Abstract
In vivo, urinary crystals are associated with proteins located within the mineral bulk as well as upon their surfaces. Proteins incarcerated within the mineral phase of retained crystals could act as a defence against urolithiasis by rendering them more vulnerable to destruction by intracellular and interstitial proteases. The aim of this study was to examine the effects of intracrystalline and surface-bound osteopontin (OPN) on the degradation and dissolution of urinary calcium oxalate dihydrate (COD) crystals in cultured Madin Darby canine kidney (MDCK) cells. [14C]-oxalate-labelled COD crystals with intracrystalline (IC), surface-bound (SB) and IC + SB OPN, were generated from ultrafiltered (UF) urine containing 0, 1 and 5 mg/L human milk OPN and incubated with MDCKII cells, using UF urine as the binding medium. Crystal size and degradation were assessed using field emission scanning electron microscopy (FESEM) and dissolution was quantified by the release of radioactivity into the culture medium. Crystal size decreased directly with OPN concentration. FESEM examination indicated that crystals covered with SB OPN were more resistant to cellular degradation than those containing IC OPN, whose degree of disruption appeared to be related to OPN concentration. Whether bound to the crystal surface or incarcerated within the mineral interior, OPN inhibited crystal dissolution in direct proportion to its concentration. Under physiological conditions OPN may routinely protect against stone formation by inhibiting the growth of COD crystals, which would encourage their excretion in urine and thereby perhaps partly explain why, compared with calcium oxalate monohydrate crystals, COD crystals are more prevalent in urine, but less common in kidney stones.
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References
Vervaet BA, Verhulst A, D’Haese PC, De Broe ME (2009) Nephrocalcinosis: new insights into mechanisms and consequences. Nephrol Dial Transpl 24:2030–2035
Coe FL, Evan AP, Worcester EM, Lingeman JE (2010) Three pathways for human kidney stone formation. Urol Res 38:147–160
Khan SR (1995) Experimental calcium oxalate nephrolithiasis and the formation of human urinary stones. Scan Microsc Int 9:89–101
Evan AP, Coe FL, Rittling SR, Bledsoe SB, Shao Y, Lingeman JE, Worcester EM (2005) Apatite plaque particles in inner medulla of kidneys of calcium oxalate stone formers: osteopontin localization. Kidney Int 68:145–154
Evan AP, Lingeman JE, Worcester EM, Bledsoe SB, Sommer AJ, Williams JC, Krambeck AE, Philips CL, Coe FL (2010) Renal histopathology and crystal deposits in patients with small bowel resection and calcium oxalate stone disease. Kidney Int 78:310–317
Evan AP, Coe FL, Gillen D, Lingeman JE, Bledsoe S, Worcester EM (2008) Renal intratubular crystals and hyaluronan staining occur in stone formers with bypass surgery but not with idiopathic CaOx stones. Anat Rec 291:325–334
Verhulst A, Asselman M, De Naeyer S, Vervaet BA, Mengel M, Gwinner W, D’Haese PC, Verkoelen CF, De Broe ME (2005) Preconditioning of the distal tubular epithelium of the human kidney precedes nephrocalcinosis. Kidney Int 68:1643–1647
Vervaet BA, Verhulst A, Dauwe SE, De Broe ME, D’Haese PC (2009) An active renal crystal clearance mechanism in rat and man. Kidney Int 75:41–51
Evan AP, Lingeman JE, Coe FL, Parks JH, Bledsoe SB, Shao Y, Sommers AJ, Paterson RF, Kuo RL, Grynpas M (2003) Randall’s plaque of patients with nephrolithiasis begins in basement membranes of thin loops of Henle. J Clin Invest 111:607–616
Beer E (1904) Lime deposits especially the so-called “kalkmetastasen”, in the kidney. J Pathol Bacteriol 9:225–233
Stout HA, Akin RH, Morton E (1955) Nephrocalcinosis in routine necropsies: its relationship to stone formation. J Urol 74:8–22
Bennington JL, Haber SL, Smith JV, Warner NE (1964) Crystals of calcium oxalate in the human kidney. Am J Clin Pathol 41:8–14
Ebisuno S, Kohjimoto Y, Tamura M, Inagaki T, Ohkawa T (1997) Histological observations of the adhesion and endocytosis of calcium oxalate crystals in MDCK cells and in rat and human kidney. Urol Int 58:227–231
Vervaet BA, D’Haese PC, De Broe ME, Verhulst A (2009) Crystalluric and tubular epithelial parameters during the onset of intratubular nephrocalcinosis: illustration of the ‘fixed particle’ theory in vivo. Nephrol Dial Transpl 24:3659–3668
Kumar V, Farell G, Yu S, Harrington S, Fitzpatrick L, Rzewuska E, Miller VM, Lieske JC (2006) Cell biology of pathologic renal calcification: contribution of crystal transcytosis, cell-mediated calcification, and nanoparticles. J Invest Med 54:412–424
Ryall RL (2011) The possible roles of inhibitors, promoters and macromolecules in the formation of calcium kidney stones. In: Rao N, Kavanagh JP, Preminger G (eds) Urinary tract stone disease. Springer, London, pp 31–60
Khan SR, Kok DJ (2004) Modulators of urinary stone formation. Front Biosci 9:1450–1482
Ryall RL (2004) Macromolecules and urolithiasis: parallels and paradoxes. Nephron Physiol 98:37–42
Kumar V, Yu S, Farell G, Toback FG, Lieske JC (2004) Renal epithelial cells constitutively produce a protein that blocks adhesion of crystals to their surface. Am J Physiol Renal Physiol 287:F373–F383
Lieske JC, Leonard R, Toback FG (1995) Adhesion of calcium oxalate monohydrate crystals to renal epithelial cells is inhibited by specific anions. Am J Physiol Renal Physiol 268:F604–F612
Kohjimoto Y, Ebisuno S, Tamura M, Ohkawa T (1996) Adhesion and endocytosis of calcium oxalate crystals on renal tubular cells. Scanning Microsc 10:459–470
Lieske JC, Toback FG (1993) Regulation of renal epithelial cell endocytosis of calcium oxalate monohydrate crystals. Am J Physiol Renal Physiol 264:F800–F807
Tsujihata M, Yoshimura K, Tsujikawa K, Tei N, Okuyama A (2006) Fibronectin inhibits endocytosis of calcium oxalate crystals by renal tubular cells. Int J Urol 13:743–746
Ebisuno S, Nishihata M, Inagaki T, Umehara M, Kohjimoto Y (1999) Bikunin prevents adhesion of calcium oxalate crystal to renal tubular cells in human urine. J Am Soc Nephrol 10(Suppl 14):S436–S440
Tei N, Tsujihata M, Tsujikawa K, Yoshimura K, Nonomura N, Okuyama A (2006) Hepatocyte growth factor has protective effects on crystal–cell interactions and crystal deposits. Urology 67:864–869
Verkoelen CF, Van Der Boom BG, Romijn JC (2000) Identification of hyaluronan as a crystal-binding molecule at the surface of migrating and proliferating MDCK cells. Kidney Int 58:1045–1054
Verkoelen CF, van der Boom BG, Houtsmuller AB, Schröder FH, Romijn JC (1998) Increased calcium oxalate monohydrate crystal binding to injured renal tubular epithelial cells in culture. Am J Physiol 274:F958–F965
Verhulst A, Asselman M, Persy VP, Schepers MS, Helbert MF, Verkoelen CF, De Broe ME (2003) Crystal retention capacity of cells in the human nephron: involvement of CD44 and its ligands hyaluronic acid and osteopontin in the transition of a crystal binding- into a non-adherent epithelium. J Am Soc Nephrol 14:107–114
Asselman M, Verhulst A, De Broe ME, Verkoelen CF (2003) Calcium oxalate crystal adherence to hyaluronan-, osteopontin-, and CD44-expressing injured/regenerating tubular epithelial cells in rat kidneys. J Am Soc Nephrol 14:3155–3166
Yamate T, Kohri K, Umekawa T, Amasaki N, Amasaki N, Isikawa Y, Iguchi M, Kurita T (1996) The effect of osteopontin on the adhesion of calcium oxalate crystals to Madin–Darby canine kidney cells. Eur Urol 30:388–393
Yamate T, Kohri K, Umekawa T, Iguchi M, Kurita T (1998) Osteopontin antisense oligonucleotide inhibits adhesion of calcium oxalate crystals in Madin–Darby canine kidney cell. J Urol 160:1506–1512
Yamate T, Kohri K, Umekawa T, Konya E, Ishikawa Y, Iguchi M, Kurita T (1999) Interaction between osteopontin on Madin Darby canine kidney cell membrane and calcium oxalate crystal. Urol Int 62:81–86
Sorokina EA, Wesson JA, Kleinman JG (2004) An acidic peptide sequence of nucleolin-related protein can mediate the attachment of calcium oxalate to renal tubule cells. J Am Soc Nephrol 15:2057–2065
Kumar V, Farell G, Deganello S, Lieske JC (2003) Annexin II is present on renal epithelial cells and binds calcium oxalate monohydrate crystals. J Am Soc Nephrol 14:289–297
Kohri K, Kodama M, Ishikawa Y, Katayama Y, Matsuda H, Imanishi M, Takada M, Katoh Y, Kataoka K, Akiyama T (1991) Immunofluorescent study on the interaction between collagen and calcium oxalate crystals in the renal tubules. Eur Urol 19:249–252
Asselman M, Verkoelen CF (2002) Crystal-cell interaction in the pathogenesis of kidney stone disease. Curr Opin Urol 12:271–276
Kramer G, Steiner GE, Prinz-Kashani M, Bursa B, Marberger M (2003) Cell-surface matrix proteins and sialic acids in cell–crystal adhesion; the effect of crystal binding on the viability of human CAKI-1 renal epithelial cells. Br J Urol 91:554–559
de Bruijn WC, Boevé ER, van Run PR, van Miert PP, de Water R, Romijn JC, Verkoelen CF, Cao LC, Schröder FH (1995) Etiology of calcium oxalate nephrolithiasis in rats. I. Can this be a model for human stone formation? Scanning Microsc 9:103–114
de Bruijn WC, Boevé ER, van Run PR, van Miert PP, Romijn JC, Verkoelen CF, Cao LC, Schröder FH (1994) Etiology of experimental cacluium oxalate monohydrate nephrolithiasis in rats. Scanning Microsc 8:541–549
de Water R, Noordermeer C, Houtsmuller AB, Nigg AL, Stijnen T, Schröder FH, Kok DJ (2000) The role of macrophages in nephrolithiasis in rats: an analysis of the renal interstitium. Am J Kidney Dis 36:615–625
de Water R, Leenen PJ, Noordermeer C, Nigg AL, Houtsmuller AB, Kok DJ, Schröder FH (2001) Cytokine production induced by binding and processing of calcium oxalate crystals in cultured macrophages. Am J Kidney Dis 38:331–338
de Water R, Nordermeer C, van der Kwast TH, Nizze H, Boevé ER, Kok DJ, Schröder FH (1999) Calcium oxalate nephrolithiasis: effect of renal crystal deposition on the cellular composition of the renal interstitium. Am J Kidney Dis 33:761–771
Schepers MS, Duim RA, Asselman M, Romijn JC, Schröder FH, Verkoelen CF (2003) Internalization of calcium oxalate crystals by renal tubular cells: a nephron segment-specific process? Kidney Int 64:493–500
Chauvet MC, Ryall RL (2005) Intracrystalline proteins and calcium oxalate crystal degradation in MDCK II cells. J Struct Biol 151:12–17
Grover PK, Thurgood LA, Fleming DE, van Bronswijk W, Wang T, Ryall RL (2008) Intracrystalline urinary proteins facilitate degradation and dissolution of calcium oxalate crystals in cultured renal cells. Am J Physiol Renal Physiol 294:F355–F361
Lieske JC, Swift H, Martin T, Patterson B, Toback FG (1994) Renal epithelial cells rapidly bind and internalize calcium oxalate monohydrate crystals. Proc Natl Acad Sci 91:6987–6991
Lieske JC, Norris R, Swift H, Toback FG (1997) Adhesion, internalization and metabolism of calcium oxalate monohydrate crystals by renal epithelial cells. Kidney Int 52:1291–1301
Lieske JC, Deganello S, Toback FG (1999) Cell-crystal interactions and kidney stone formation. Nephron 81:8–17
Lieske JC, Walsh‐Reitz MM, Toback FG (1992) Calcium oxalate monohydrate crystals are endocytosed by renal epithelial cells and induce proliferation. Am J Physiol 262:F622–F630
Lieske JC, Toback FG, Deganello S (1998) Direct nucleation of calcium oxalate dihydrate crystals onto the surface of living renal epithelial cells in culture. Kidney Int 54:796–803
Ryall RL, Fleming DE, Grover PK, Chauvet M, Dean CJ, Marshall VR (2000) The hole truth: intracrystalline proteins and calcium oxalate kidney stones. Mol Urol 4:391–402
Ryall RL, Fleming DE, Doyle IR, Evans NA, Dean CJ, Marshall VR (2001) Intracrystalline proteins and the hidden ultrastructure of calcium oxalate urinary crystals: implications for kidney stone formation. J Struct Biol 134:5–14
Ryall RL, Chauvet MC, Grover PK (2005) Intracrystalline proteins and urolithiasis: a comparison of the protein content and ultrastructure of urinary calcium oxalate monohydrate and dihydrate crystals. Br J Urol 96:654–663
Fleming DE, van Riessen A, Chauvet MC, Grover PK, Hunter B, van Bronswijk W, Ryall RL (2003) Intracrystalline proteins and urolithiasis: a synchrotron X-ray diffraction study of calcium oxalate monohydrate. J Bone Min Res 18:1282–1291
Wang T, Thurgood LA, Grover PK, Ryall RL (2010) A comparison of the binding of urinary calcium oxalate monohydrate and dihydrate crystals to human kidney cells in urine. Br J Urol Int 106:1768–1774
Lieske JC, Deganello S (1999) Nucleation, adhesion and internalization of calcium-containing urinary crystals by renal cells. J Am Nephrol Soc 10:S422–S429
Semangoen T, Sinchaikul S, Chen ST, Thongboonkerd V (2008) Altered proteins in MDCK renal tubular cells in response to calcium oxalate dihydrate crystal adhesion: a proteomics approach. J Proteome Res 7:2889–2896
Webber D, Chauvet MC, Ryall RL (2005) Proteolysis and partial dissolution of calcium oxalate: a comparative, morphological study of urinary crystals from black and white subjects. Urol Res 33:273–284
Chien YC, Masica DL, Gray JJ, Nguyen S, Vali H, McKee MD (2009) Modulation of calcium oxalate dihydrate growth by selective crystal-face binding of phosphorylated osteopontin and poly-aspartate peptide showing occlusion by sectoral (compositional) zoning. J Biol Chem 284:23491–23501
Thurgood LA, Cook AF, Sørensen ES, Ryall RL (2010) Face-specific incorporation of osteopontin into urinary and inorganic calcium oxalate monohydrate and dihydrate crystals. Urol Res 38:357–376
Thurgood LA, Wang T, Chataway TK, Ryall RL (2010) Comparison of the specific incorporation of intracrystalline proteins into urinary calcium oxalate monohydrate and dihydrate crystals. J Proteome Res 9:4745–4757
Shiraga H, Min W, VanDusen WJ, Clayman MD, Miner D, Terrell CH, Sherbotie JR, Foreman JW, Przysiecki C, Neilson EG, Hoyer JR (1992) Inhibition of calcium oxalate crystal growth in vitro by uropontin: another member of the aspartic acid-rich protein superfamily. PNAS 89:426–430
Asplin JR, Arsenault D, Parks JH, Coe FL, Hoyer JR (1998) Contribution of uropontin to inhibition of calcium oxalate crystallization. Kidney Int 53:194–199
Nishio S, Hatanaka M, Takeda H, Aoki K, Iseda T, Iwata H, Yokoyama M (2001) Calcium phosphate crystal-associated proteins: alpha-2-HS-glycoprotein, prothrombin fragment 1 and osteopontin. Int J Urol 8:S58–S62
Thurgood LA, Sorensen ES, Ryall RL (2011) The effect of intracrystalline and surface-bound osteopontin on the attachment of calcium oxalate dihydrate crystals to MDCKII cells in ultrafiltered human urine. Br J Urol (in press)
Kleinman JG, Wesson JA, Hughes J (2004) Osteopontin and calcium stone formation. Nephron Physiol 98:43–47
Okada A, Nomura S, Saeki Y, Higashibata Y, Hamamoto S, Hirose M, Itoh Y, Yasui T, Tozawa K, Kohri K (2008) Morphological conversion of calcium oxalate crystals into stones is regulated by osteopontin in mouse kidney. J Bone Miner Res 23:1629–1637
Hamamoto S, Nomura S, Yasui T, Okada A, Hirose M, Shimizu H, Itoh Y, Tozawa K, Kohri K (2010) Effects of impaired functional domains of osteopontin on renal crystal formation: analyses of OPN-transgenic and OPN-knockout mice. J Bone Miner Res 25:2436–2447
Senger DR, Perruzzi CA, Papadopoulos A, Tenen DG (1989) Purification of a human milk protein closely similar to tumor-secreted phosphoproteins and osteopontin. Biochim Biophys Acta 996:43–48
Christensen B, Nielsen MS, Haselmann KF, Petersen TE, Sørensen ES (2005) Post-translationally modified residues of native human osteopontin are located in clusters: identification of 36 phosphorylation and five O-glycosylation sites and their biological implications. Biochem J 390:285–292
Bautista DS, Denstedt JM, Chamber AF, Harris JF (1996) Low-molecular-weight variants of osteopontin generated by serine proteinases in urine of patients with kidney stones. J Cell Biochem 61:402–409
Thurgood LA, Grover PK, Ryall RL (2008) High calcium concentration and calcium oxalate crystals cause significant inaccuracies in the measurement of urinary osteopontin by enzyme linked immunosorbent assay. Urol Res 36:103–110
Ryall RL, Grover PK, Thurgood LA, Chauvet MC, Fleming DE, van Bronswijk W (2007) The importance of a clean face: the effect of different washing procedures on the association of Tamm-Horsfall glycoprotein and other urinary proteins with calcium oxalate crystals. Urol Res 35:1–14
Verkoelen CF, van der Boom BG, Kok DJ, Houtsmuller AB, Visser P, Schröder FH, Romijn JC (1999) Cell type-specific acquired protection from crystal adherence by renal tubule cells in culture. Kidney Int 55:1426–1433
Grover PK, Thurgood LA, Ryall RL (2007) Effect of urine fractionation on attachment of calcium oxalate crystals to renal epithelial cells: implications for studying renal calculogenesis. Am J Physiol Renal Physiol 292:F1396–F1403
Walton RC, Kavanagh JP, Heywood BR (2003) The density and protein content of calcium oxalate crystals precipitated from human urine: a tool to investigate ultrastructure and the fractional volume occupied by organic matrix. J Struct Biol 143:2–14
Belliveau J, Griffin H (2001) The solubility of calcium oxalate in tissue culture media. Anal Biochem 291:69–73
Grover PK, Thurgood LA, Wang T, Ryall RL (2010) The effects of intracrystalline and surface-bound proteins on the attachment of calcium oxalate monohydrate crystals to renal cells in undiluted human urine. Br J Urol 105:708–715
Hsu WL, Lin MJ, Hsu JP (2009) Dissolution of solid particles in liquids: a shrinking core model. World Acad Sci Eng Technol Chem Mater Eng 2:4–8
Addadi L, Joester D, Nudelman F, Weiner S (2006) Mollusk shell formation: a source of new concepts for understanding biomineralization processes. Chemistry 12:980–987
Qiu SR, Orme CA (2008) Dynamics of biomineral formation at the near-molecular level. Chem Rev 108:4784–4822
Fleming DE (2004) Urolithiasis: occurrence and function of intracrystalline proteins in calcium oxalate monohydrate crystals. Dissertation, Curtin University of Technology, Western Australia. http://espace.library.curtin.edu.au/R?func=search-simple-go&ADJACENT=Y&REQUEST=adt-WCU20050124.093851
White DJ, Coyle-Rees M, Nancollas GH (1988) Kinetic factors influencing the dissolution behaviour of calcium oxalate stones: a constant composition study. Calcif Tissue Int 43:319–327
Lepage L, Tawashi R (1982) Growth and characterization of calcium oxalate dihydrate crystals (weddellite). J Pharm Sci 71:1059–1062
Harrell PC, McCawley LJ, Fingleton B, McIntyre JO, Matrisian LM (2005) Proliferative effects of apical, but not basal, matrix metalloproteinase-7 activity in polarized MDCK cells. Exp Cell Res 303:308–320
McGwire GB, Becker RP, Skidgel RA (1999) Carboxypeptidase M, a glycosylphosphatidylinositol-anchored protein, is localized on both the apical and basolateral domains of polarized Madin-Darby canine kidney cells. J Biol Chem 274:31632–31640
Gstraunthaler G, Pfaller W, Kotanko P (1985) Biochemical characterization of renal epithelial cell cultures (LLC-PK1 and MDCK). Am J Physiol 248:F536–F544
Hackett RL, Shevock PN, Khan SR (1994) Madin-Darby canine kidney cells are injured by exposure to oxalate and to calcium oxalate crystals. Urol Res 22:197–204
Richardson JC, Scalera V, Simmons NL (1981) Identification of two strains of MDCK cells which resemble separate nephron tubule segments. Biochim Biophys Acta 673:26–36
Oliveira V, Ferro ES, Gomes MD, Oshiro ME, Almeida PC, Juliano MA, Juliano L (2000) Characterization of thiol-, aspartyl-, and thiol-metallo-peptidase activities in Madin-Darby canine kidney cells. J Cell Biochem 76:478–488
Shalamanova L, Kübler B, Scharf JG, Braulke T (2001) MDCK cells secrete neutral proteases cleaving insulin-like growth factor-binding protein-2 to -6. Am J Physiol Endocrinol Metab 281:E1221–E1229
Andersson G, Ek-Rylander B, Hollberg K, Ljusberg-Sjölander J, Lång P, Norgård M, Wang Y, Zhang SJ (2003) TRACP as an osteopontin phosphatase. J Bone Miner Res 18:1912–1915
Christensen B, Schack L, Kläning E, Sørensen ES (2010) Osteopontin is cleaved at multiple sites close to its integrin-binding motifs in milk and is a novel substrate for plasmin and cathepsin D. J Biol Chem 285:7929–7937
Agnihotri R, Crawford HC, Haro H, Matrisian LM, Havrda MC, Liaw L (2001) Osteopontin, a novel substrate for matrix metalloproteinase-3 (stromelysin-1) and matrix metalloproteinase-7 (matrilysin). J Biol Chem 276:28261–28267
Moriyama MT, Domiki C, Miyazawa K, Tanaka T, Suzuki K (2005) Effects of oxalate exposure on Madin-Darby canine kidney cells in culture: renal prothrombin fragment-1 mRNA expression. Urol Res 33:470–475
Hartz PA, Wilson PD (1997) Functional defects in lysosomal enzymes in autosomal dominant polycystic kidney disease (ADPKD): abnormalities in synthesis, molecular processing, polarity, and secretion. Biochem Mol Med 60:8–26
Neame PJ, Butler WT (1996) Post-translational modification in rat bone osteopontin. Connect Tissue Res 35:145–150
Christensen B, Kazanecki CC, Petersen TE, Rittling SR, Denhardt DT, Sørensen ES (2007) Cell type-specific post-translational modifications of mouse osteopontin are associated with different adhesive properties. J Biol Chem 282:19463–19472
Kasemo B, Lausmaa J (1994) Material-tissue interfaces: the role of surface properties and processes. Environ Health Perspect 102(Suppl 5):41–45
Malmström J, Shipovskov S, Christensen B, Sørensen ES, Kingshott P, Sutherland DS (2009) Adsorption and enzymatic cleavage of osteopontin at interfaces with different surface chemistries. Biointerphases 4:47–55
Nishiyama K, Sugawara K, Nouchi T, Kawano N, Soejima K, Abe S, Mizokami H (2008) Purification and cDNA cloning of a novel protease inhibitor secreted into culture supernatant by MDCK cells. Biologicals 36:122–133
Kon S, Ikesue M, Kimura C, Aoki M, Nakayama Y, Saito Y, Kurotaki D, Diao H, Matsui Y, Segawa T, Maeda M, Kojima T, Uede T (2008) Syndecan-4 protects against osteopontin-mediated acute hepatic injury by masking functional domains of osteopontin. J Exp Med 205:25–33
Shanmugam V, Chackalaparampil I, Kundu GC, Mukherjee AB, Mukherjee BB (1997) Altered sialylation of osteopontin prevents its receptor-mediated binding on the surface of oncogenically transformed TSB77 cells. Biochem 36:5729–5738
Kugler P, Wolf G, Scherberich J (1985) Histochemical demonstration of peptidases in the human kidney. Histochem 83:337–341
Singh AK (1993) Presence of lysosomal enzymes in the normal glomerular basement membrane matrix. Histochem J 25:562–568
Yokota S, Tsuji H, Kato K (1985) Immunocytochemica localization of cathepsin D in lysosomes of cortical collecting tubule cells of the rat kidney. J Histochem Cytochem 33:191–200
ATCC (2011) ATCC catalogue search. http://www.atcc.org/ATCCAdvancedCatalogSearch/ProductDetails/tabid/452/Default.aspx?ATCCNum=CRL-2936&Template=cellBiology. Accessed 16 March 2011
Huang HS, Chen CF, Chien CT, Chen J (2000) Possible biphasic changes of free radicals in ethylene glycol-induced nephrolithaisis in rats. BJU Int 85:1143–1149
Baggio B, Gambaro G, Ossi E, Favaro S, Borsatti A (1983) Increased urinary excretion of renal enzymes in idiopathic calcium oxalate nephrolithiasis. J Urol 129:1161–1162
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Support from the National Institute of Diabetes and Digestive and Kidney Diseases (Grant 1R01-DK-064050-01A1), and Flinders Medical Centre Foundation and Volunteer Service is gratefully acknowledged.
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Thurgood, L.A., Sørensen, E.S. & Ryall, R.L. The effect of intracrystalline and surface-bound osteopontin on the degradation and dissolution of calcium oxalate dihydrate crystals in MDCKII cells. Urol Res 40, 1–15 (2012). https://doi.org/10.1007/s00240-011-0423-5
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DOI: https://doi.org/10.1007/s00240-011-0423-5