Skip to main content
SpringerLink
Log in

Stimulus-induced translocation of the protein kinase A catalytic subunit to the apical membrane in blowfly salivary glands

  • Short Communication
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Secretion in blowfly (Calliphora vicina) salivary glands is regulated by the neurohormone serotonin (5-HT), which activates the InsP3/Ca2+ pathway and the cAMP/protein kinase A (PKA) pathway in the secretory cells. The latter signaling cascade induces the activation of a vacuolar H+-ATPase on the apical membrane. Here, we have determined the distribution of PKA by using antibodies against the PKA regulatory subunit-II (PKA-RII) and the PKA catalytic subunit (PKA-C) of Drosophila. PKA is present in high concentrations within the secretory cells. PKA-RII and PKA-C co-distribute in non-stimulated glands, being enriched in the basal portion of the secretory cells. Exposure to 8-CPT-cAMP or 5-HT induces the translocation of PKA-C to the apical membrane, whereas the PKA-RII distribution remains unchanged. The recruitment of PKA-C to the apical membrane corroborates our hypothesis that vacuolar H+-ATPase, which is enriched in this membrane domain, is a target protein for PKA.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Almholt K, Tullin S, Skyggebjerg O, Scudder K, Thastrup O, Terry R (2004) Changes in intracellular cAMP reported by a redistribution assay using a cAMP-dependent protein kinase-green fluorescent protein chimera. Cell Signal 16:907–920

    Article  PubMed  CAS  Google Scholar 

  • Berridge MJ, Heslop JP (1981) Separate 5-hydroxytryptamine receptors on the salivary gland of the blowfly are linked to the generation of either cyclic adenosine 3′,5′-monophosphate or calcium signals. Br J Pharmacol 73:729–738

    PubMed  CAS  Google Scholar 

  • Berridge MJ, Patel NG (1968) Insect salivary glands: stimulation of fluid secretion by 5-hydroxytryptamine and adenosine-3′,5′-monophosphate. Science 162:462–463

    Article  PubMed  CAS  Google Scholar 

  • Canaves JM, Taylor SS (2002) Classification and phylogenetic analysis of the cAMP-dependent protein kinase regulatory subunit family. J Mol Evol 54:17–29

    Article  PubMed  CAS  Google Scholar 

  • Corbin JD, Sugden PH, Lincoln TM, Keely SL (1977) Compartmentalization of adenosine 3′:5′-monophosphate and adenosine 3′:5′-monophosphate-dependent protein kinase in heart tissue. J Biol Chem 252:3854–3861

    PubMed  CAS  Google Scholar 

  • Dames P, Zimmermann B, Schmidt R, Rein J, Voss M, Schewe B, Walz B, Baumann O (2006) cAMP regulates plasma membrane vacuolar-type H+-ATPase assembly and activity in blowfly salivary glands. Proc Natl Acad Sci USA 103:3926–3931

    Article  PubMed  CAS  Google Scholar 

  • Eisenhardt D, Kühn C, Leboulle G (2006) The PKA-CREB system encoded by the honeybee genome. Insect Mol Biol 15:551–561

    Article  PubMed  CAS  Google Scholar 

  • Feliciello A, Gottesman ME, Avvedimento EV (2001) The biological functions of A-kinase anchor proteins. J Mol Biol 308:99–114

    Article  PubMed  CAS  Google Scholar 

  • Foster JL, Guttman JJ, Hall LM, Rosen OM (1984) Drosophila cAMP-dependent protein kinase. J Biol Chem 259:13049–13055

    PubMed  CAS  Google Scholar 

  • Inoue H, Yoshioka T (1997) Purification of a regulatory subunit of type II cAMP-dependent protein kinase from Drosophila heads. Biochem Biophys Res Commun 235:223–226

    Article  PubMed  CAS  Google Scholar 

  • Lane ME, Kalderon D (1993) Genetic investigation of cAMP-dependent protein kinase function in Drosophila development. Genes Dev 7:1229–1243

    Article  PubMed  CAS  Google Scholar 

  • Meinkoth JL, Ji Y, Taylor SS, Feramisco JR (1990) Dynamics of the distribution of cyclic AMP-dependent protein kinase in living cells. Proc Natl Acad Sci USA 87:9595–9599

    Article  PubMed  CAS  Google Scholar 

  • Meinkoth JL, Alberts AS, Went W, Fantozzi D, Taylor SS, Hagiwara M, Montminy M, Feramisco JR (1993) Signal transduction through the cAMP-dependent protein kinase. Mol Cell Biochem 127:179–186

    Article  PubMed  Google Scholar 

  • Müller U (1997) Neuronal cAMP-dependent protein kinase type II is concentrated in mushroom bodies of Drosophila melanogaster and the honeybee Apis mellifera. J Neurobiol 33:33–44

    Article  PubMed  Google Scholar 

  • Müller U, Spatz HC (1989) Ca2+-dependent proteolytic modification of the cAMP-dependent protein kinase in Drosophila wild-type and dunce memory mutants. J Neurogenet 6:95–114

    Article  PubMed  Google Scholar 

  • Rein J, Voss M, Blenau W, Walz B, Baumann O (2008) Hormone-induced assembly and activation of V-ATPase in blowfly salivary glands is mediated by protein kinase A. Am J Physiol Cell Physiol 294:C56–C65

    Article  PubMed  CAS  Google Scholar 

  • Rotte C, Walz B, Baumann O (2008) Morphological and functional characterization of the thoracic portion of blowfly salivary glands. Arthropod Struct Dev 37:372–382

    Article  PubMed  CAS  Google Scholar 

  • Sastri M, Barraclough DM, Carmichael PT, Taylor SS (2005) A-kinase-interacting protein localizes protein kinase A in the nucleus. Proc Natl Acad Sci USA 102:349–354

    Article  PubMed  CAS  Google Scholar 

  • Skoulakis EM, Kalderon D, Davis RL (1993) Preferential expression in mushroom bodies of the catalytic subunit of protein kinase A and its role in learning and memory. Neuron 11:197–208

    Article  PubMed  CAS  Google Scholar 

  • Takeyasu K, Tamkun MM, Renaud KJ, Fambrough DM (1988) Ouabain-sensitive (Na+ + K+)-ATPase activity expressed in mouse L cells by transfection with DNA encoding the alpha-subunit of an avian sodium pump. J Biol Chem 263:4347–4354

    PubMed  CAS  Google Scholar 

  • Taskén K, Aandahl EM (2004) Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol Rev 84:137–167

    Article  PubMed  Google Scholar 

  • Taylor SS, Buechler JA, Yonemoto W (1990) cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu Rev Biochem 59:971–1005

    Article  PubMed  CAS  Google Scholar 

  • Taylor SS, Yang J, Wu J, Haste NM, Radzio-Andzelm E, Anand G (2004) PKA: a portrait of protein kinase dynamics. Biochim Biophys Acta 1697:259–269

    PubMed  CAS  Google Scholar 

  • Voss M, Vitavska O, Walz B, Wieczorek H, Baumann O (2007) Stimulus-induced phosphorylation of V-ATPase by protein kinase A. J Biol Chem 282:33735–33742

    Article  PubMed  CAS  Google Scholar 

  • Wong W, Scott JD (2004) AKAP signalling complexes: focal points in space and time. Nat Rev Mol Cell Biol 5:959–970

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann B (2000) Subcellular organization of agonist-evoked Ca2+ waves in the blowfly salivary gland. Cell Calcium 27:297–307

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann B, Walz B (1997) Serotonin-induced intercellular calcium waves in salivary glands of the blowfly Calliphora erythrocephala. J Physiol (Lond) 500:17–28

    CAS  Google Scholar 

  • Zimmermann B, Somlyo AV, Ellis-Davies GC, Kaplan JH, Somlyo AP (1995) Kinetics of prephosphorylation reactions and myosin light chain phosphorylation in smooth muscle. Flash photolysis studies with caged calcium and caged ATP. J Biol Chem 270:23966–23974

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann B, Dames P, Walz B, Baumann O (2003) Distribution and serotonin-induced activation of vacuolar-type H+-ATPase in the salivary glands of the blowfly Calliphora vicina. J Exp Biol 206:1867–1876

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Daniel Kalderon and Kunio Takeyasu for providing antibodies and to Mrs. Bärbel Wuntke for technical assistance.

Author information

Authors and Affiliations

  1. Institut für Biochemie und Biologie, Universität Potsdam, Karl-Liebknecht-Strasse 24–25, 14476, Potsdam, Germany

    Martin Voss, Ruth Schmidt, Bernd Walz & Otto Baumann

Authors
  1. Martin Voss
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ruth Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bernd Walz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Otto Baumann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Otto Baumann.

Additional information

This work was supported by grants Wa463/9–5 and GRK837 from the Deutsche Forschungsgemeinschaft.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Voss, M., Schmidt, R., Walz, B. et al. Stimulus-induced translocation of the protein kinase A catalytic subunit to the apical membrane in blowfly salivary glands. Cell Tissue Res 335, 657–662 (2009). https://doi.org/10.1007/s00441-008-0673-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-008-0673-x

Keywords

Search

Navigation