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; M. K. Bhattacharyya

doi:10.1055/s-2002-20436

Plant Biology, Table of Contents

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

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

Full Text

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
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
03 Berridge, M. J.. (1993); Inositol trisphosphate and calcium signalling. Nature. 361 315-325
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
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
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
07 Coté, G. G., and Crain, R. C.. (1993); Biochemistry of phosphoinositides. Annual Review of Plant Physiology and Plant Molecular Biology. 44 333-356
08 Dennis, E. A.. (1983) Phospholipases. The Enzymes, Vol. 16. Boyer, P. D., ed. New York, NY; Academic Press pp. 307-353
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
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
11 Ettlinger, C., and Lehle, L.. (1988); Auxin induces rapid changes in phosphatidylinositol metabolites. Nature. 331 176-178
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
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
14 Gietzen, K.. (1983); Comparison of the calmodulin antagonists compound 48/80 and calmidazolium. Biochemical Journal. 216 611-616
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
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
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
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
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
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
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
22 Joseph, S. K.,, Esch, T.,, and Bonner, W. D.. (1989); Hydrolysis of inositol phosphates by plant cell extracts. Biochemical Journal. 264 851-856
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
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
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
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
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
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
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
30 Majerus, P.. (1992); Inositol phosphate biochemistry. Annual Review of Biochemistry. 61 225-250
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
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
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
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
35 Munnik, T.,, Irvine, R. F.,, and Musgrave, A.. (1998); Phospholipid signalling in plants. Biochimica et Biophysica Acta. 1389 222-272
36 Murashige, T., and Skoog, F.. (1962); A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum. 15 473-497
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
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
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
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
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
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
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
44 Shigaki, T., and Bhattacharyya, M. K.. (1999); Color coding the cell death status of plant suspension cells. BioTechniques. 26 1060-1062
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
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
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
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
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
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
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
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
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
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
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
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
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

M. K. Bhattacharyya

G303 Agronomy Hall
Iowa State University

Ames
Iowa 50011-1010
USA

Email: mbhattac@iastate.edu

Section Editor: A. Läuchli