Regulation of Cardiac Na+,Ca2+ Exchange and KATP Potassium Channels by PIP2
Abstract
Cardiac Na+,Ca2+ exchange is activated by a mechanism that requires hydrolysis of adenosine triphosphate (ATP) but is not mediated by protein kinases. In giant cardiac membrane patches, ATP acted to generate phosphatidylinositol-4,5-bisphosphate (PIP2) from phosphatidylinositol (PI). The action of ATP was abolished by a PI-specific phospholipase C (PLC) and recovered after addition of exogenous PI; it was reversed by a PIP2-specific PLC; and it was mimicked by exogenous PIP2. High concentrations of free Ca2+ (5 to 20 μM) accelerated reversal of the ATP effect, and PLC activity in myocyte membranes was activated with a similar Ca2+ dependence. Aluminum reversed the ATP effect by binding with high affinity to PIP2. ATP-inhibited potassium channels (KATP) were also sensitive to PIP2, whereas Na+,K+ pumps and Na+ channels were not. Thus, PIP2 may be an important regulator of both ion transporters and channels.
References
•
AGUILARBRYAN L, CLONING OF THE BETA-CELL HIGH-AFFINITY SULFONYLUREA RECEPTOR - A REGULATOR OF INSULIN-SECRETION, SCIENCE 268, 423 (1995).
•
BIRCHALL J.D., THE CHEMISTRY OF ALUMINUM AND SILICON IN RELATION TO ALZHEIMERS-DISEASE, CLINICAL CHEMISTRY 34, 265 (1988).
•
BUSER C.A., DOES THE BINDING OF CLUSTERS OF BASIC RESIDUES TO ACIDIC LIPIDS INDUCE DOMAIN FORMATION IN MEMBRANES, MOLECULAR MEMBRANE BIOLOGY 12, 69 (1995).
•
CHOQUETTE D, REGULATION OF PLASMA-MEMBRANE CA-2+ ATPASES BY LIPIDS OF THE PHOSPHATIDYLINOSITOL CYCLE, BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS 125, 908 (1984).
•
COLLINS A, J PHYSL 454, 37 (1992).
•
COLLINS A, A NOVEL METHOD FOR DIRECT APPLICATION OF PHOSPHOLIPIDS TO GIANT EXCISED MEMBRANE PATCHES IN THE STUDY OF SODIUM-CALCIUM EXCHANGE AND SODIUM-CHANNEL CURRENTS, PFLUGERS ARCHIV-EUROPEAN JOURNAL OF PHYSIOLOGY 423, 347 (1993).
•
CONDRESCU M, ATP-DEPENDENT REGULATION OF SODIUM-CALCIUM EXCHANGE IN CHINESE-HAMSTER OVARY CELLS TRANSFECTED WITH THE BOVINE CARDIAC SODIUM-CALCIUM EXCHANGER, JOURNAL OF BIOLOGICAL CHEMISTRY 270, 9137 (1995).
•
CONNOR J, TRANSBILAYER MOVEMENT OF PHOSPHATIDYLSERINE IN ERYTHROCYTES - INHIBITION OF TRANSPORT AND PREFERENTIAL LABELING OF A 31 000-DALTON PROTEIN BY SULFHYDRYL REACTIVE REAGENTS, BIOCHEMISTRY 27, 848 (1988).
•
FILOTEO A.G., THE LIPID-BINDING PEPTIDE FROM THE PLASMA-MEMBRANE CA2+ PUMP BINDS CALMODULIN, AND THE PRIMARY CALMODULIN-BINDING DOMAIN INTERACTS WITH LIPID, JOURNAL OF BIOLOGICAL CHEMISTRY 267, 11800 (1992).
•
FURUKAWA T, Functional linkage of the cardiac ATP sensitive K+ channel to the actin cytoskeleton, PFLUGERS ARCHIV-EUROPEAN JOURNAL OF PHYSIOLOGY 431, 504 (1996).
•
GILMORE A.P., Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-4-5-bisphosphate, NATURE 381, 531 (1996).
•
GILMORE A.P., NATURE 381, 5311 (1996).
•
GOTO K, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 50, 235 (1995).
•
HALL A, SMALL GTP-BINDING PROTEINS AND THE REGULATION OF THE ACTIN CYTOSKELETON, ANNUAL REVIEW OF CELL BIOLOGY 10, 31 (1994).
•
HARTWIG J.H., THROMBIN RECEPTOR LIGATION AND ACTIVATED RAC UNCAP ACTIN FILAMENT BARBED ENDS THROUGH PHOSPHOINOSITIDE SYNTHESIS IN PERMEABILIZED HUMAN PLATELETS, CELL 82, 643 (1995).
•
HILGEMANN D.W., STEADY-STATE AND DYNAMIC PROPERTIES OF CARDIAC SODIUM-CALCIUM EXCHANGE - SECONDARY MODULATION BY CYTOPLASMIC CALCIUM AND ATP, JOURNAL OF GENERAL PHYSIOLOGY 100, 933 (1992).
•
HILGEMANN D.W., MECHANISM OF CARDIAC NA+-CA2+ EXCHANGE CURRENT STIMULATION BY MGATP - POSSIBLE INVOLVEMENT OF AMINOPHOSPHOLIPID TRANSLOCASE, JOURNAL OF PHYSIOLOGY-LONDON 454, 59 (1992).
•
HILGEMANN D.W., REGULATION AND DEREGULATION OF CARDIAC NA+-CA2+ EXCHANGE IN GIANT EXCISED SARCOLEMMAL MEMBRANE PATCHES, NATURE 344, 242 (1990).
•
HILGEMANN D.W., SINGLE CHANNEL RECOR: 307 (1995).
•
HILGEMANN D.W., unpublished data.
•
IKEZAWA H, STUDIES ON PHOSPHATIDYLINOSITOL PHOSPHODIESTERASE (PHOSPHOLIPASE-C TYPE) OF BACILLUS-CEREUS .1. PURIFICATION, PROPERTIES AND PHOSPHATASE-RELEASING ACTIVITY, BIOCHIMICA ET BIOPHYSICA ACTA 450, 154 (1976).
•
IKEZAWA H, METHODS ENZYMOLOGY C 71, 731 (1981).
•
INAGAKI N, RECONSTITUTION OF I-KATP - AN INWARD RECTIFIER SUBUNIT PLUS THE SULFONYLUREA RECEPTOR, SCIENCE 270, 1166 (1995).
•
ITO H, ON THE MECHANISM OF G-PROTEIN-BETA-GAMMA SUBUNIT ACTIVATION OF THE MUSCARINIC K+-CHANNEL IN GUINEA-PIG ATRIAL CELL-MEMBRANE - COMPARISON WITH THE ATP-SENSITIVE K+-CHANNEL, JOURNAL OF GENERAL PHYSIOLOGY 99, 961 (1992).
•
JANMEY P.A., PHOSPHOINOSITIDES AND CALCIUM AS REGULATORS OF CELLULAR ACTIN ASSEMBLY AND DISASSEMBLY, ANNUAL REVIEW OF PHYSIOLOGY 56, 169 (1994).
•
JOHNSON B.D., A CYTOSKELETAL MECHANISM FOR CA2+ CHANNEL METABOLIC DEPENDENCE AND INACTIVATION BY INTRACELLULAR CA2+, NEURON 10, 797 (1993).
•
KANOH H, DIACYLGLYCEROL KINASE AND PHOSPHATIDIC-ACID PHOSPHATASE - ENZYMES METABOLIZING LIPID 2ND MESSENGERS, CELLULAR SIGNALLING 5, 495 (1993).
•
LEE S.B., SIGNIFICANCE OF PIP2 HYDROLYSIS AND REGULATION OF PHOSPHOLIPASE-C ISOZYMES, CURRENT OPINION IN CELL BIOLOGY 7, 183 (1995).
•
LEVITSKY D.O., IDENTIFICATION OF THE HIGH-AFFINITY CA2+-BINDING DOMAIN OF THE CARDIAC NA+-CA2+ EXCHANGER, JOURNAL OF BIOLOGICAL CHEMISTRY 269, 22847 (1994).
•
LI Z.P., THE CARDIAC NA+-CA2+ EXCHANGER BINDS TO THE CYTOSKELETAL PROTEIN ANKYRIN, JOURNAL OF BIOLOGICAL CHEMISTRY 268, 11489 (1993).
•
LISCOVITCH M, NOVEL FUNCTION OF PHOSPHATIDYLINOSITOL 4,5-BISPHOSPHATE AS A COFACTOR FOR BRAIN MEMBRANE PHOSPHOLIPASE-D, JOURNAL OF BIOLOGICAL CHEMISTRY 269, 21403 (1994).
•
LUCIANI S, ANN NY ACAD SCI 639, 156 (1993).
•
MARTELL A.E., CRITICAL STABILITY C 3, (1977).
•
MARTIN R.B., TERNARY HYDROXIDE COMPLEXES IN NEUTRAL SOLUTIONS OF AL-3+ AND F-, BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS 155, 1194 (1988).
•
MATSUOKA S, REGULATION OF THE CARDIAC NA+-CA2+ EXCHANGER BY CA2+ - MUTATIONAL ANALYSIS OF THE CA2+-BINDING DOMAIN, JOURNAL OF GENERAL PHYSIOLOGY 105, 403 (1995).
•
MATSUOKA S, INITIAL LOCALIZATION OF REGULATORY REGIONS OF THE CARDIAC SARCOLEMMAL NA+-CA2+ EXCHANGER, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 90, 3870 (1993).
•
MCDONALD L.J., PHOSPHOINOSITIDE HYDROLYSIS BY PHOSPHOLIPASE-C MODULATED BY MULTIVALENT CATIONS LA3+, AL3+, NEOMYCIN, POLYAMINES, AND MELITTIN, JOURNAL OF LIPID MEDIATORS AND CELL SIGNALLING 11, 81 (1995).
•
NICHOLS C.G., ADENOSINE TRIPHOSPHATE-SENSITIVE POTASSIUM CHANNELS IN THE CARDIOVASCULAR-SYSTEM, AMERICAN JOURNAL OF PHYSIOLOGY 261, H1675 (1991).
•
OHNOSHOSAKU T, DUAL EFFECTS OF ATP ON K+ CURRENTS OF MOUSE PANCREATIC BETA-CELLS, PFLUGERS ARCHIV-EUROPEAN JOURNAL OF PHYSIOLOGY 408, 133 (1987).
•
REDMAN C, INHIBITION OF DIACYLGLYCEROL KINASE BY THE ANTITUMOR AGENT CALPHOSTIN-C - EVIDENCE FOR SIMILARITY BETWEEN THE ACTIVE-SITE OF DIACYLGLYCEROL KINASE AND THE REGULATORY SITE OF PROTEIN-KINASE-C, BIOCHEMICAL PHARMACOLOGY 50, 235 (1995).
•
REITER M, CALCIUM MOBILIZATION AND CARDIAC INOTROPIC MECHANISMS, PHARMACOLOGICAL REVIEWS 40, 189 (1988).
•
RIBALET B, ATP MEDIATES BOTH ACTIVATION AND INHIBITION OF K(ATP) CHANNEL ACTIVITY VIA CAMP-DEPENDENT PROTEIN-KINASE IN INSULIN-SECRETING CELL-LINES, JOURNAL OF GENERAL PHYSIOLOGY 94, 693 (1989).
•
RIBALET B, CHARACTERIZATION OF THE G-PROTEIN COUPLING OF A GLUCAGON RECEPTOR TO THE K-ATP CHANNEL IN INSULIN-SECRETING CELLS, JOURNAL OF MEMBRANE BIOLOGY 142, 395 (1994).
•
SCHOFL C, ALUMINUM PERTURBS OSCILLATORY PHOSPHOINOSITIDE-MEDIATED CALCIUM SIGNALING IN HORMONE-STIMULATED HEPATOCYTES, BIOCHEMICAL JOURNAL 269, 547 (1990).
•
SEIGNEURET M, ATP-DEPENDENT ASYMMETRIC DISTRIBUTION OF SPIN-LABELED PHOSPHOLIPIDS IN THE ERYTHROCYTE-MEMBRANE - RELATION TO SHAPE CHANGES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 81, 3751 (1984).
•
SHANNON T.R., INTERACTION OF CARDIAC NA-CA EXCHANGER AND EXCHANGE INHIBITORY PEPTIDE WITH MEMBRANE PHOSPHOLIPIDS, AMERICAN JOURNAL OF PHYSIOLOGY 266, C1350 (1994).
•
SMRCKA A.V., REGULATION OF PURIFIED SUBTYPES OF PHOSPHATIDYLINOSITOL-SPECIFIC PHOSPHOLIPASE-C BETA BY G-PROTEIN ALPHA-SUBUNIT AND BETA-GAMMA-SUBUNITS, JOURNAL OF BIOLOGICAL CHEMISTRY 268, 9667 (1993).
•
STEPHENS L.R., AGONIST-STIMULATED SYNTHESIS OF PHOSPHATIDYLINOSITOL(3,4,5)-TRISPHOSPHATE - A NEW INTRACELLULAR SIGNALING SYSTEM, BIOCHIMICA ET BIOPHYSICA ACTA 1179, 27 (1993).
•
TAKANO M, ATP-DEPENDENT DECAY AND RECOVERY OF K+ CHANNELS IN GUINEA-PIG CARDIAC MYOCYTES, AMERICAN JOURNAL OF PHYSIOLOGY 258, H45 (1990).
•
TANG X.J., A subfamily of P-type ATPases with aminophospholipid transporting activity, SCIENCE 272, 1495 (1996).
•
TSIEN R.W., ADV CYCLIC NUCLEOTID 8, 363 (1977).
•
VEMURI R, PHOSPHOLIPID-COMPOSITION MODULATES THE NA+-CA-2+ EXCHANGE ACTIVITY OF CARDIAC SARCOLEMMA IN RECONSTITUTED VESICLES, BIOCHIMICA ET BIOPHYSICA ACTA 937, 258 (1988).
•
VOLWERK J.J., PHOSPHATIDYLINOSITOL-SPECIFIC PHOSPHOLIPASE-C FROM BACILLUS-CEREUS COMBINES INTRINSIC PHOSPHOTRANSFERASE AND CYCLIC PHOSPHODIESTERASE ACTIVITIES - A P-31 NMR-STUDY, BIOCHEMISTRY 29, 8056 (1990).
•
WEBER G, BIOCHIM BIOPHYS ACTA 694, 1 (1982).
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Volume 273 | Issue 5277
16 August 1996
16 August 1996
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© 1996 American Association for the Advancement of Science.
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