Visualization of Phosphoinositides That Bind Pleckstrin Homology Domains: Calcium- and Agonist-induced Dynamic Changes and Relationship to Myo-[3H]inositol-labeled Phosphoinositide Pools

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© The Rockefeller University Press, 0021-9525/1998//501 $5.00
The Journal of Cell Biology, Volume 143, Number 2, , 1998 501-510

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Visualization of Phosphoinositides That Bind Pleckstrin Homology Domains: Calcium- and Agonist-induced Dynamic Changes and Relationship to Myo-[³H]inositol-labeled Phosphoinositide Pools

Péter Várnai and Tamás Balla

Endocrinology and Reproduction Research Branch, National Institutes of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892-4510

Phosphatidylinositol 4,5-bisphosphate (PtdIns[4,5]P₂) poolsthat bind pleckstrin homology (PH) domains were visualizedby cellular expression of a phospholipase C (PLC) ${delta}$ PH domain–greenfluorescent protein fusion construct and analysis of confocal images in living cells. Plasma membrane localization of thefluorescent probe required the presence of three basic residueswithin the PLC ${delta}$ PH domain known to form critical contacts withPtdIns(4,5)P₂. Activation of endogenous PLCs by ionophoresor by receptor stimulation produced rapid redistribution ofthe fluorescent signal from the membrane to cytosol, whichwas reversed after Ca²⁺ chelation. In both ionomycin- and agonist-stimulatedcells, fluorescent probe distribution closely correlated withchanges in absolute mass of PtdIns(4,5)P₂. Inhibition of PtdIns(4,5)P₂synthesis by quercetin or phenylarsine oxide prevented therelocalization of the fluorescent probe to the membranes after Ca²⁺ chelation in ionomycin-treated cells or during agoniststimulation. In contrast, the synthesis of the PtdIns(4,5)P₂imaged by the PH domain was not sensitive to concentrationsof wortmannin that had been found inhibitory of the synthesisof myo-[³H]inositol– labeled PtdIns(4,5)P₂. Identificationand dynamic imaging of phosphoinositides that interact withPH domains will further our understanding of the regulationof such proteins by inositol phospholipids.

Key Words: phosphoinositides • calcium • green fluorescent protein • pleckstrin-homology domain • phospholipase C

Abbreviations used in this paper: Ang II, angiotensin II; BAG, bovine adrenal glomerulosa; BAL, 2,3-dimercaptopropanol; BAPTA, 1,2-bis(2-aminophenoxy)ethane N,N,N',N-tetraacetic acid; GFP, green fluorescent protein; Ins(1,4,5)P₃, inositol-1,4,5-trisphosphate; PAO, phenylarsine oxide; PH, pleckstrin homology; PLC, phospholipase C; PtdIns, phosphatidylinositol; PtdIns(4)P, phosphatidylinositol 4-phosphate; PtdIns(4,5)P₂, phosphatidylinositol 4,5-bisphosphate; WT, wortmannin.

The skillful technical work of Ms. Y. Zhang is greatly appreciated.

Address all correspondence to T. Balla, National Institutesof Health, Bldg. 49, Rm. 6A35, 49 Convent Drive, Bethesda,MD 20892-4510. Tel.: (301) 496-2136. Fax: (301) 480-8010. E-mail:tambal{at}box-t.nih.gov

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Bittner, M. A., Holz, R. W. (2005). Phosphatidylinositol-4,5-bisphosphate: Actin Dynamics and the Regulation of ATP-Dependent and -Independent Secretion. Mol. Pharmacol. 67: 1089-1098 [Abstract] [Full Text]
Lopes, C. M. B, Rohacs, T., Czirjak, G., Balla, T., Enyedi, P., Logothetis, D. E (2005). PIP2 hydrolysis underlies agonist-induced inhibition and regulates voltage gating of two-pore domain K+ channels. J. Physiol. 564: 117-129 [Abstract] [Full Text]
Winks, J. S., Hughes, S., Filippov, A. K., Tatulian, L., Abogadie, F. C., Brown, D. A., Marsh, S. J. (2005). Relationship between Membrane Phosphatidylinositol-4,5-Bisphosphate and Receptor-Mediated Inhibition of Native Neuronal M Channels. J. Neurosci. 25: 3400-3413 [Abstract] [Full Text]
Sidhu, G., Li, W., Laryngakis, N., Bishai, E., Balla, T., Southwick, F. (2005). Phosphoinositide 3-Kinase Is Required for Intracellular Listeria monocytogenes Actin-based Motility and Filopod Formation. J. Biol. Chem. 280: 11379-11386 [Abstract] [Full Text]
Weixel, K. M., Blumental-Perry, A., Watkins, S. C., Aridor, M., Weisz, O. A. (2005). Distinct Golgi Populations of Phosphatidylinositol 4-Phosphate Regulated by Phosphatidylinositol 4-Kinases. J. Biol. Chem. 280: 10501-10508 [Abstract] [Full Text]
Milosevic, I., Sorensen, J. B., Lang, T., Krauss, M., Nagy, G., Haucke, V., Jahn, R., Neher, E. (2005). Plasmalemmal Phosphatidylinositol-4,5-Bisphosphate Level Regulates the Releasable Vesicle Pool Size in Chromaffin Cells. J. Neurosci. 25: 2557-2565 [Abstract] [Full Text]
Balla, A., Tuymetova, G., Tsiomenko, A., Varnai, P., Balla, T. (2005). A Plasma Membrane Pool of Phosphatidylinositol 4-Phosphate Is Generated by Phosphatidylinositol 4-Kinase Type-III Alpha: Studies with the PH Domains of the Oxysterol Binding Protein and FAPP1. Mol. Biol. Cell 16: 1282-1295 [Abstract] [Full Text]
Tateishi, Y., Hattori, M., Nakayama, T., Iwai, M., Bannai, H., Nakamura, T., Michikawa, T., Inoue, T., Mikoshiba, K. (2005). Cluster Formation of Inositol 1,4,5-Trisphosphate Receptor Requires Its Transition to Open State. J. Biol. Chem. 280: 6816-6822 [Abstract] [Full Text]
Liu, B., Qin, F. (2005). Functional Control of Cold- and Menthol-Sensitive TRPM8 Ion Channels by Phosphatidylinositol 4,5-Bisphosphate. J. Neurosci. 25: 1674-1681 [Abstract] [Full Text]
Wang, Y. J., Li, W. H., Wang, J., Xu, K., Dong, P., Luo, X., Yin, H. L. (2004). Critical role of PIP5KI{gamma}87 in InsP3-mediated Ca2+ signaling. JCB 167: 1005-1010 [Abstract] [Full Text]
Gamper, N., Reznikov, V., Yamada, Y., Yang, J., Shapiro, M. S. (2004). Phosphotidylinositol 4,5-Bisphosphate Signals Underlie Receptor-Specific Gq/11-Mediated Modulation of N-Type Ca2+ Channels. J. Neurosci. 24: 10980-10992 [Abstract] [Full Text]