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Urolithiasis

pp 1–14 | Cite as

Development of a two-stage in vitro model system to investigate the mineralization mechanisms involved in idiopathic stone formation: stage 1—biomimetic Randall’s plaque using decellularized porcine kidneys

  • Archana C. Lovett
  • Saeed R. Khan
  • Laurie B. GowerEmail author
Original Paper
  • 136 Downloads

Abstract

Idiopathic calcium oxalate (CaOx) stone formers form stones that are commonly attached to calcium phosphate (CaP) deposits in the renal tissue, known as Randall’s plaques (RP). Plaques are suggested to originate in the renal tubular basement membrane, where they exhibit a morphology of concentrically laminated apatitic spherules, while in the interstitial regions, the collagen fibrils and vesicles become mineralized. We hypothesize that these minerals might form by non-classical crystallization mechanisms, such as via amorphous precursors, some of which might originate from a polymer-induced liquid-precursor (PILP) process. Thus, our goal is to identify mineralogical ‘signatures’ of various stone formation mechanisms. To do this for idiopathic CaOx stones, we are developing a two-stage model system of CaP–CaOx composite stones, consisting of stage (1) CaP mineralized plaque, followed by stage (2) CaOx overgrowth into a stone. For the studies presented here, decellularized porcine kidneys were mineralized with CaP using polyaspartic acid or the protein osteopontin (OPN) to induce the PILP process and create biomimetic RP. Analysis of the PILP-mineralized tissues shows features that resemble the native plaques, including mineral spherules and collagen with intrafibrillar mineral. In contrast, the classical crystallization produced large apatitic spherulites, which is a very different morphology, but one which is also found in some stones. An alternative hypothesis regarding Randall’s plaque, and if or when it becomes pathological, is discussed.

Keywords

Randall’s plaque Urolithiasis Kidney Stones Osteopontin Biomimetic model system PILP 

Notes

Acknowledgements

Research reported in this publication was supported by the National Institute of Diabetes And Digestive And Kidney Diseases of the National Institutes of Health under Award Number R01DK092311. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. We thank Drs. Brad Willenberg, Edward Ross (College of Medicine, University of Central Florida), and Christopher Batich (Department of Materials Science and Engineering, University of Florida) for providing the decellularized porcine kidney tissues. We would also like to thank Drs. Sharon Matthews and Jill Verlander for their training and expertise in tissue sample preparation, microtomy, and microscopy done at the College of Medicine Electron Microscopy Core Facility at the University of Florida.

Funding

There were no external sources of funding beyond the NIH grant acknowledged above.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest in this work.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed (UF IACUC Protocol # 201607895).

Supplementary material

240_2018_1060_MOESM1_ESM.doc (43.7 mb)
Supplementary material 1 (DOC 44698 KB)

References

  1. 1.
    Miller NL, Gillen DL, Williams JC, Evan AP, Bledsoe SB, Coe FL, Worcester EM, Matlaga BR, Munch LC, Lingeman JE (2009) A formal test of the hypothesis that idiopathic calcium oxalate stones grow on Randall’s plaque. BJU Int 103(7):966–971.  https://doi.org/10.1111/j.1464-410X.2008.08193.x CrossRefPubMedGoogle Scholar
  2. 2.
    Rodgers AL, De Klerk DP (1986) Crystalluria and urolithiasis in a relatively stone-free population. Scan Electron Microsc (Pt 3):1157–1167Google Scholar
  3. 3.
    Coe FL, Evan AP, Worcester EM, Lingeman JE (2010) Three pathways for human kidney stone formation. Urol Res 38(3):147–160.  https://doi.org/10.1007/soo240-010-0271-8 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Evan A, Worcester E, Coe F, Williams J Jr, Lingeman J (2015) Mechanisms of human kidney stone formation. Urolithiasis 43(Suppl 1):S19–S32.  https://doi.org/10.1007/s00240-014-0701-0 CrossRefGoogle Scholar
  5. 5.
    Randall A (1937) The origin and growth of renal calculi. Ann Surg 105(6):1009–1027CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Evan A, Lingeman J, Coe FL, Worcester E (2006) Randall’s plaque: pathogenesis and role in calcium oxalate nephrolithiasis. Kidney Int 69(8):1313–1318CrossRefPubMedGoogle Scholar
  7. 7.
    Evan AP, Coe FL, Lingeman JE, Shao Y, Sommer AJ, Bledsoe SB, Anderson JC, Worcester EM (2007) Mechanism of formation of human calcium oxalate renal stones on Randall’s Plaque. Anat Rec 290(10):1315–1323.  https://doi.org/10.1002/ar.20580 CrossRefGoogle Scholar
  8. 8.
    Evan AP (2010) Physiopathology and etiology of stone formation in the kidney and the urinary tract. Pediatric Nephrol 25:831–841.  https://doi.org/10.1007/s00467-009-1116-y CrossRefGoogle Scholar
  9. 9.
    Evan AP, Coe FL, Rittling SR, Bledsoe SM, 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(1):145–154CrossRefPubMedGoogle Scholar
  10. 10.
    Evan AP, Lingeman JE, Coe FL, Parks JH, Bledsoe SB, Shao YZ, Sommer 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 Investig 111(5):607–616CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Bushinsky DA (2003) Nephrolithiasis: site of the initial solid phase. J Clin Investig 111(5):602–605.  https://doi.org/10.1172/JCI18016 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Khan SR, Rodriguez DE, Gower LB, Monga M (2012) Association of Randall Plaque with collagen fibers and membrane vesicles. J Urol 187:1094–1100.  https://doi.org/10.1016/j.juro.2011.10.125 doiCrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Bagga HS, Chi T, Miller J, Stoller ML (2013) New insights into the pathogenesis of renal calculi. Urol Clin North Am 40(1):1–12CrossRefPubMedGoogle Scholar
  14. 14.
    Matlaga BR, Williams JC Jr, Kim SC, Kuo RL, Evan AP, Bledsoe SB, Coe FL, Worcester EM, Munch LC, Lingeman JE (2006) Endoscopic evidence of calculus attachment to Randall’s plaque. J Urol 175(5):1720–1724.  https://doi.org/10.1016/S0022-5347(05)01017-7 CrossRefPubMedGoogle Scholar
  15. 15.
    Sayer JA, Carr G, Simmons NL (2004) Nephrocalcinosis: molecular insights into calcium precipitation within the kidney. Clin Sci 106(6):549–561CrossRefPubMedGoogle Scholar
  16. 16.
    Khan SR (1997) Calcium phosphate/calcium oxalate crystal association in urinary stones: implications for heterogeneous nucleation of calcium oxalate. J Urol 157(1):376–383CrossRefPubMedGoogle Scholar
  17. 17.
    Bazin D, Daudon M (2012) Pathological calcifications and selected examples at the medicine-solid-state physics interface. J Phys D Appl Phys 45(38):383001CrossRefGoogle Scholar
  18. 18.
    Khan SR, Finlayson B, Hackett R (1984) Renal papillary changes in patient with calcium oxalate lithiasis. Urology 23(2):194–199CrossRefPubMedGoogle Scholar
  19. 19.
    Stoller ML, Meng MV, Abrahams HM, Kane JP (2004) The primary stone event: a new hypothesis involving a vascular etiology. J Urol 171(5):1920–1924CrossRefPubMedGoogle Scholar
  20. 20.
    Khan S (2006) Renal tubular damage/dysfunction: key to the formation of kidney stones. Urol Res 34(2):86–91.  https://doi.org/10.1007/s00240-005-0016-2 CrossRefPubMedGoogle Scholar
  21. 21.
    Coe FL, Evan AP, Lingeman JE, Worcester EM (2010) Plaque and deposits in nine human stone diseases. Urol Res.  https://doi.org/10.1007/s00240-010-0296-z CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Tiselius H-G (2011) A hypothesis of calcium stone formation: an interpretation of stone research during the past decades. Urol Res 39(4):231–243.  https://doi.org/10.1007/s00240-010-0349-3 doiCrossRefPubMedGoogle Scholar
  23. 23.
    Hug S, Grohe B, Jalkanen J, Chan B, Galarreta B, Vincent K, Lagugne-Labarthet F, Lajoie G, Goldberg HA, Karttunen M, Hunter GK (2012) Mechanism of inhibition of calcium oxalate crystal growth by an osteopontin phosphopeptide. Soft Matter 8(4):1226–1233.  https://doi.org/10.1039/C1SM06232H CrossRefGoogle Scholar
  24. 24.
    Stoller ML, Low RK, Shami GS, Mccormick VD, Kerschma RL (1996) High resolution radiography of cadaveric kidneys: unraveling the mystery of randall’s plaque formation. J Urol 156:1263–1266CrossRefPubMedGoogle Scholar
  25. 25.
    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.  https://doi.org/10.1007/s00240-010-0300-7 CrossRefPubMedGoogle Scholar
  26. 26.
    Canales BK, Anderson L, Higgins L, Slaton J, Roberts KP, Liu NT, Monga M (2008) Comprehensive proteomic analysis of human calcium oxalate monohydrate kidney stone matrix. J Endourol 22(6):1161–1167.  https://doi.org/10.1089/end.2007.0440 CrossRefPubMedGoogle Scholar
  27. 27.
    Gower LB, Amos FF, Khan SR (2010) Mineralogical signatures of stone formation mechanisms. Urol Res 38(4):281–292.  https://doi.org/10.1007/s00240-010-0288-z CrossRefPubMedGoogle Scholar
  28. 28.
    Khan SR, Atmani F, Glenton P, Hou ZC, Talham DR, Khurshid M (1996) Lipids and membranes in the organic matrix of urinary calcific crystals and stones. Calcif Tissue Int 59(5):357–365CrossRefPubMedGoogle Scholar
  29. 29.
    Sheng XX, Jung TS, Wesson JA, Ward MD (2005) Adhesion at calcium oxalate crystal surfaces and the effect of urinary constituents. Proc Natl Acad Sci USA 102(2):267–272.  https://doi.org/10.1073/pnas.0406835101 CrossRefPubMedGoogle Scholar
  30. 30.
    Christmas KG, Gower LB, Khan SR, El-Shall H (2002) Aggregation and dispersion characteristics of calcium oxalate monohydrate: effect of urinary species. J Colloid Interface Sci 256:168–174CrossRefPubMedGoogle Scholar
  31. 31.
    Khan SR, Kok DJ (2004) Modulators of urinary stone formation. Front Biosci 9:1450–1482CrossRefPubMedGoogle Scholar
  32. 32.
    Kolbach AM, Afzal O, Halligan B, Sorokina E, Kleinman JG, Wesson JA (2012) Relative deficiency of acidic isoforms of osteopontin from stone former urine. Urol Res 40(5):447–454.  https://doi.org/10.1007/s00240-012-0459-1 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Lan M, Lucy L, Andrew PE, Andre JS, John CL, Xue-Ru W (2007) Renal calcinosis and stone formation in mice lacking osteopontin, Tamm-Horsfall protein, or both. Am J Physiol Renal Physiol 293(6):F1935–F1943.  https://doi.org/10.1152/ajprenal.00383.2007 CrossRefGoogle Scholar
  34. 34.
    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(1):45–54CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    De Yoreo JJ, Gilbert PUPA., Sommerdijk NAJM., Penn RL, Whitelam S, Joester D, Zhang H, Rimer JD, Navrotsky A, Banfield JF, Wallace AF, Michel FM, Meldrum FC, Cölfen H, Dove PM (2015) Crystallization by particle attachment in synthetic, biogenic, and geologic environments. Science.  https://doi.org/10.1126/science.aaa6760 PubMedCrossRefGoogle Scholar
  36. 36.
    Karthika S, Radhakrishnan TK, Kalaichelvi P (2016) A review of classical and nonclassical nucleation theories. Cryst Growth Des 16(11):6663–6681.  https://doi.org/10.1021/acs.cgd.6b00794 CrossRefGoogle Scholar
  37. 37.
    Lee J, Yang J, Kwon SG, Hyeon T (2016) Nonclassical nucleation and growth of inorganic nanoparticles. Nature Rev Mater.  https://doi.org/10.1038/natrevmats.2016.34 CrossRefGoogle Scholar
  38. 38.
    Rodriguez-Navarro C, Ruiz-Agudo E, Harris J, Wolf SE (2016) Nonclassical crystallization in vivo et in vitro (II): nanogranular features in biomimetic minerals disclose a general colloid-mediated crystal growth mechanism. J Struct Biol.  https://doi.org/10.1016/j.jsb.2016.09.005 CrossRefPubMedGoogle Scholar
  39. 39.
    Wolf SE, Gower LB (2017) Challenges and perspectives of the polymer-induced liquid-precursor process: the pathway from liquid-condensed mineral precursors to mesocrystalline products. In: Driessche AESV, Kellermeier M, Benning LG, Gebauer D (eds) New perspectives on mineral nucleation and growth: from solution precursors to solid materials. Springer International Publishing, Switzerland, pp 43–75.  https://doi.org/10.1007/978-3-319-45669-0$43 CrossRefGoogle Scholar
  40. 40.
    Amos FF, Dai L, Kumar R, Khan SR, Gower LB (2009) Mechanism of formation of concentrically laminated spherules: implication to Randall’s plaque and stone formation. Urol Res 37(1):11–17.  https://doi.org/10.1007/s00240-008-0169-x CrossRefPubMedGoogle Scholar
  41. 41.
    Olszta MJ, Cheng X, Jee SS, Kumar R, Kim Y-Y, Kaufman MJ, Douglas EP, Gower LB (2007) Bone structure and formation: a new perspective. Mater Sci Eng Rep 58(3–5):77–116.  https://doi.org/10.1016/j.mser.2007.05.001 CrossRefGoogle Scholar
  42. 42.
    Gower LB (2008) Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization. Chem Rev 108(11):4551–4627.  https://doi.org/10.1021/cr800443h CrossRefPubMedGoogle Scholar
  43. 43.
    Amos FF, Olszta MJ, Khan SR, Gower LB (2006) Relevance of a polymer-induced liquid-precursor (PILP) mineralization process to normal and pathological biomineralization. In: Königsberger E, Königsberger L (eds) Biomineralization- medical aspects of solubility, vol 4. Wiley, West Sussex, pp 125–217CrossRefGoogle Scholar
  44. 44.
    Jee S-S, Thula TT, Gower LB (2010) Development of bone-like composites via the polymer-induced liquid-precursor (PILP) process. Part 1: influence of polymer molecular weight. Acta Biomater 6(9):3676–3686.  https://doi.org/10.1016/j.actbio.2010.03.036 CrossRefPubMedGoogle Scholar
  45. 45.
    Gower LB, Odom DJ (2000) Deposition of calcium carbonate films by a polymer-induced liquid-precursor (PILP) process. J Crystal Growth 210(4):719–734CrossRefGoogle Scholar
  46. 46.
    Wolf SLP, Caballero L, Melo F, Cölfen H (2016) Gel-like calcium carbonate precursors observed by in-situ AFM. Langmuir.  https://doi.org/10.1021/acs.langmuir.6b03974 CrossRefPubMedGoogle Scholar
  47. 47.
    Bewernitz MA, Gebauer D, Long J, Cölfen H, Gower LB (2012) A metastable liquid precursor phase of calcium carbonate and its interactions with polyaspartate. Faraday Discuss 159:291–312.  https://doi.org/10.1039/c2fd20080e CrossRefGoogle Scholar
  48. 48.
    Olszta MJ, Odom DJ, Douglas EP, Gower LB (2003) A new paradigm for biomineral formation: Mineralization via an amorphous liquid-phase precursor. Connect Tissue Res 44:326–334.  https://doi.org/10.1080/03008200390181852 CrossRefPubMedGoogle Scholar
  49. 49.
    Kim Y-Y, Hetherington NBJ, Noel EH, Kroeger R, Charnock JM, Christenson HK, Meldrum FC (2011) Capillarity creates single-crystal calcite nanowires from amorphous calcium carbonate. Angew Chem-Int Edit 50(52):12572–12577.  https://doi.org/10.1002/anie.201104407 CrossRefGoogle Scholar
  50. 50.
    Kim Y-Y, Douglas EP, Gower LB (2007) Patterning inorganic (CaCO3) thin films via a polymer-induced liquid-precursor process. Langmuir 23(9):4862–4870.  https://doi.org/10.1021/la0619751 CrossRefPubMedGoogle Scholar
  51. 51.
    Kim YY, Kulak AN, Li YT, Batten T, Kuball M, Armes SP, Meldrum FC (2009) Substrate-directed formation of calcium carbonate fibres. J Mater Chem 19(3):387–398.  https://doi.org/10.1039/b813101e CrossRefGoogle Scholar
  52. 52.
    Niu L-n, Jee SE, Jiao K, Tonggu L, Li M, Wang L, Yang Y-d, Bian J-h, Breschi L, Jang SS, Chen J-h, Pashley DH, Tay FR (2017) Collagen intrafibrillar mineralization as a result of the balance between osmotic equilibrium and electroneutrality. Nat Mater 16(3):370–378.  https://doi.org/10.1038/nmat4789.CrossRefPubMedGoogle Scholar
  53. 53.
    Nudelman F, Pieterse K, George A, Bomans PHH, Friedrich H, Brylka LJ, Hilbers PAJ, de With G, Sommerdijk NAJM (2010) The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat Mater 9(12):1004–1009.  https://doi.org/10.1038/NMAT2875 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Rodriguez DE, Thula-Mata T, Toro EJ, Yeh Y-W, Holt C, Holliday LS, Gower LB (2014) Multifunctional role of osteopontin in directing intrafibrillar mineralization of collagen and activation of osteoclasts. Acta Biomater 10(1):494–507.  https://doi.org/10.1016/j.actbio.2013.10.010 CrossRefPubMedGoogle Scholar
  55. 55.
    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(1):139–147.  https://doi.org/10.1097/01.asn.0000040593.93815.9d CrossRefPubMedGoogle Scholar
  56. 56.
    Kleinman JG, Beshensky A, Worcester EM, Brown D (1995) Expression of osteopontin, a urinary inhibitor of stone mineral crystal growth, in rat kidney. Kidney Int 47(6):1585–1596.  https://doi.org/10.1038/ki.1995.222 CrossRefPubMedGoogle Scholar
  57. 57.
    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. Proc Natl Acad Sci USA 89(1):426–430CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Worcester EM, Beshensky AM (1995) Osteopontin inhibits nucleation of calcium oxalate crystals. Ann NY Acad Sci 760:375–377CrossRefPubMedGoogle Scholar
  59. 59.
    Chidambaram A, Rodriguez D, Khan S, Gower L (2015) Biomimetic Randall’s plaque as an in vitro model system for studying the role of acidic biopolymers in idiopathic stone formation. Urolithiasis 43(1):77–92. https://doi.org/10.1007/s00240-014-0704-x. PMC http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4285617
  60. 60.
    Ross EA, Williams MJ, Hamazaki T, Terada N, Clapp WL, Adin C, Ellison GW, Jorgensen M, Batich CD (2009) Embryonic stem cells proliferate and differentiate when seeded into kidney Scaffolds. J Am Soc Nephrol 20:2338–2347.  https://doi.org/10.1681/ASN.2008111196 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Sørensen ES, Ostersen S, Chatterton D, Holst HH, Albertsen K (2007) Process for isolation of osteopontin from milk. Google PatentsGoogle Scholar
  62. 62.
    Ross R (1973) The elastic fiber—a review. J Histochem Cytochem 21(3):199–208CrossRefPubMedGoogle Scholar
  63. 63.
    Badylak SF, Freytes DO, Gilbert TW (2009) Extracellular matrix as a biological scaffold material: structure and function. Acta Biomater 5(1):1–13.  https://doi.org/10.1016/j.actbio.2008.09.013 CrossRefPubMedGoogle Scholar
  64. 64.
    Saxena NS (2017) Optimization of the polymer-induced liquid-precursor process for dentin remineralization. Doctoral, University of Florida, Gainesville, FLGoogle Scholar
  65. 65.
    Saxena N, Mizels J, Rodriguez VGD, Wingender ALB, Gower L (2018) Comparative study of osteopontin versus polyaspartate for collagen mineralization. Acta Biomaterialia (in preparation)Google Scholar
  66. 66.
    Scatena M, Liaw L, Giachelli CM (2007) Osteopontin. A multifunctional molecule regulating chronic inflammation and vascular disease. Arterioscler Thromb Vasc Biol 27(11):2302–2309.  https://doi.org/10.1161/atvbaha.107.144824 CrossRefPubMedGoogle Scholar
  67. 67.
    Kaartinen MT, Pirhonen A, Linnala-Kankkunen A, Mäenpää PH (1997) Transglutaminase-catalyzed cross-linking of osteopontin is inhibited by osteocalcin. J Biol Chem 272(36):22736–22741CrossRefPubMedGoogle Scholar
  68. 68.
    Martin SM, Schwartz JL, Giachelli CM, Ratner BD (2004) Enhancing the biological activity of immobilized osteopontin using a type-1 collagen affinity coating. J Biomed Mater Res Part A 70A(1):10–19.  https://doi.org/10.1002/jbm.a.30052 CrossRefGoogle Scholar
  69. 69.
    Thula TT, Svedlund F, Rodriguez DE, Podschun J, Pendi L, Gower LB (2011) Mimicking the nanostructure of bone: comparison of polymeric process-directing agents. Polymers 3(1):10–35.  https://doi.org/10.3390/polym3010010 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Dai L, Cheng X, Gower LB (2008) Transition bars during transformation of an amorphous calcium carbonate precursor. Chem Mat 20(22):6917–6928.  https://doi.org/10.1021/cm800760p CrossRefGoogle Scholar
  71. 71.
    McKee MD, Nancl A, Khan SR (1995) Ultrastructural immunodetection of osteopontin and osteocalcin as major matrix components of renal calculi. J Bone Miner Res 10(12):1913–1929.  https://doi.org/10.1002/jbmr.5650101211 CrossRefPubMedGoogle Scholar
  72. 72.
    Hunter GK, O’Young J, Grohe B, Karttunen M, Goldberg HA (2010) The flexible polyelectrolyte hypothesis of protein-biomineral interaction. Langmuir 26(24):18639–18646.  https://doi.org/10.1021/la100401r CrossRefPubMedGoogle Scholar
  73. 73.
    Ryall RL (2008) The future of stone research: rummagings in the attic, Randall’s plaque, nanobacteria, and lessons from phylogeny. Urol Res.  https://doi.org/10.1007/s00240-007-0131-3 CrossRefPubMedGoogle Scholar
  74. 74.
    Golub EE (2011) Biomineralization and matrix vesicles in biology and pathology. Semin Immunopathol 33(5):409–417.  https://doi.org/10.1007/s00281-010-0230-z CrossRefPubMedGoogle Scholar
  75. 75.
    Deshpande AS, Beniash E (2008) Bioinspired synthesis of mineralized collagen fibrils. Cryst Growth Des 8(8):3084–3090.  https://doi.org/10.1021/cg800252f CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Price PA, Toroian D, Lim JE (2009) Mineralization by Inhibitor exclusion—the calcification of collagen with fetuin. J Biol Chem 284(25):17092–17101.  https://doi.org/10.1074/jbc.M109.007013 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Tang R, Wang L, Nancollas GH (2004) Size-effects in the dissolution of hydroxyapatite: an understanding of biological demineralization. J Mater Chem 14:2341–2346.  https://doi.org/10.1039/b401097c CrossRefGoogle Scholar
  78. 78.
    Kusmartsev S, Dominguez-Gutierrez PR, Canales BK, Bird VG, Vieweg J, Khan SR (2016) Calcium oxalate stone fragment and crystal phagocytosis by human macrophages. J Urol 195(4, part 1):1143–1151.  https://doi.org/10.1016/j.juro.2015.11.048 CrossRefPubMedGoogle Scholar
  79. 79.
    Haggitt RC, Pitcock JA (1971) Renal medullary calcifications: a light and electron microscopic study. J Urol 106(3):342–347CrossRefPubMedGoogle Scholar
  80. 80.
    Low RK, Stoller ML (1997) Endoscopic mapping of renal papillae for Randall’s plaques in patients with urinary stone disease. J Urol 158:2062–2064CrossRefPubMedGoogle Scholar
  81. 81.
    Taguchi T, Ikoma T, Tanaka J (2002) An improved method to prepare hyaluronic acid and type II collagen composite matrices. J Biomed Mater Res 61(2):330–336CrossRefPubMedGoogle Scholar
  82. 82.
    Okada A, Yasui T, Fujii Y, Niimi K, Hamamoto S, Hirose M, Kojima Y, Itoh Y, Tozawa K, Hayashi Y, Kohri K (2010) Renal macrophage migration and crystal phagocytosis via inflammatory-related gene expression during kidney stone formation and elimination in mice: detection by association analysis of stone-related gene expression and microstructural observation. J Bone Miner Res 25(12):2701–2711.  https://doi.org/10.1002/jbmr.158 CrossRefPubMedGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Materials Science and EngineeringUniversity of FloridaGainesvilleUSA
  2. 2.Department of Pathology, College of MedicineUniversity of FloridaGainesvilleUSA

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