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Address correspondence to Troy Stevens, Department of Pharmacology, MSB 3360, University of South Alabama College of Medicine, Mobile, AL 36688. Tel.: (334) 460-6010. Fax: (334) 460-6798. E-mail:tstevens{at}jaguar1.usouthal.edu
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Abstract |
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Key Words: store-operated Ca2+ entry; capacitative Ca2+ entry; ICRAC; protein 4.1; F-actin
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Introduction |
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The role of F-actin in regulation of store-operated Ca2+ entry is controversial, however, and may be cell typespecific (Rosado and Sage, 2000a). F-actin appears to play a central role in mechanically sensitive cells, namely platelets (Rosado et al., 2000) and endothelial cells (Holda and Blatter, 1997; Norwood et al., 2000), but not in NIH 3T3 cells (Ribeiro et al., 1997) or DDT1MF-2 and A7r5 muscle cell lines (Patterson et al., 1999). Though speculative, Rosado and Sage (2000a) suggested recently that the cell-specific distribution of F-actin, or alternatively its dynamic regulation, may account for these disparate findings. F-actin appears in a cortical membrane rim in platelets and endothelial cells. Particularly in endothelial cells, activation of store-operated Ca2+ entry is tightly coupled to reorganization of the F-actin membrane skeleton into stress fibers (Moore et al., 1998). Disruption of F-actin prevents activation of store-operated Ca2+ entry currents and stabilization of F-actin has similar effects (Norwood et al., 2000; Rosado et al., 2000), suggesting that in platelets and endothelial cells the dynamic activity of F-actin is required to link Ca2+ store depletion to Ca2+ entry. In contrast, F-actin is distributed throughout the cytosol of NIH 3T3 and smooth muscle cells and does not similarly reorganize in response to activation of store-operated Ca2+ entry (Ribeiro et al., 1997; Patterson et al., 1999).
It is unclear how the F-actin membrane skeleton regulates store-operated Ca2+ entry channel function. Spectrin is a principal component of the membrane skeleton that crosslinks F-actin and provides structural support for the plasmalemma and intracellular organelles (Bennett and Gilligan, 1993; Hartwig, 1994, 1995; Goodman, 1999), including the endoplasmic reticulum (Devarajan et al., 1997). In its simplest form spectrin is a large heterodimer comprised of and ß subunits oriented in an antiparallel fashion. Spectrin interacts with integral membrane proteins both directly and through its binding to ankyrin and protein 4.1 (Hartwig, 1994, 1995). The spectrinprotein 4.1 locus is functionally significant because it resides within the NH2 terminus of ß spectrin (residues A207V445), 21 amino acids downstream of the actin binding domain (residues A47K186) (Ma et al., 1993; Zimmer et al., 2000). Although ß spectrin normally binds and crosslinks F-actin with a KD = 2 x 10-4 M, its affinity for F-actin increases eight orders of magnitude in the presence of protein 4.1 (KD = 10-12 M) (Goodman et al., 1988). Thus, protein 4.1 tethers spectrin to the membrane and controls F-actin crosslinking, providing a cytoskeletal connection between the endoplasmic reticulum and the plasmalemma. Prior studies have established that the spectrin-based membrane skeleton localizes ion channels to discrete cellular microdomains. In premyelinated axons spectrin localizes voltage-gated Na+ channels to nodes of Ranvier (Srinivasan et al., 1988; Bennett and Lambert, 1999), and in MDCK cells it localizes the Na+/K+ ATPase to the basal-lateral plasma membrane with E-cadherin (Piepenhagen and Nelson, 1998). Therefore, we sought to explore whether coupling between store depletion and Ca2+ entry was dependent on the spectrin-based membrane skeleton.
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Results |
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Discussion |
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Two general approaches have been used previously to illustrate the role of F-actin in regulation of store-operated Ca2+ entry (Rosado and Sage, 2000a). First, dissolution of F-actin using cytochalasin D immediately accentuates store-operated Ca2+ entry or directly activates a cationic conductance, and over time reduces store-operated Ca2+ entry or prevents ISOC (Holda and Blatter, 1997; Norwood et al., 2000; Rosado et al., 2000; Rosado and Sage, 2000a). Second, stabilization of F-actin using jasplakinolide prevents activation of store-operated Ca2+ entry and ISOC (Holda and Blatter, 1997; Norwood et al., 2000; Rosado et al., 2000; Rosado and Sage, 2000a). These apparently disparate findings are rectified by the idea that dynamic activity of the F-actin cytoskeleton is required for channel function, consistent with physical-coupling models. This requisite for dynamic activity of F-actin supports the possibility that channel activation involves an actomyosin-based molecular motor (Gregory et al., 1999; Norwood et al., 2000), a mechanism of channel regulation also consistent with physical-coupling models.
Several features of these models implicate a role for spectrin in regulation of Ca2+ entry, particularly the ß spectrin locus residing across the actin and protein 4.1 binding domains. Spectrin crosslinks F-actin, contributes to formation of the cortical actin rim, and regulates Mg2+myosin ATPase activity (Wang et al., 1987). Spectrin also localizes both voltage-gated Na+ channels (Srinivasan et al., 1988; Bennett and Lambert, 1999) and the Na+/K+ ATPase (Piepenhagen and Nelson, 1998) to discrete microdomains in other cell types. Thus, we initially examined whether the spectrinactin association is required for Ca2+ store depletion to promote Ca2+ entry, thinking that specific disruption of this association might mimic the effects of other experimental strategies to disrupt F-actin. However, the results did not support the idea that F-actin regulates store-operated Ca2+ entry channels, particularly ISOC, through its direct interaction with spectrin, because disruption of this interaction did not prevent thapsigargin from activating ISOC.
The spectrinactin interaction is stabilized in a ternary complex by protein 4.1, which also tethers the spectrin membrane skeleton to transmembrane proteins. Consequently, reorganization of the membrane skeleton could alter protein 4.1's interaction with transmembrane proteins dependent or independent of the spectrinactin association. Though prior studies have not specifically demonstrated that protein 4.1 binds directly to cation channels, our data indicate store-operated Ca2+ entry is regulated by a spectrin- and protein 4.1dependent interaction. Disruption of the spectrinprotein 4.1 interaction using antibodies targeting either the NH2 or COOH region of ß spectrin's 4.1 binding domain reduced store-operated Ca2+ entry by 50%. Most importantly, disruption of the spectrinprotein 4.1 interaction abolished ISOC and had no effect on cyclic nucleotidegated cation channel activity, indicating a specific subset of thapsigargin-stimulated channels are selectively regulated through this component of the cytoskeleton.
In summary, our studies have addressed the role of the spectrin membrane skeleton in regulation of store-operated Ca2+ entry. Our findings support the idea that a highly localized region of ß spectrin (residues A207V445), through its interaction with protein 4.1, contributes to the linkage between Ca2+ store depletion and ISOC consistent with physical coupling models. The physiological significance of these findings remain speculative. However, these data suggest the possibility that a restricted locus on ß spectrin (e.g., protein 4.1 binding domain on ß-spectrin; Fig. 3 A) functionally links calcium store depletion with calcium entry through specific ISOC channels. Molecular identity of endogenous ISOC channels will be required to ultimately define the proteinprotein interactions responsible for regulation of calcium entry through this pathway.
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Materials and methods |
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Molecular biology
Standard techniques for RT-PCR subcloning were followed. All chemical reagents used were molecular biology grade. In brief, total RNA was extracted with RNA Stat-60 (Tel-Test "B") from cells grown to 100% confluence (107 cells) in 75-cm2 tissue culture flasks. First strand synthesis was performed with reverse transcriptase and oligo(dT) primer (Life Technologies) on
1 µg of DNaseI-treated total RNA. PCR was then performed with the following sets of primers:
-spectrin, 5'-CCT GAA TGG CTG GTT CGT GTG -3' (sense) and 5'-ATG GCA ACC TCC CGA AGA G-3' (antisense); ß-spectrin, 5'-CAT CCA GAA GCG TGA GAA TG-3' (sense) and 5'-CTT GAG AAC TGA TGG ACC TC-3' (antisense). PCR products were ligated into TA cloning vector pCR2.1 (Invitrogen) and transformed into chemically competent Escherichia coli. Positive clones (verified by PCR analysis) were selected and grown in Lauria-Bertani broth with kanamycin (50 µg/ml) for 1820 h at 37°C. Plasmids were isolated by the QIAprep® spinprep system (QIAGEN) and submitted to the Biopolymer Laboratory at the University of South Alabama for automated fluorescence sequence analysis (AB373XL DNA stretch sequencer). Sequencing of both strands using double-stranded plasmids as templates and universal primers confirmed the product accuracy. Nucleotide and amino acid alignments were achieved with BLAST (NCBI) and DNASIS v2.0 (Hitachi Software) programs.
Western blots
Cells were rinsed and then scraped into ice-cold detergent extraction buffer (40 µl per 60-mm dish; detergent extraction buffer, 10 mM Tris-HCl, pH 7.2, 150 mM NaCl, 10 mM MgCl2, 2 mM EDTA, 0.25 mM DTT, 1 mM PMSF, 1% [vol/vol] Triton-X, 4 mM DFP, 100 µg/ml antipain, 100 µg/ml leupeptin, 100 µg/ml E-64 [L-trans-3-Carboxyoxiran-2-carbonyl-L-leucylagmatine], 0.4 mM benzamidine, and 10 mM iodoacetamide) (all chemicals from Sigma-Aldrich). The mixtures were cleared by centrifugation and subjected to SDS-PAGE for analysis.
Electrophoresis of and ß spectrins was through standard 5% SDS-PAGE gels at 100 V for 1.5 h. Proteins were transferred to nitrocellulose membrane in buffer containing 150 mM glycine, 20 mM Tris-base, and 20% (vol/vol) methanol. Transfer of proteins was performed overnight at 30 V, at 4°C. Blots were stained with Ponceau S to visualize marker proteins, destained with TBS (50 mM Tris-HCl, 120 mM NaCl), and blocked with TBS plus 0.05% Tween-20 and 5% nonfat dry milk for 1 h. Spectrin antibodies (provided by Dr. Steven R. Goodman) were diluted 1:1,000 in blocking buffer. Incubations were at 4°C overnight with constant, gentle agitation. Blots were washed with TBSTween-20 (0.1%) three times for 30 min each. HRP-conjugated antirabbit IgG (1:20,000) was added to the blots in blocking buffer (room temperature) for 1 h then washed off as described above. Detection of secondary antibody was achieved using the SuperSignal® West Pico Chemiluminescent System (Pierce Chemical Co.).
Isolation of lung spectrin, human erythrocyte 4.1, and binding analysis
Rat lung spectrin (-SpII
1/ß-SpII
1) was isolated by low ionic strength extraction (37o C) of crude membranes as described previously for brain spectrin (Sikorski et al., 1991). Modifications from our previously published procedure included a reduction in buffer volumes and size of the Sephacryl S-500 column (1.8 x 20 cm) because we started the isolation with only 10 g of frozen rat lungs and we eliminated steps that demyelinate brain homogenates. The final yield of lung spectrin was 100 µg from 10 g of tissue. Erythrocyte protein 4.1 was isolated by the method of Tyler et al. (1979). Rabbit muscle actin was purchased from Sigma-Aldrich and then further purified on a Sephacryl S-100 column to remove contaminants from the commercial preparation.
We tested the ability of ß-SpII1 peptidespecific antibodies SG43 (residues 824, adjacent to the actin binding domain), SG921 (residues 206221 at a synapsin attachment site), and SG48 (residues 417428 within the protein 4.1synapsin binding domain) (Ma et al., 1993; Sikorski et al., 2000; Zimmer et al., 2000) to block the spectrinprotein 4.1 or spectrinactin interaction. To test the effect of the peptide-specific antibodies on the spectrinprotein 4.1 interaction, we loaded 1 µg/lane of pure lung spectrin on a 7% polyacrylamide mini gel and performed SDS-PAGE followed by transfer to nitrocellulose paper. The nitrocellulose paper was then blocked with 5% dry milk in PBS plus 0.05% Tween, and then dried strips were incubated with PBS or antibodies SG43, SG48, and SG921 diluted to 1:100 in PBS. The strips were then incubated with 125I-protein 4.1 (10 ng/ml; 1,073,742 cpm/µg) and autoradiography was performed. After autoradiography, the antibodies were detected by immunoperoxidase staining and the spectrin bands were excised and counted in a Packard 500 gamma counter.
To observe the effect of the peptide-specific antibodies on the spectrinactin interaction, we conducted spectrinactin cosedimentation assays as described previously (Karinch et al., 1990). In brief, we preincubated 10 µg/ml lung spectrin (12,849 cpm/µg) with (1:10 dilution) peptide-specific antibodies SG43, SG48, SG921, or buffer for 30 min at 4°C. We then added an equal volume of actin (500 µg/ml) in polymerization buffer and incubated for 1 h at 4°C. The spectrinactin complexes were separated from free spectrin by sedimentation at 50,000 g for 30 min at 4°C. Supernatants and pellets were loaded on 7% polyacrylamide minigels and SDS-PAGE was performed followed by autoradiography.
Antibody microinjection
Rat PAECs were seeded onto 25-mm circle microscope glass coverslips or Cellocate coverslips (Eppendorf) and grown for 2448 h. Microinjection was performed as described in detail elsewhere (Norwood et al., 2000).
Cytosolic Ca2+ measurements
Rat PAECs were seeded onto 25-mm circle microscope glass coverslips (Fisher Scientific) and grown to confluence. Cytosolic Ca2+ [Ca2+]i was estimated with the Ca2+-sensitive fluorophore fura 2/acetoxymethylester (Molecular Probes) according to methods described previously (Norwood et al., 2000). Calculations of free [Ca2+]i are routinely made using modifications of the formula described by Grynkiewicz et al. (1985) (Stevens et al., 1994).
Patch clamp electrophysiology
Conventional whole-cell voltage clamp configuration was performed to measure transmembrane currents in single rat PAECs by the standard giga-seal patch clamp technique, as described by Moore et al. (1998). Confluent rat PAECs were enzyme dispersed, seeded onto 35-mm plastic culture dishes, and then allowed to reattach for at least 24 h before patch clamp experiments were performed. Patch clamp recordings were obtained from single (electrically isolated) rat PAECs exhibiting a flat, polyhedral morphology. These cells were chosen for study because their morphology was consistent with rat PAECs from a confluent monolayer. Recording pipettes were heat polished to produce a tip resistance in the range of 35 megaohms in the internal solution. To examine Ca2+ currents, the pipette solution contained (in mM) 130 N-methyl-D-glucamine, 10 Hepes, 1.15 EGTA, 1 Ca2+, 2 Mg2+-ATP, 1 N-phenylanthranilic acid, 0.1 5-Nitro-2(3-phenylprcpylamino benzoic acid) (pH 7.2, adjusted with methane sulfonic acid). The external (bath) solution contained (in mM) 120 aspartic acid, 5 Ca(OH)2, 5 CaCl2, 10 Hepes, 0.5 3,4-diaminopyridine (pH 7.4, adjusted with tetraethylammonium hydroxide). To examine nonselective currents the pipette solution contained (in mM) 140 KOH, 5 NaOH, 145 glutamic acid, 10 EGTA, 10 Hepes, 1 N-phenylanthranilic acid, pH 7.2. The external (bath) solution contained (in mM) 140 NaOH, 5 KOH, 145 glutamic acid, 15 Hepes, 1 N-phenylanthranilic acid, pH 7.4. All solutions were adjusted to 290300 mosM with sucrose. Currents were recorded with a computer-controlled EPC9 patch clamp amplifier (HEKA). Cell capacitance and series resistance were calculated with the software-supported internal routines of the EPC9 and compensated before each experiment. Voltage pulses were applied from 100 to +60 mV in 20 mV increments after the whole-cell configuration was achieved, with 200 ms duration during each voltage step and a 2 s interval between steps. The holding potential between each step was 0 mV. Data acquisition and analysis were performed with Pulse/PulseFit software (HEKA) and filtered at 2.9 kHz.
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Footnotes |
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Acknowledgments |
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This work was supported by HL56056 and HL60024 (to T. Stevens), NS35937 (to S.R. Goodman), and DK50151 (to M. Li). Dr. Songwei Wu is an American Heart Association, Southeastern Consortium Fellow.
Submitted: 29 June 2001
Accepted: 6 August 2001
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