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Annexin II Is Present on Renal Epithelial Cells and Binds Calcium Oxalate Monohydrate Crystals

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Annexin II Is Present on Renal Epithelial Cells and Binds Calcium Oxalate Monohydrate Crystals J Am Soc Nephrol 14: 289–297, 2003 Annexin II Is Present on Renal Epithelial Cells and Binds Calcium Oxalate Monohydrate Crystals VIVEK KUMAR,* GERARD FARELL,* SERGIO DEGANELLO,† and JOHN C. LIESKE* *Division of Nephrology, Department of Internal Medicine, Mayo Clinic and Foundation, Rochester, Minnesota; and †Department C.F.T.A., University of Palermo, Palermo, Italy. Abstract. Attachment of newly formed crystals to renal epithe- suggesting that at least a portion of cellular Ax-II is an intrinsic lial cells appears to be a critical step in the development of membrane-bound protein. Using confocal immunofluores- kidney stones. The current study was undertaken to identify cence microscopy, Ax-II was visualized together with Caveo- potential calcium oxalate monohydrate (COM) crystal-binding lin-1 (Cav-1) on the apical membrane of intact MDCKI cells. proteins on the surface of renal tubular cells. Apical mem- Cells pretreated with a monoclonal anti-Ax-II antibody bound branes were prepared from confluent monolayers of renal significantly fewer COM crystals, whereas anti-LDL receptor epithelial cells (MDCKI line), and COM crystal affinity was antibody did not decrease COM binding, further suggesting a used to isolate crystal-binding proteins that were then subjected functional role for Ax-II during adhesion of crystals to intact to electrophoresis and electroblotting. Microsequencing of the cells. These results suggest that Ax-II avidly binds COM most prominent COM crystal-binding protein (Mr of 37 kD) crystals and is present on the apical surface of MDCKI cells. identified it as annexin II (Ax-II). When exposed proteins on Therefore, in the intact nephron, Ax-II could mediate adhesion the surface of intact monolayers were biotinylated and then of COM crystals to cells, and altered exposure of Ax-II on the isolated using streptavidin agarose beads, Ax-II was detected, surface of renal tubular cells could promote crystal retention suggesting that at least a portion is exposed on the apical cell and possibly kidney stone formation. surface. Ax-II was not completely extracted by 0.1 M Na2CO3, Nephrolithiasis is common, affecting up to 10% of the popu- gested that anionic glycoproteins could mediate COM crystal lation at some point during their life (1,2). Although many adhesion to cultured tubular cells (9). More recently, renal cell patients have metabolic abnormalities, such as over-excretion surface nucleolin-related protein (NRP) (18) and hyaluronan of calcium in the urine, that seem to explain their tendency (17) have been identified as potential crystal-binding mole- toward kidney stone formation, many do not (3). In addition, it cules. Hyaluronan appears to be present on the surface of appears mathematically unlikely that nucleation and growth of cultured cells that are proliferating in response to injury (17), an individual crystal could produce a particle large enough to and anionic phospholipids may also mediate COM crystal occlude a nephron lumen (4). Therefore, our laboratory (5–11) adhesion to injured and possibly apoptotic cells (19,20). and others (12–17) have investigated the mechanism(s) Evidence to date suggests that more than one apical mem- whereby urinary crystals can interact with renal epithelial cells; brane molecule could mediate adhesion and internalization of once adherent to a cell, smaller particles could be retained and crystals; the current study was therefore undertaken to identify serve as a nidus for renal stone formation. additional potential candidates, because cell surface crystal- Indeed, studies using diverse cultured renal epithelial cells binding molecules could be a critical factor that mediates the demonstrate that calcium oxalate monohydrate (COM) crys- earliest events in kidney stone formation. tals, the most common crystal in human stones, rapidly adhere to molecules on the apical cell surface (8,9,12,13,16). Internal- Materials and Methods ization (5,7) and potential dissolution within lysosomal bodies Monoclonal antibodies against annexin II (Ax-II) were obtained (10) follow adhesion of COM crystals. Earlier evidence sug- from BD Transduction Labs (Franklin Lakes, NJ), against nucleolin from MBL Co. Ltd., Japan, and against LDL receptor from Oncogene Research Products, La Jolla, CA, and a polyclonal antibody against caveolin-1 was obtained from Santa Cruz Biotechnology, CA. All Received July 11, 2002. Accepted October 21, 2002. Correspondence to Dr. John C. Lieske, Division of Nephrology, Department of other reagents were obtained from Sigma Chemical Co., St. Louis, Internal Medicine, Mayo Clinic and Foundation, 200 1st St SW, Rochester, MO, unless otherwise indicated. MN 55905. Phone: 507-284-2064; Fax: 507-266-9315; E-mail: [email protected] Cell Culture 1046-6673/1402-0289 Renal epithelial cells of the Madin-Darby Canine Kidney (MDCK) Journal of the American Society of Nephrology line, type I, were a gift from Carl Verkoelen (Erasmus University, Copyright © 2003 by the American Society of Nephrology Rotterdam, The Netherlands). Cells were grown in Dulbecco-Vogt DOI: 10.1097/01.ASN.0000046030.24938.0A modified Eagle’s medium (DMEM) containing 25 mM glucose at 290 Journal of the American Society of Nephrology J Am Soc Nephrol 14: 289–297, 2003 38°CinaCO2 incubator as described previously (5). To prepare 100 V constant current using a Mini-Protean II apparatus (Bio-Rad, high-density, quiescent cultures, 1 ϫ 106 cells/35-mm plastic plate Hercules, CA). After electrophoresis, the gel was either stained using (9.62 cm2; Nunc, Naperville, IL) were plated in DMEM containing 0.1% Coomassie blue or transferred onto a Sequi-Blot membrane 10% calf serum and 1.6 ␮M biotin. Two days later, when confluent, (Bio-Rad) in CAPS buffer (10 mM CAPS, 40% methanol, pH 11.0) at cells were harvested to prepare apical membrane vesicles. 250 mA constant current for 60 min using a Trans-Blot apparatus (Bio-Rad). Blots were stained using Coomassie blue, or probed with Preparation of MDCKI Cell Apical Membrane a monoclonal anti-Ax-II antibody (BD Transduction Labs) and de- MDCKI cell apical membrane vesicles were prepared according to tected using an HRP-conjugated secondary antibody and an Enhanced a differential centrifugation procedure (21). Confluent monolayers Chemiluminescence (ECL) kit (Amersham Pharmacia Biotech, Pis- were rinsed with ice-cold phosphate-buffered saline (PBS; pH 7.4) cataway, NJ). and then scraped into ice-cold PBS and maintained at 4°C for all subsequent steps. These detached cells were washed twice with ice- Microsequencing of COM-Binding Protein ϫ cold PBS via alternating centrifugation (500 g for 5 min) and In the Mayo Clinic Protein Core, the most prominent COM crystal- resuspension. The cell pellet was resuspended in 10 volumes of buffer binding protein (Mr, 37 kD) was subjected to in situ enzymatic A (50 mM D-mannitol, 15 mM Tris-HEPES, pH 7.2, containing 1 digestion with trypsin at 37°C overnight. The resulting peptide frag- ␮ mM PMSF and 0.1 g/ml pepstatin A) and treated with a Potter- ments were separated by HPLC, collected directly onto a strip of ϫ Elvehjem homogenizer (20 strokes for 1 min 3) followed by a polyvinylidinedifluoride (PVDF) membrane that was subsequently Polytron homogenizer for 1 min (Brinkmann Instruments, Westbury, treated with Biobrene (Applied Biosystems, Foster City, CA) in NY). Magnesium chloride was added to the resulting homogenate methanol and applied to Applied Biosystems Procise 492 HT (Ap- (final concentration, 12 mM), which was stirred continuously for 10 plied Biosystems). The data were analyzed with the ABI Model 610A ϫ min on ice. The suspension was then centrifuged (3000 g for 20 data analysis software (Applied Biosystems). Mass spectrometry anal- ϫ min), and the resulting supernatant further centrifuged (28,000 g for ysis of the digest mixtures was also performed at the Mayo Clinic 20 min). The pellet obtained was homogenized in buffer B (280 mM Protein Core. D-mannitol, 20 mM Tris-HEPES, pH 7.4, containing 1 mM PMSF and 0.1 ␮g/ml pepstatin A) and centrifuged (28,000 ϫ g for 20 min), resuspended in buffer B, and centrifuged once again (28,000 ϫ g for Biotinylation and Streptavidin Precipitation of Cell 20 min). This final pellet was reconstituted in buffer C (50 mM NaCl, Surface Proteins 10 mM Tris, pH 7.4) and stored at Ϫ80°C until used. Exposed surface proteins on intact confluent monolayers were biotinylated using EZ-link Sulfo-NHS-Biotin and isolated using Measurement of Enzyme Markers Streptavidin agarose beads (Pierce) essentially as described (27). Purity of the resulting apical membranes was assessed via activities Confluent MDCKI cell monolayers were placed on ice and washed of apical and basolateral membrane marker enzymes. Alkaline phos- three times with 0.1 M phosphate-buffered saline (PBS-C/M, pH 7.4: ϩ ϩ phatase (22), Na /K -ATPase (23), ␥–glutamyl transpeptidase (24), 0.1 mM CaCl2; 1.0 mM MgCl2). Cells were then incubated with succinate dehydrogenase (25), and glucose-6-phosphatase (26) activ- EZ-link Sulfo-NHS-Biotin (Pierce) at a final concentration of 1.5 ities were all measured as described previously. The protein content of mg/ml into PBS-C/M, pH 8.0, for 60 min at 4°C, followed by glycine the homogenates and apical membrane preparation was determined (100 mM) in PBS-C/M, pH 8.0, to quench unbound labeling reagent, using the BCA-Protein estimation kit (Pierce, Rockford, IL). and then washed two times with PBS-C/M to completely remove any remaining quenching buffer. Biotinylated cells were scraped off the Solubilization of Apical Membrane Proteins and COM plates in lysis buffer-RIPA (150 mM NaCl, 5 mM EDTA, 50 mM Crystal Binding Tris-HCl, pH 7.4, containing 1% Triton X-100, 0.5% sodium deoxy- The non-ionic detergent n-octyl-␤-D-glucopyranoside (NOG) was cholate, 1% SDS, and a EDTA-free protease inhibitor mix), passed ten used to solubilize apical membrane proteins because of its high times through a 23-G needle, and agitated on a shaker for 30 min at ϫ critical micellar concentration.
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