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Plant Biol (Stuttg) 2002; 4(1): 53-61
DOI: 10.1055/s-2002-20436
Original Paper
Georg Thieme Verlag Stuttgart ·New York

Nutrients Induce an Increase in Inositol 1,4,5-Trisphosphate in Soybean Cells: Implication for the Involvement of Phosphoinositide-Specific Phospholipase C in DNA Synthesis

T. Shigaki 1, 2 , M. K. Bhattacharyya 1, 3
  • 1 Plant Biology Division, Samuel Roberts Noble Foundation, 2510 Sam Noble Parkway, Ardmore, Oklahoma 73401, USA
  • 2 New address: Plant Physiology Laboratories, Children's Nutrition Research Center, Baylor College of Medicine, 1100 Bates St., Houston, Texas, USA
  • 3 New address: G303 Agronomy Hall, Department of Agronomy, Iowa State University, Ames, Iowa, USA
Further Information

Publication History

August 7, 2001

December 18, 2001

Publication Date:
28 February 2002 (online)

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Abstract

Phosphoinositide-specific phospholipase C (PI-PLC) hydrolyzes the membrane lipid phosphatidylinositol 4,5-bisphosphate (PtdInsP2) to generate 1,2-diacylglycerol (DAG) and inositol 1,4,5-trisphosphate (InsP3). Both molecules serve as second messengers to carry out various cellular functions in mammals. In the present study, we demonstrate that many organic and inorganic nutrients cause the elevation of InsP3 concentrations in cultured soybean cells. This elevation of InsP3 content is sustained for several hours following treatment with Murashige-Skoog (MS) inorganic nutrients. Phosphate and calcium are the major components in MS salts responsible for the increase in InsP3 levels. DNA synthesis, a measure of cell growth, was significantly suppressed by the PI-PLC-specific inhibitor 1-(6-{[17β-3-methoxyestra-1,3,5(10)-trien-17-yl]amino}hexyl)-1H-pyrrole-2,5-dione (U-73122), whereas its near-identical analogue 1-(6-{[17β-3-methoxyestra-1,3,5(10)-trien-17-yl]amino}hexyl)-2,5-pyrrolidinedione did not cause any suppression. Activation of PI-PLC by MS salts increased DNA synthesis and abolished the suppression of DNA synthesis caused by U-73122. Thus, we conclude that the higher cellular concentration of InsP3 induced by MS treatment is involved in DNA synthesis.

Abbreviations

DAG: 1,2-diacylglycerol

InsP3: inositol 1,4,5-trisphosphate

PtdInsP2: phosphatidylinositol 4,5-bisphosphate

PI-PLC: phosphoinositide-specific phospholipase C

Key words

InsP3 - phospholipase C - signal transduction - soybean

References

  • 01 Bala,  G. A.,, Thakur,  N. R.,, and Bleasdale,  J. E.. (1990);  Characterization of the major phosphoinositide-specific phospholipase C of human amnion.  Biology of Reproduction. 43 704-711
    Google Scholar
  • 02 Beekman,  A.,, Helfrich,  B.,, Bunn,  J. P. A.,, and Heasley,  L. E.. (1998);  Expression of catalytically inactive phospholipase Cβ disrupts phospholipase Cβ and mitogen-activated protein kinase signaling and inhibits small cell lung cancer growth.  Cancer Research. 58 910-913
    Google Scholar
  • 03 Berridge,  M. J.. (1993);  Inositol trisphosphate and calcium signalling.  Nature. 361 315-325
    Google Scholar
  • 04 Bleasdale,  J. E.,, Thakur,  N. R.,, Gremban,  R. S.,, Bundy,  G. L.,, Fitzpatrick,  F. A.,, Smith,  R. J.,, and Bunting,  S.. (1990);  Selective inhibition of receptor-coupled phospholipase C-dependent processes in human platelets and polymorphonuclear neutrophios.  Journal of Pharmacology and Experimental Therapeutics. 255 756-768
    Google Scholar
  • 05 Brearley,  C. A.,, Parmar,  P. N.,, and Hanke,  D. E.. (1997);  Metabolic evidence for PtdIns(4,5)P2-directed phospholipase C in permeabilized plant protoplasts.  Biochemical Journal. 324 123-131
    Google Scholar
  • 06 Bronner,  C.,, Wiggins,  C.,, Monté,  D.,, Märki,  F.,, Capron,  A.,, Landry,  Y.,, and Franson,  R. C.. (1987);  Compound 48/80 is a potent inhibitor of phospholipase C and a dual modulator of phospholipase A2 from human platelet.  Biochimica et Biophysica Acta. 920 301-305
    Google Scholar
  • 07 Coté,  G. G., and Crain,  R. C.. (1993);  Biochemistry of phosphoinositides.  Annual Review of Plant Physiology and Plant Molecular Biology. 44 333-356
    Google Scholar
  • 08 Dennis,  E. A.. (1983) Phospholipases. The Enzymes, Vol. 16. Boyer, P. D., ed. New York, NY; Academic Press pp. 307-353
    Google Scholar
  • 09 Drayer,  A. L.,, Van der Kaay,  J.,, Mayr,  G. W.,, and Van Haastert,  P. J.. (1994);  Role of phospholipase C in Dictyostelium: formation of inositol 1,4,5-trisphosphate and normal development in cells lacking phospholipase C activity.  EMBO Journal. 13 1601-1609
    Google Scholar
  • 10 Drøbak,  B. K.,, Watkins,  P. A. C.,, Chattaway,  J. A.,, Roberts,  K.,, and Dawson,  A. P.. (1991);  Metabolism of inositol (1,4,5)trisphosphate by a soluble enzyme fraction from pea (Pisum sativum) roots.  Plant Physiology. 95 412-419
    PubMedGoogle Scholar
  • 11 Ettlinger,  C., and Lehle,  L.. (1988);  Auxin induces rapid changes in phosphatidylinositol metabolites.  Nature. 331 176-178
    CrossrefPubMedGoogle Scholar
  • 12 Flick,  J. S., and Thorner,  J.. (1993);  Genetic and biochemical characterization of a phosphatidylinositol-specific phospholipase C in Saccharomyces cerevisiae. .  Molecular and Cellular Biology. 13 5861-5876
    PubMedGoogle Scholar
  • 13 Franklin-Tong,  V. E.,, Drøbak,  B. K.,, Allan,  A. C.,, Watkins,  P. A. C.,, and Trewavas,  A. J.. (1996);  Growth of pollen tubes of Papaver rhoeas is regulated by a slow-moving calcium wave propagated by inositol 1,4,5-trisphosphate.  Plant Cell. 8 1305-1321
    CrossrefPubMedGoogle Scholar
  • 14 Gietzen,  K.. (1983);  Comparison of the calmodulin antagonists compound 48/80 and calmidazolium.  Biochemical Journal. 216 611-616
    PubMedGoogle Scholar
  • 15 Hartweck,  L. M.,, Llewellyn,  D. J.,, and Dennis,  E. S.. (1997);  The Arabidopsis thaliana genome has multiple divergent forms of phosphoinoisitol-specific phospholipase C.  Gene. 202 151-156
    CrossrefPubMedGoogle Scholar
  • 16 Heilmann,  I.,, Perera,  I. Y.,, Gross,  W.,, and Boss,  W. F.. (1999);  Changes in phosphoinositide metabolism with days in culture affect signal transduction pathways in Galdieria sulphuraria. .  Plant Physiology. 119 1331-1339
    CrossrefPubMedGoogle Scholar
  • 17 Hirayama,  T.,, Mitsukawa,  N.,, Shibata,  D.,, and Shinozaki,  K.. (1997);  AtPLC2, a gene encoding phosphoinositide-specific phospholipase C, is constitutively expressed in vegetative and floral tissues in Arabidopsis thaliana. .  Plant Molecular Biology. 34 175-180
    CrossrefPubMedGoogle Scholar
  • 18 Hirayama,  T.,, Ohto,  C.,, Mizocguchi,  T.,, and Shinozaki,  K.. (1995);  A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. .  Proceedings of the National Academy of Sciences of the United States of America. 92 3903-3907
    PubMedGoogle Scholar
  • 19 Hirose,  K.,, Kadowaki,  S.,, Tanabe,  M.,, Takeshima,  H.,, and Iino,  M.. (1999);  Spatiotemporal dynamics of inositol 1,4,5-trisphosphate that underlies complex Ca2+ mobilization patterns.  Science. 284 1527-1530
    CrossrefPubMedGoogle Scholar
  • 20 Irvine,  R. F.,, Ånggård,  E. E.,, Letcher,  A. J.,, and Downes,  C. P.. (1985);  Metabolism of inositol 1,4,5-trisphosphate and inositol 1,3,4-trisphosphate in rat parotid glands.  Biochemical Journal. 229 505-511
    PubMedGoogle Scholar
  • 21 Jones,  D. L., and Kochian,  L. V.. (1995);  Aluminum inhibition of the inositol 1,4,5-trisphosphate signal transduction pathway in wheat roots: A role in aluminum toxicity?.  Plant Cell. 7 1913-1922
    CrossrefPubMedGoogle Scholar
  • 22 Joseph,  S. K.,, Esch,  T.,, and Bonner,  W. D.. (1989);  Hydrolysis of inositol phosphates by plant cell extracts.  Biochemical Journal. 264 851-856
    PubMedGoogle Scholar
  • 23 Kamada,  Y., and Muto,  S.. (1994);  Stimulation by fungal elicitor of inositol phospholipid turnover in tobacco suspension culture cells.  Plant and Cell Physiology. 35 397-404
    PubMedGoogle Scholar
  • 24 Knight,  H.,, Trewavas,  A. J.,, and Knight,  M. R.. (1997);  Calcium signalling in Arabidopsis thaliana responding to drought and salinity.  Plant Journal. 12 1067-1078
    CrossrefPubMedGoogle Scholar
  • 25 Koch,  W.,, Wagner,  C.,, and Seitz,  H. U.. (1998);  Elicitor-induced cell death and phytoalexin synthesis in Daucus carota L.  Planta. 206 523-532
    CrossrefPubMedGoogle Scholar
  • 26 Kopka,  J.,, Pical,  C.,, Gray,  J. E.,, and Müller-Röber,  B.. (1998);  Molecular and enzymatic characterization of three phosphoinoside-specific phospholipase C isoforms from potato.  Plant Physiology. 116 239-250
    CrossrefPubMedGoogle Scholar
  • 27 Lee,  Y.,, Choi,  Y. B.,, Suh,  S.,, Lee,  J.,, Assmann,  S. M.,, Joe,  C. O.,, Kelleher,  J. F.,, and Crain,  R. C.. (1996);  Abscisic acid-induced phosphoinositide turnover in guard cell protoplasts of Vicia faba. .  Plant Physiology. 110 987-996
    PubMedGoogle Scholar
  • 28 Legendre,  L.,, Yueh,  Y. G.,, Crain,  R.,, Haddock,  N.,, Heinstein,  P. F.,, and Low,  P. S.. (1993);  Phospolipase C activation during elicitation of the oxidative burst in cultured plant cells.  Journal of Biological Chemistry. 268 24559-24563
    PubMedGoogle Scholar
  • 29 Loewus,  F. A., and Loewus,  M. W.. (1980) myo-Inositol: biosynthesis and metabolism. The Biochemistry of Plants, Vol. 3. New York, NY; Academic Press pp. 43-76
    Google Scholar
  • 30 Majerus,  P.. (1992);  Inositol phosphate biochemistry.  Annual Review of Biochemistry. 61 225-250
    CrossrefPubMedGoogle Scholar
  • 31 Martinoia,  E.,, Locher,  R.,, and Vogt,  E.. (1993);  Inositol trisphosphate metabolism in subcellular fractions of barley (Hordeum vulgare L.) mesophyll cells.  Plant Physiology. 102 101-105
    PubMedGoogle Scholar
  • 32 Memon,  A. R.,, Rincon,  M.,, and Boss,  W. F.. (1989);  Inositol trisphosphate metabolism in carrot (Daucus carota L.) cells.  Plant Physiology. 91 477-480
    PubMedGoogle Scholar
  • 33 Morse,  M. J.,, Crain,  R. C.,, Coté,  G. G.,, and Satter,  R. L.. (1989);  Light-stimulated inositol phospholipid turnover in Samanea saman pulvini. Increased levels of diacylglycerol.  Plant Physiology. 89 724-727
    PubMedGoogle Scholar
  • 34 Morse,  M. J.,, Crain,  R. C.,, and Satter,  R. L.. (1987);  Light-stimulated inositolphospholipid turnover in Samanea saman leaf pulvini.  Proceedings of the National Academy of Sciences of the United States of America. 84 7075-7078
    PubMedGoogle Scholar
  • 35 Munnik,  T.,, Irvine,  R. F.,, and Musgrave,  A.. (1998);  Phospholipid signalling in plants.  Biochimica et Biophysica Acta. 1389 222-272
    PubMedGoogle Scholar
  • 36 Murashige,  T., and Skoog,  F.. (1962);  A revised medium for rapid growth and bioassays with tobacco tissue cultures.  Physiologia Plantarum. 15 473-497
    PubMedGoogle Scholar
  • 37 Nebigil,  C. G.. (1997);  Suppression of phospholipase C beta, gamma, and delta families alters cell growth and phosphatidylinositol 4,5-bisphosphate levels.  Biochemistry. 36 15949-15958
    CrossrefPubMedGoogle Scholar
  • 38 Perera,  I. Y.,, Heilmann,  I. H.,, and Boss,  W. F.. (1999);  Transient and sustained increases in inositol 1,4,5-trisphosphate precede the differential growth response in gravistimulated maize pulvini.  Proceedings of the National Academy of Sciences of the United States of America. 96 5838-5843
    CrossrefPubMedGoogle Scholar
  • 39 Pical,  C.,, Kopka,  J.,, Müller-Röber,  B.,, Hetherington,  A. M.,, and Gray,  J. E.. (1997);  Isolation of two cDNA clones for phosphoinositide-specific phospholipase C from epidermal peels (Accession No. Y11931) of Nicotiana rustica. .  Physiologia Plantarum. 114 748
    PubMedGoogle Scholar
  • 40 Pingret,  J. L.,, Journet,  E. P.,, and Barker,  D. G.. (1998);  Rhizobium nod factor signaling. Evidence for a g protein-mediated transduction mechanism.  Plant Cell. 10 659-672
    CrossrefPubMedGoogle Scholar
  • 41 Powis,  G.,, Lowry,  S.,, Forrai,  L.,, Secrist,  P.,, and Abraham,  R.. (1991);  Inhibition of phosphoinositide phospholipase C by compounds U-73122 and D-609.  Journal of Cellular Pharmacology. 2 257-262
    PubMedGoogle Scholar
  • 42 Sanchez,  J.-P., and Nam-Hai Chua,  N.-H.. (2001);  Arabidopsis PLC1 is required for secondary responses to abscisic acid signals.  Plant Cell. 13 1143-1154
    CrossrefPubMedGoogle Scholar
  • 43 Shi,  J.,, Gonzales,  R. A.,, and Bhattacharyya,  M. K.. (1995);  Characterization of a plasma membrane-associated phosphoinositide-specific phospholipase C from soybean.  Plant Journal. 8 381-390
    CrossrefPubMedGoogle Scholar
  • 44 Shigaki,  T., and Bhattacharyya,  M. K.. (1999);  Color coding the cell death status of plant suspension cells.  BioTechniques. 26 1060-1062
    PubMedGoogle Scholar
  • 45 Shigaki,  T., and Bhattacharyya,  M. K.. (2000);  Decreased inositol 1,4,5-trisphosphate content in pathogen-challenged soybean cells.  Molecular Plant-Microbe Interactions. 13 563-567
    PubMedGoogle Scholar
  • 46 Singer,  W. D.,, Brown,  H. A.,, and Sternweis,  P. C.. (1997);  Regulation of eukaryotic phosphatidylinositol-specific phospholipase C and phospholipase D.  Annual Review of Biochemistry. 66 475-509
    CrossrefPubMedGoogle Scholar
  • 47 Smith,  M. R.,, Court,  D. W.,, Kim,  H. K.,, Park,  J. B.,, Rhee,  S. G.,, Rhim,  J. S.,, and Kung,  H. F.. (1998);  Overexpression of phosphoinositide-specific phospholipase Cγ in NIH 3T3 cells promotes transformation and tumorigenicity.  Carcinogenesis. 19 177-185
    CrossrefPubMedGoogle Scholar
  • 48 Smith,  M. R.,, Liu,  Y.-L.,, Kim,  H.,, Rhee,  S. G.,, and Kung,  H.-F.. (1990 a);  Inhibition of serum- and ras-stimulated DNA synthesis by antibodies to phospholipase C.  Science. 247 1074-1077
    PubMedGoogle Scholar
  • 49 Smith,  M. R.,, Ryu,  S.-H.,, Suh,  P.-G.,, Rhee,  S.-G.,, and Kung,  H.-F.. (1989);  S-phase induction and transformation of quiescent NIH 3T3 cells by microinjection of phospholipase C.  Proceedings of the National Academy of Sciences of the United States of America. 86 3659-3663
    PubMedGoogle Scholar
  • 50 Smith,  R. J.,, Sam,  L. M.,, Justen,  J. M.,, Bundy,  G. L.,, Bala,  G. A.,, and Bleasdale,  J. E.. (1990 b);  Receptor-coupled signal transduction in human polymorphonuclear neutrophils: effects of a novel inhibitor of phospholipase C-dependent processes on cell responsiveness.  Journal of Pharmacology and Experimental Therapeutics. 253 688-697
    PubMedGoogle Scholar
  • 51 Srivastava,  A.,, Pines,  M.,, and Jacoby,  B.. (1989);  Enhanced potassium uptake and phosphatidylinositol-phosphate turnover by hypertonic mannitol shock.  Physiologia Plantarum. 77 320-325
    PubMedGoogle Scholar
  • 52 Staxén,  I.,, Pical,  C.,, Montgomery,  L. T.,, Gray,  J. E.,, Hetherington,  A. M.,, and McAinsh,  M. R.. (1999);  Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C.  Proceedings of the National Academy of Sciences of the United States of America. 96 1779-1784
    CrossrefPubMedGoogle Scholar
  • 53 Van Dijken,  P.,, De Haas,  J. R.,, Craxton,  A.,, Erneux,  C.,, Shears,  S. B.,, and Van Haastert,  P. J. M.. (1995);  A novel, phospholipase C-independent pathway of inositol 1,4,5-trisphosphate formation in Dictyostelium and rat liver.  Journal of Biological Chemistry. 270 29724-29731
    CrossrefPubMedGoogle Scholar
  • 54 Walton,  T. J.,, Cooke,  C. J.,, Newton,  R. P.,, and Smith,  C. J.. (1993);  Evidence that generation of inositol 1,4,5-trisphosphate and hydrolysis of phosphatidylinositol 4,5-bisphosphate are rapid responses following addition of fungal elicitor which induces phytoalexin synthesis in Lucerne (Medicago sativa) suspension culture cells.  Cellular Signalling. 5 345-356
    CrossrefPubMedGoogle Scholar
  • 55 Yamamoto,  Y. T.,, Conkling,  M. A.,, Sussex,  I. M.,, and Irish,  V. F.. (1995);  An Arabidopsis cDNA related to animal phosphoinositide-specific phospholipase C genes.  Plant Physiology. 107 1029-1030
    CrossrefPubMedGoogle Scholar
  • 56 Yang,  H.,, Shen,  F.,, Herenyiova,  M.,, and Weber,  G.. (1998);  Phospholipase C (EC 3.1.4.11): a malignancy linked signal transduction enzyme.  Anticancer Research. 18 1399-1404
    PubMedGoogle Scholar
  • 57 Yoko-o,  T.,, Matsu,  Y.,, Yagisawa,  H.,, Nojima,  H.,, Uno,  I.,, and Toh-e,  A.. (1993);  The putative phosphoinositide-specific phospholipase C gene, PLC1, of the yeast Saccharomyces cerevisiae is important for cell growth.  Proceedings of the National Academy of Sciences of the United States of America. 90 1804-1808
    PubMedGoogle Scholar

M. K. Bhattacharyya

G303 Agronomy Hall
Iowa State University

Ames
Iowa 50011-1010
USA

Email: mbhattac@iastate.edu

Section Editor: A. Läuchli

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