Skip to main content
Plant Physiology logoLink to Plant Physiology
. 1995 Mar;107(3):845–856. doi: 10.1104/pp.107.3.845

The effects of mastoparan on the carrot cell plasma membrane polyphosphoinositide phospholipase C.

M H Cho 1, Z Tan 1, C Erneux 1, S B Shears 1, W F Boss 1
PMCID: PMC157201  PMID: 7716245

Abstract

When [3H]inositol-labeled carrot (Daucus carota L.) cells were treated with 10 or 25 microM wasp venom peptide mastoparan or the active analog Mas-7 there was a rapid loss of more than 70% of [3H]phosphatidylinositol-4-monophosphate (PIP) and [3H]phosphatidylinositol-4,5-bisphosphate (PIP2) and a 3- and 4-fold increase in [3H]inositol-1,4-P2 and [3H]inositol-1,4,5-P3, respectively. The identity of [3H]inositol-1,4,5-P3 was confirmed by phosphorylation with inositol-1,4,5-P3 3-kinase and co-migration with inositol-1,3,4,5-P4. The changes in phosphoinositides were evident within 1 min. The loss of [3H]PIP was evident only when cells were treated with the higher concentrations (10 and 25 microM) of mastoparan or Mas-7. At 1 microM Mas-7, [3H]PIP increased. The inactive mastoparan analog Mas-17 had little or no effect on [3H]PIP or [3H]PIP2 hydrolysis in vivo. Neomycin (100 microM) inhibited the uptake of Mas-7 and thereby inhibited the Mas-7-stimulated hydrolysis of [3H]PIP and [3H]PIP2. Plasma membranes isolated from mastoparan-treated cells had increased PIP-phospholipase C (PLC) activity. However, when Mas-7 was added to isolated plasma membranes from control cells, it had no effect on PIP-PLC activity at low concentrations and inhibited PIP-PLC at concentrations greater than 10 microM. In addition, guanosine-5'-O-(3-thiotriphosphate) had no effect on the PIP-PLC activity when added to plasma membranes isolated from either the Mas-7-treated or control cells. The fact that Mas-7 did not stimulate PIP-PLC activity in vitro indicated that the Mas-7-induced increase in PIP-PLC in vivo required a factor that was lost from the membrane during isolation.

Full Text

The Full Text of this article is available as a PDF (1.7 MB).

Selected References

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

  1. Aderem A. Signal transduction and the actin cytoskeleton: the roles of MARCKS and profilin. Trends Biochem Sci. 1992 Oct;17(10):438–443. doi: 10.1016/0968-0004(92)90016-3. [DOI] [PubMed] [Google Scholar]
  2. Argiolas A., Pisano J. J. Facilitation of phospholipase A2 activity by mastoparans, a new class of mast cell degranulating peptides from wasp venom. J Biol Chem. 1983 Nov 25;258(22):13697–13702. [PubMed] [Google Scholar]
  3. Aridor M., Rajmilevich G., Beaven M. A., Sagi-Eisenberg R. Activation of exocytosis by the heterotrimeric G protein Gi3. Science. 1993 Dec 3;262(5139):1569–1572. doi: 10.1126/science.7504324. [DOI] [PubMed] [Google Scholar]
  4. Balch W. E. Small GTP-binding proteins in vesicular transport. Trends Biochem Sci. 1990 Dec;15(12):473–477. doi: 10.1016/0968-0004(90)90301-q. [DOI] [PubMed] [Google Scholar]
  5. Berridge M. J., Dawson R. M., Downes C. P., Heslop J. P., Irvine R. F. Changes in the levels of inositol phosphates after agonist-dependent hydrolysis of membrane phosphoinositides. Biochem J. 1983 May 15;212(2):473–482. doi: 10.1042/bj2120473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Berridge M. J., Irvine R. F. Inositol phosphates and cell signalling. Nature. 1989 Sep 21;341(6239):197–205. doi: 10.1038/341197a0. [DOI] [PubMed] [Google Scholar]
  7. Chauhan A., Chauhan V. P., Deshmukh D. S., Brockerhoff H. Phosphatidylinositol 4,5-bisphosphate competitively inhibits phorbol ester binding to protein kinase C. Biochemistry. 1989 Jun 13;28(12):4952–4956. doi: 10.1021/bi00438a007. [DOI] [PubMed] [Google Scholar]
  8. Chauhan V. P., Brockerhoff H. Phosphatidylinositol-4,5-bisphosphate may antecede diacylglycerol as activator of protein kinase C. Biochem Biophys Res Commun. 1988 Aug 30;155(1):18–23. doi: 10.1016/s0006-291x(88)81043-x. [DOI] [PubMed] [Google Scholar]
  9. Cockcroft S., Thomas G. M. Inositol-lipid-specific phospholipase C isoenzymes and their differential regulation by receptors. Biochem J. 1992 Nov 15;288(Pt 1):1–14. doi: 10.1042/bj2880001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Craxton A., Erneux C., Shears S. B. Inositol 1,4,5,6-tetrakisphosphate is phosphorylated in rat liver by a 3-kinase that is distinct from inositol 1,4,5-trisphosphate 3-kinase. J Biol Chem. 1994 Feb 11;269(6):4337–4342. [PubMed] [Google Scholar]
  11. Drobak B. K. Plant Phosphoinositides and Intracellular Signaling. Plant Physiol. 1993 Jul;102(3):705–709. doi: 10.1104/pp.102.3.705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fairley-Grenot K., Assmann S. M. Evidence for G-Protein Regulation of Inward K+ Channel Current in Guard Cells of Fava Bean. Plant Cell. 1991 Sep;3(9):1037–1044. doi: 10.1105/tpc.3.9.1037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gil J., Higgins T., Rozengurt E. Mastoparan, a novel mitogen for Swiss 3T3 cells, stimulates pertussis toxin-sensitive arachidonic acid release without inositol phosphate accumulation. J Cell Biol. 1991 May;113(4):943–950. doi: 10.1083/jcb.113.4.943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hetherington A. M., Drøbak B. K. Inositol-containing lipids in higher plants. Prog Lipid Res. 1992;31(1):53–63. doi: 10.1016/0163-7827(92)90015-b. [DOI] [PubMed] [Google Scholar]
  15. Higashijima T., Burnier J., Ross E. M. Regulation of Gi and Go by mastoparan, related amphiphilic peptides, and hydrophobic amines. Mechanism and structural determinants of activity. J Biol Chem. 1990 Aug 25;265(24):14176–14186. [PubMed] [Google Scholar]
  16. Higashijima T., Ross E. M. Mapping of the mastoparan-binding site on G proteins. Cross-linking of [125I-Tyr3,Cys11]mastoparan to Go. J Biol Chem. 1991 Jul 5;266(19):12655–12661. [PubMed] [Google Scholar]
  17. Hillaire-Buys D., Mousli M., Landry Y., Bockaert J., Fehrentsz J. A., Carrette J., Rouot B. Insulin releasing effects of mastoparan and amphiphilic substance P receptor antagonists on RINm5F insulinoma cells. Mol Cell Biochem. 1992 Feb 12;109(2):133–138. doi: 10.1007/BF00229767. [DOI] [PubMed] [Google Scholar]
  18. Irvine R. F., Letcher A. J., Dawson R. M. Phosphatidylinositol phosphodiesterase in higher plants. Biochem J. 1980 Oct 15;192(1):279–283. doi: 10.1042/bj1920279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Joyce-Brady M., Rubins J. B., Panchenko M. P., Bernardo J., Steele M. P., Kolm L., Simons E. R., Dickey B. F. Mechanisms of mastoparan-stimulated surfactant secretion from isolated pulmonary alveolar type 2 cells. J Biol Chem. 1991 Apr 15;266(11):6859–6865. [PubMed] [Google Scholar]
  20. Knight M. R., Smith S. M., Trewavas A. J. Wind-induced plant motion immediately increases cytosolic calcium. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):4967–4971. doi: 10.1073/pnas.89.11.4967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Komatsu M., McDermott A. M., Gillison S. L., Sharp G. W. Mastoparan stimulates exocytosis at a Ca(2+)-independent late site in stimulus-secretion coupling. Studies with the RINm5F beta-cell line. J Biol Chem. 1993 Nov 5;268(31):23297–23306. [PubMed] [Google Scholar]
  22. Li W., Assmann S. M. Characterization of a G-protein-regulated outward K+ current in mesophyll cells of vicia faba L. Proc Natl Acad Sci U S A. 1993 Jan 1;90(1):262–266. doi: 10.1073/pnas.90.1.262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Marks P. W., Maxfield F. R. Preparation of solutions with free calcium concentration in the nanomolar range using 1,2-bis(o-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid. Anal Biochem. 1991 Feb 15;193(1):61–71. doi: 10.1016/0003-2697(91)90044-t. [DOI] [PubMed] [Google Scholar]
  24. Melin P. M., Sommarin M., Sandelius A. S., Jergil B. Identification of Ca2+-stimulated polyphosphoinositide phospholipase C in isolated plant plasma membranes. FEBS Lett. 1987 Oct 19;223(1):87–91. doi: 10.1016/0014-5793(87)80515-x. [DOI] [PubMed] [Google Scholar]
  25. Memon A. R., Chen Q. Y., Boss W. F. Inositol phospholipids activate plasma membrane ATPase in plants. Biochem Biophys Res Commun. 1989 Aug 15;162(3):1295–1301. doi: 10.1016/0006-291x(89)90814-0. [DOI] [PubMed] [Google Scholar]
  26. Memon A. R., Clark G. B., Thompson G. A., Jr Identification of an ARF type low molecular mass GTP-binding protein in pea (Pisum sativum). Biochem Biophys Res Commun. 1993 Jun 30;193(3):809–813. doi: 10.1006/bbrc.1993.1697. [DOI] [PubMed] [Google Scholar]
  27. Memon A. R., Herrin D. L., Thompson G. A., Jr Intracellular translocation of a 28 kDa GTP-binding protein during osmotic shock-induced cell volume regulation in Dunaliella salina. Biochim Biophys Acta. 1993 Oct 7;1179(1):11–22. doi: 10.1016/0167-4889(93)90070-6. [DOI] [PubMed] [Google Scholar]
  28. Michell R. H. Inositol lipids in cellular signalling mechanisms. Trends Biochem Sci. 1992 Aug;17(8):274–276. doi: 10.1016/0968-0004(92)90433-a. [DOI] [PubMed] [Google Scholar]
  29. Missiaen L., Wuytack F., Raeymaekers L., De Smedt H., Casteels R. Polyamines and neomycin inhibit the purified plasma-membrane Ca2+ pump by interacting with associated polyphosphoinositides. Biochem J. 1989 Aug 1;261(3):1055–1058. doi: 10.1042/bj2611055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Pfaffmann H., Hartmann E., Brightman A. O., Morré D. J. Phosphatidylinositol specific phospholipase C of plant stems : membrane associated activity concentrated in plasma membranes. Plant Physiol. 1987 Dec;85(4):1151–1155. doi: 10.1104/pp.85.4.1151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pical C., Sandelius A. S., Melin P. M., Sommarin M. Polyphosphoinositide Phospholipase C in Plasma Membranes of Wheat (Triticum aestivum L.) : Orientation of Active Site and Activation by Ca and Mg. Plant Physiol. 1992 Nov;100(3):1296–1303. doi: 10.1104/pp.100.3.1296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Quarmby L. M., Hartzell H. C. Two distinct, calcium-mediated, signal transduction pathways can trigger deflagellation in Chlamydomonas reinhardtii. J Cell Biol. 1994 Mar;124(5):807–815. doi: 10.1083/jcb.124.5.807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Quarmby L. M., Yueh Y. G., Cheshire J. L., Keller L. R., Snell W. J., Crain R. C. Inositol phospholipid metabolism may trigger flagellar excision in Chlamydomonas reinhardtii. J Cell Biol. 1992 Feb;116(3):737–744. doi: 10.1083/jcb.116.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schacht J. Purification of polyphosphoinositides by chromatography on immobilized neomycin. J Lipid Res. 1978 Nov;19(8):1063–1067. [PubMed] [Google Scholar]
  35. Siess W., Lapetina E. G. Neomycin inhibits inositol phosphate formation in human platelets stimulated by thrombin but not other agonists. FEBS Lett. 1986 Oct 20;207(1):53–57. doi: 10.1016/0014-5793(86)80011-4. [DOI] [PubMed] [Google Scholar]
  36. Simon M. I., Strathmann M. P., Gautam N. Diversity of G proteins in signal transduction. Science. 1991 May 10;252(5007):802–808. doi: 10.1126/science.1902986. [DOI] [PubMed] [Google Scholar]
  37. Smrcka A. V., Hepler J. R., Brown K. O., Sternweis P. C. Regulation of polyphosphoinositide-specific phospholipase C activity by purified Gq. Science. 1991 Feb 15;251(4995):804–807. doi: 10.1126/science.1846707. [DOI] [PubMed] [Google Scholar]
  38. Staiger C. J., Goodbody K. C., Hussey P. J., Valenta R., Drøbak B. K., Lloyd C. W. The profilin multigene family of maize: differential expression of three isoforms. Plant J. 1993 Oct;4(4):631–641. doi: 10.1046/j.1365-313x.1993.04040631.x. [DOI] [PubMed] [Google Scholar]
  39. Sternweis P. C., Smrcka A. V. Regulation of phospholipase C by G proteins. Trends Biochem Sci. 1992 Dec;17(12):502–506. doi: 10.1016/0968-0004(92)90340-f. [DOI] [PubMed] [Google Scholar]
  40. Takazawa K., Vandekerckhove J., Dumont J. E., Erneux C. Cloning and expression in Escherichia coli of a rat brain cDNA encoding a Ca2+/calmodulin-sensitive inositol 1,4,5-trisphosphate 3-kinase. Biochem J. 1990 Nov 15;272(1):107–112. doi: 10.1042/bj2720107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Tan Z., Boss W. F. Association of Phosphatidylinositol Kinase, Phosphatidylinositol Monophosphate Kinase, and Diacylglycerol Kinase with the Cytoskeleton and F-Actin Fractions of Carrot (Daucus carota L.) Cells Grown in Suspension Culture : Response to Cell Wall-Degrading Enzymes. Plant Physiol. 1992 Dec;100(4):2116–2120. doi: 10.1104/pp.100.4.2116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Tate B. F., Schaller G. E., Sussman M. R., Crain R. C. Characterization of a Polyphosphoinositide Phospholipase C from the Plasma Membrane of Avena sativa. Plant Physiol. 1989 Dec;91(4):1275–1279. doi: 10.1104/pp.91.4.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Taylor S. J., Chae H. Z., Rhee S. G., Exton J. H. Activation of the beta 1 isozyme of phospholipase C by alpha subunits of the Gq class of G proteins. Nature. 1991 Apr 11;350(6318):516–518. doi: 10.1038/350516a0. [DOI] [PubMed] [Google Scholar]
  44. Tysnes O. B., Steen V. M., Holmsen H. Neomycin inhibits platelet functions and inositol phospholipid metabolism upon stimulation with thrombin, but not with ionomycin or 12-O-tetradecanoyl-phorbol 13-acetate. Eur J Biochem. 1988 Oct 15;177(1):219–223. doi: 10.1111/j.1432-1033.1988.tb14365.x. [DOI] [PubMed] [Google Scholar]
  45. Van Rooijen L. A., Agranoff B. W. Inhibition of polyphosphoinositide phosphodiesterase by aminoglycoside antibiotics. Neurochem Res. 1985 Aug;10(8):1019–1024. doi: 10.1007/BF00965878. [DOI] [PubMed] [Google Scholar]
  46. Wheeler-Jones C. P., Saermark T., Kakkar V. V., Authi K. S. Mastoparan promotes exocytosis and increases intracellular cyclic AMP in human platelets. Evidence for the existence of a Ge-like mechanism of secretion. Biochem J. 1992 Jan 15;281(Pt 2):465–472. doi: 10.1042/bj2810465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Wilson S. P. Effects of mastoparan on catecholamine release from chromaffin cells. FEBS Lett. 1989 Apr 24;247(2):239–241. doi: 10.1016/0014-5793(89)81343-2. [DOI] [PubMed] [Google Scholar]
  48. Wojcikiewicz R. J., Nahorski S. R. Phosphoinositide hydrolysis in permeabilized SH-SY5Y human neuroblastoma cells is inhibited by mastoparan. FEBS Lett. 1989 Apr 24;247(2):341–344. doi: 10.1016/0014-5793(89)81366-3. [DOI] [PubMed] [Google Scholar]
  49. Yang W., Boss W. F. Regulation of phosphatidylinositol 4-kinase by the protein activator PIK-A49. Activation requires phosphorylation of PIK-A49. J Biol Chem. 1994 Feb 4;269(5):3852–3857. [PubMed] [Google Scholar]
  50. Yazawa M., Ikura M., Hikichi K., Ying L., Yagi K. Communication between two globular domains of calmodulin in the presence of mastoparan or caldesmon fragment. Ca2+ binding and 1H NMR. J Biol Chem. 1987 Aug 15;262(23):10951–10954. [PubMed] [Google Scholar]
  51. Yokokawa N., Komatsu M., Takeda T., Aizawa T., Yamada T. Mastoparan, a wasp venom, stimulates insulin release by pancreatic islets through pertussis toxin sensitive GTP-binding protein. Biochem Biophys Res Commun. 1989 Feb 15;158(3):712–716. doi: 10.1016/0006-291x(89)92779-4. [DOI] [PubMed] [Google Scholar]
  52. Yule D. I., Williams J. A. Mastoparan induces oscillations of cytosolic Ca2+ in rat pancreatic acinar cells. Biochem Biophys Res Commun. 1991 May 31;177(1):159–165. doi: 10.1016/0006-291x(91)91962-c. [DOI] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES