pfaffinger P. J., Martin J. M., Hunter D. D., Nathanson N. M., Hille B. GTP-binding proteins couple cardiac muscarinic receptors to a K channel. Nature. 1985 Oct 10;317(6037):536–538. doi: 10.1038/317536a0. [DOI] [PubMed] [Google Scholar]
  23. Trapido-Rosenthal H. G., Morse D. E. Availability of chemosensory receptors is down-regulated by habituation of larvae to a morphogenetic signal. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7658–7662. doi: 10.1073/pnas.83.20.7658. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Volpi M., Naccache P. H., Molski T. F., Shefcyk J., Huang C. K., Marsh M. L., Munoz J., Becker E. L., Sha'afi R. I. Pertussis toxin inhibits fMet-Leu-Phe- but not phorbol ester-stimulated changes in rabbit neutrophils: role of G proteins in excitation response coupling. Proc Natl Acad Sci U S A. 1985 May;82(9):2708–2712. doi: 10.1073/pnas.82.9.2708. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wallace M. A., Fain J. N. Guanosine 5'-O-thiotriphosphate stimulates phospholipase C activity in plasma membranes of rat hepatocytes. J Biol Chem. 1985 Aug 15;260(17):9527–9530. [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES