Calcified Tissue International

, Volume 84, Issue 3, pp 240–248 | Cite as

Kinetics of Calcium Oxalate Crystal Growth in the Presence of Osteopontin Isoforms: An Analysis by Scanning Confocal Interference Microcopy

  • Aaron Langdon
  • Geoffrey R. Wignall
  • Kem Rogers
  • Esben S. Sørensen
  • John Denstedt
  • Bernd Grohe
  • Harvey A. Goldberg
  • Graeme K. Hunter
Article

Abstract

Proteins that inhibit the growth and aggregation of calcium oxalate crystals play important roles in the prevention of kidney stone disease. One such protein is osteopontin (OPN), which inhibits the formation of calcium oxalate monohydrate (COM) in a phosphorylation-dependent manner. To determine the role of phosphate groups in the inhibition of COM growth by OPN, we used scanning confocal interference microscopy to compare the effects of highly phosphorylated OPN from cow milk, less phosphorylated OPN from rat bone, and nonphosphorylated recombinant OPN. COM growth was measured in the principal crystallographic directions <001>, <010>, and <100>, representing lattice-ion addition to {121}, {010}, and {100} faces, respectively. While the shapes of growth curves were very consistent from crystal to crystal, absolute growth rates varied widely. To control for this, results were expressed as changes in the aspect ratios <010>/<001> and <100>/<001>. Compared to control, bone OPN increased <010>/<001> and had no effect on <100>/<001>; milk OPN had no effect on <010>/<001>and decreased <100>/<001>; recombinant OPN had no significant effect on either aspect ratio. These findings indicate that milk OPN interacts with COM crystal faces in order of preference {100} > {121} ≈ {010}, whereas bone OPN interacts in order of preference {100}≈{121} > {010}. As {100} is the most Ca2+-rich face of COM, while {010} is the least Ca2+-rich, it appears that the OPN-mediated inhibition of COM growth occurs through a nonspecific electrostatic interaction between Ca2+ ions of the crystal and phosphate groups of the protein.

Keywords

Calcium oxalate monohydrate Osteopontin Biomineralization Confocal microscopy Kidney stone 

References

  1. 1.
    Herring LC (1962) Observations on the analysis of ten thousand urinary calculi. J Urol 88:545–562PubMedGoogle Scholar
  2. 2.
    Prien EL, Prien EL Jr (1968) Composition and structure of urinary stone. Am J Med 45:654–672PubMedCrossRefGoogle Scholar
  3. 3.
    Coe FL, Evan A, Worcester E (2005) Kidney stone disease. J Clin Invest 115:2598–2608PubMedCrossRefGoogle Scholar
  4. 4.
    Marangella M, Bagnis C, Bruno M, Vitale C, Petrarulo M, Ramello A (2004) Crystallization inhibitors in the pathophysiology and treatment of nephrolithiasis. Urol Int 72(Suppl 1):6–10PubMedCrossRefGoogle Scholar
  5. 5.
    Kumar V, Lieske JC (2006) Protein regulation of intrarenal crystallization. Curr Opin Nephrol Hypertens 15:374–380PubMedGoogle Scholar
  6. 6.
    Hunter GK, Kyle CL, Goldberg HA (1994) Modulation of crystal formation by bone phosphoproteins: structural specificity of the osteopontin-mediated inhibition of hydroxyapatite formation. Biochem J 300:723–728PubMedGoogle Scholar
  7. 7.
    Shiraga H, Min W, VanDusen WJ, Clayman MD, Miner D, Terrell CH, Sherbotie JR, Foreman JW, Przysiecki C, Nielson EG, Hoyer JR (1992) Inhibition of calcium oxalate crystal growth in vitro by uropontin: another member of the aspartic acid-rich protein superfamily. Proc Natl Acad Sci USA 89:426–430PubMedCrossRefGoogle Scholar
  8. 8.
    Worcester EM, Blumenthal SS, Beshensky AM, Lewand DL (1992) The calcium oxalate crystal growth inhibitor protein produced by mouse kidney cortical cells in culture is osteopontin. J Bone Miner Res 7:1029–1036PubMedCrossRefGoogle Scholar
  9. 9.
    Wesson JA, Ganne V, Beshensky AM, Kleinman JG (2005) Regulation by macromolecules of calcium oxalate crystal aggregation in stone formers. Urol Res 33:206–212PubMedCrossRefGoogle Scholar
  10. 10.
    Qiu SR, Wierzbicki A, Orme CA, Cody AM, Hoyer JR, Nancollas GH, Zepeda S, De Yoreo JJ (2004) Molecular modulation of calcium oxalate crystallization by osteopontin and citrate. Proc Natl Acad Sci USA 101:1811–1815PubMedCrossRefGoogle Scholar
  11. 11.
    Wesson JA, Worcester EM, Wiessner JH, Mandel NS, Kleinman JG (1998) Control of calcium oxalate crystal structure and cell adherence by urinary macromolecules. Kidney Int 53:952–957PubMedCrossRefGoogle Scholar
  12. 12.
    Taller A, Grohe B, Rogers K, Goldberg HA, Hunter GK (2007) Specific adsorption of osteopontin and synthetic polypeptides to calcium oxalate monohydrate crystals. Biophys J 93:1768–1777PubMedCrossRefGoogle Scholar
  13. 13.
    Jiang XJ, Feng T, Chang LS, Kong XT, Wang G, Zhang ZW, Guo YL (1998) Expression of osteopontin mRNA in normal and stone-forming rat kidney. Urol Res 26:389–394PubMedCrossRefGoogle Scholar
  14. 14.
    Kohri K, Nomura S, Kitamura Y, Nagata T, Yoshioka K, Iguchi M, Yamate T, Umekawa T, Suzuki Y, Sinohara H, Kurita T (1993) Structure and expression of the mRNA encoding urinary stone protein (osteopontin). J Biol Chem 268:15180–15184PubMedGoogle Scholar
  15. 15.
    Yasui T, Fujita K, Sasaki S, Sato M, Sugimoto M, Hirota S, Kitamura Y, Nomura S, Kohri K (1999) Expression of bone matrix proteins in urolithiasis model rats. Urol Res 27:255–261PubMedCrossRefGoogle Scholar
  16. 16.
    Wesson JA, Johnson RJ, Mazzali M, Beshensky AM, Stietz S, Giachelli C, Liaw L, Alpers CE, Couser WG, Kleinman JG, Hughes J (2003) Osteopontin is a critical inhibitor of calcium oxalate crystal formation and retention in renal tubules. J Am Soc Nephrol 14:139–147PubMedCrossRefGoogle Scholar
  17. 17.
    Mo L, Huang HY, Zhu XH, Shapiro E, Hasty DL, Wu XR (2004) Tamm-Horsfall protein is a critical renal defense factor protecting against calcium oxalate crystal formation. Kidney Int 66:1159–1166PubMedCrossRefGoogle Scholar
  18. 18.
    Sørensen ES, Højrup P, Petersen TE (1995) Posttranslational modifications of bovine osteopontin: identification of twenty-eight phosphorylation and three O-glycosylation sites. Protein Sci 4:2040–2049PubMedCrossRefGoogle Scholar
  19. 19.
    Christensen B, Nielsen MS, Haselmann KF, Petersen TE, Sorensen 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 390:285–292PubMedCrossRefGoogle Scholar
  20. 20.
    Hunter GK, Grohe B, Jeffrey S, O’Young J, Sørensen ES, Goldberg HA (2009) Role of phosphate groups in inhibition of calcium oxalate crystal growth by osteopontin. Cells Tissues Organs. 189(1–4):44–50Google Scholar
  21. 21.
    Keykhosravani M, Doherty-Kirby A, Zhang C, Brewer D, Goldberg HA, Hunter GK, Lajoie G (2005) Comprehensive identification of post-translational modifications of rat bone osteopontin by mass spectrometry. Biochemistry 44:6990–7003PubMedCrossRefGoogle Scholar
  22. 22.
    Christensen B, Petersen TE, Sorensen ES (2008) Post-translational modification and proteolytic processing of urinary osteopontin. Biochem J 411:53–61PubMedCrossRefGoogle Scholar
  23. 23.
    Hoyer JR, Asplin JR, Otvos L (2001) Phosphorylated osteopontin peptides suppress crystallization by inhibiting the growth of calcium oxalate crystals. Kidney Int 60:77–82PubMedCrossRefGoogle Scholar
  24. 24.
    Wang LJ, Guan XY, Tang RK, Hoyer JR, Wierzbicki A, De Yoreo JJ, Nancollas GH (2008) Phosphorylation of osteopontin is required for inhibition of calcium oxalate crystallization. J Phys Chem B 112:9151–9157PubMedCrossRefGoogle Scholar
  25. 25.
    Hincke MT, St Maurice M (2000) Phosphorylation-dependent modulation of calcium carbonate precipitation by chicken eggshell matrix proteins. In: Goldberg M, Boskey A, Robinson C (eds) Chemistry and biology of mineralized tissues. American Academy of Orthopaedic Surgeons, Rosemont, IL, pp 13–17Google Scholar
  26. 26.
    Tazzoli V, Domenghetti C (1980) The crystal structures of whewellite and weddellite: re-examination and comparison. Am Mineralog 65:327–334Google Scholar
  27. 27.
    Grohe W, Rogers K, Goldberg HA, Hunter GK (2006) Crystallization kinetics of calcium oxalate hydrates studied by scanning confocal interference microscopy. J Crystal Growth 295:148–157CrossRefGoogle Scholar
  28. 28.
    Goldberg HA, Sodek J (1994) Purification of mineralized tissue-associated osteopontin. J Tissue Culture Methods 16:211–215CrossRefGoogle Scholar
  29. 29.
    Sorensen ES, Petersen TE (1993) Purification and characterization of three proteins isolated from the proteose peptone fraction of bovine milk. J Dairy Res 60:189–197PubMedCrossRefGoogle Scholar
  30. 30.
    Millan A (2001) Crystal growth shape of whewellite polymorphs: influence of structure distortions on crystal shape. Crystal Growth Des 1:245–254CrossRefGoogle Scholar
  31. 31.
    Guo SW, Ward MD, Wesson JA (2002) Direct visualization of calcium oxalate monohydrate crystallization and dissolution with atomic force microscopy and the role of polymeric additives. Langmuir 18:4284–4291CrossRefGoogle Scholar
  32. 32.
    Jung T, Sheng X, Choi CK, Kim WS, Wesson JA, Ward MD (2004) Probing crystallization of calcium oxalate monohydrate and the role of macromolecule additives with in situ atomic force microscopy. Langmuir 20:8587–8596PubMedCrossRefGoogle Scholar
  33. 33.
    Addadi L, Weiner S (1985) Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization. Proc Natl Acad Sci USA 82:4110–4114PubMedCrossRefGoogle Scholar
  34. 34.
    Kile DE, Eberl DD, Hoch AR, Reddy MM (2000) An assessment of calcite crystal growth mechanisms based on crystal size distributions. Geochim Cosmochim Acta 64:2937–2950CrossRefGoogle Scholar
  35. 35.
    Kile DE, Eberl DD (2003) On the origin of size-dependent and size-independent crystal growth: influence of advection and diffusion. Am Mineralog 88:1514–1521Google Scholar
  36. 36.
    McCabe WL (1929) Crystal growth in aqueous solutions. Ind Eng Chem 21:30–33CrossRefGoogle Scholar
  37. 37.
    Tomazic B, Nancollas GH (1979) Kinetics of dissolution of calcium-oxalate hydrates. J Crystal Growth 46:355–361CrossRefGoogle Scholar
  38. 38.
    Zauner R, Jones AG (2000) Determination of nucleation, growth, agglomeration and disruption kinetics from experimental precipitation data: the calcium oxalate system. Chem Eng Sci 55:4219–4232CrossRefGoogle Scholar
  39. 39.
    Sheng X, Jung T, Wesson JA, Ward MD (2005) Adhesion at calcium oxalate crystal surfaces and the effect of urinary constituents. Proc Natl Acad Sci USA 102:267–272PubMedCrossRefGoogle Scholar
  40. 40.
    Qiu SR, Wierzbicki A, Salter EA, Zepeda S, Orme CA, Hoyer JR, Nancollas GH, Cody AM, De Yoreo JJ (2005) Modulation of calcium oxalate monohydrate crystallization by citrate through selective binding to atomic steps. J Am Chem Soc 127:9036–9044PubMedCrossRefGoogle Scholar
  41. 41.
    Boskey AL, Maresca M, Ullrich W, Doty SB, Butler WT, Prince CW (1993) Osteopontin–hydroxyapatite interactions in vitro. Inhibition of hydroxyapatite formation and growth in a gelatin-gel. Bone Miner 22:147–159PubMedCrossRefGoogle Scholar
  42. 42.
    Jono S, Peinado C, Giachelli CM (2000) Phosphorylation of osteopontin is required for inhibition of vascular smooth muscle cell calcification. J Biol Chem 275:20197–20203PubMedCrossRefGoogle Scholar
  43. 43.
    Pampena DA, Robertson KA, Litvinova O, Lajoie G, Goldberg HA, Hunter GK (2004) Inhibition of hydroxyapatite formation by osteopontin phosphopeptides. Biochem J 378:1083–1087PubMedCrossRefGoogle Scholar
  44. 44.
    Grohe B, O’Young J, Ionescu DA, Lajoie G, Rogers KA, Karttunen M, Goldberg HA, Hunter GK (2007) Control of calcium oxalate crystal growth by face-specific adsorption of an osteopontin phosphopeptide. J Am Chem Soc 129(48):14946–14951PubMedCrossRefGoogle Scholar
  45. 45.
    Hauschka PV, Wians FH Jr (1989) Osteocalcin–hydroxyapatite interaction in the extracellular organic matrix of bone. Anat Rec 224:180–188PubMedCrossRefGoogle Scholar
  46. 46.
    Huq NL, Cross KJ, Reynolds EC (2000) Molecular modelling of a multiphosphorylated sequence motif bound to hydroxyapatite surfaces. J Mol Model 6:35–47CrossRefGoogle Scholar
  47. 47.
    Wen D, Laursen RA (1992) A model for binding of an antifreeze polypeptide to ice. Biophys J 63:1659–1662PubMedCrossRefGoogle Scholar
  48. 48.
    Furedi-Milhofer H, Moradian-Oldak J, Weiner S, Veis A, Mintz KP, Addadi L (1994) Interactions of matrix proteins from mineralized tissues with octacalcium phosphate. Connect Tissue Res 30:251–264PubMedCrossRefGoogle Scholar
  49. 49.
    Fisher LW, Torchia DA, Fohr B, Young MF, Fedarko NS (2001) Flexible structures of SIBLING proteins, bone sialoprotein and osteopontin. Biochem Biophys Res Commun 280:460–465PubMedCrossRefGoogle Scholar
  50. 50.
    Gericke A, Qin C, Spevak L, Fujimoto Y, Butler WT, Sorensen ES, Boskey AL (2005) Importance of phosphorylation for osteopontin regulation of biomineralization. Calcif Tissue Int 77:45–54PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Aaron Langdon
    • 1
    • 2
    • 3
  • Geoffrey R. Wignall
    • 4
  • Kem Rogers
    • 5
  • Esben S. Sørensen
    • 6
  • John Denstedt
    • 4
  • Bernd Grohe
    • 1
    • 2
  • Harvey A. Goldberg
    • 1
    • 2
    • 3
  • Graeme K. Hunter
    • 1
    • 2
    • 3
  1. 1.CIHR Group in Skeletal Development and RemodelingUniversity of Western OntarioLondonCanada
  2. 2.School of DentistryUniversity of Western OntarioLondonCanada
  3. 3.Department of BiochemistryUniversity of Western OntarioLondonCanada
  4. 4.Department of SurgeryUniversity of Western OntarioLondonCanada
  5. 5.Department of Anatomy and Cell BiologyUniversity of Western OntarioLondonCanada
  6. 6.Department of Molecular BiologyUniversity of AarhusAarhusDenmark

Personalised recommendations