Comparison of the specific incorporation of intracrystalline proteins into urinary calcium oxalate monohydrate and dihydrate crystals

Journal of Proteome Research

Volumn 9, Issue 9, 2010, Pages 4745-4757

  Thurgood, Lauren A ^a   Wang, Tingting ^a   Chataway, Timothy K ^a   Ryall, Rosemary L ^a  

^a FLINDERS UNIVERSITY   (Australia)

Author keywords

calcium oxalate dihydrate crystals; calcium oxalate monohydrate crystals; kidney stone; LC MS MS; proteomics; urolithiasis

Indexed keywords

ALPHA 1 ANTITRYPSIN; CALGRANULIN B; DERMCIDIN; DESMOGLEIN 1; FATTY ACID BINDING PROTEIN; FETUIN; GAMMA GLUTAMYL HYDROLASE; HISTONE H4; HORNERIN; HUMAN SERUM ALBUMIN; IFAPSORIASIN; IMMUNOGLOBULIN KAPPA CHAIN; INTRACYSTALLINE PROTEIN; KERATIN; KININOGEN; LIPOCORTIN 1; LIPOCORTIN 2; OSTEOPONTIN; PROTHROMBIN FRAGMENT 1; RIBOSOME PROTEIN; SERINE PROTEINASE INHIBITOR; STEFIN A; SYNDECAN 4; TAMM HORSFALL GLYCOPROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; VASORIN; WEDDELLITE; WHEWELLITE;

ARTICLE; CRYSTAL STRUCTURE; DEMINERALIZATION; FEMALE; FOURIER TRANSFORMATION; HUMAN; LIQUID CHROMATOGRAPHY; MALE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEOMICS; TANDEM MASS SPECTROMETRY; URINALYSIS;

CALCIUM OXALATE; CHROMATOGRAPHY, LIQUID; CRYSTALLIZATION; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; HUMANS; KIDNEY CALCULI; MALE; PROTEOME; PROTEOMICS; TANDEM MASS SPECTROMETRY;

EID: 77956326621     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr100467z     Document Type: Article

References (86)

1. Thorne, I.; Resnick, M. I. Urinary macromolecules and renal lithiasis World J. Urol. 1983, 1, 138-145
2. Boyce, W. H.; Garvey, F. K. The amount and nature of the organic matrix in urinary calculi: a review J. Urol. 1956, 76, 213-227
3. Boyce, W. H. Organic matrix of human urinary concretions Am. J. Med. 1968, 45, 673-683
4. Gower, L. B. Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization Chem. Rev. 2008, 108, 4551-4627
5. Jahnen-Dechent, W.; Schaöfer, C.; Ketteler, M.; McKee, M. D. Mineral chaperones: a role for fetuin-A and osteopontin in the inhibition and regression of pathologic calcification J. Mol. Med. 2008, 86, 379-389
6. Ryall, R. L. Macromolecules and urolithiasis: Parallels and paradoxes Nephron 2004, 98, 37-42
7. Khan, S. R.; Kok, D. J. Modulators of urinary stone formation Front. Biosci. 2004, 9, 1450-1482
8. Chen, W. C.; Lai, C. C.; Tsai, Y. H.; Lin, W. Y.; Tsai, F. J. Mass spectroscopic characteristics of low molecular weight proteins extracted from calcium oxalate stones: preliminary study J. Clin. Lab. Anal. 2008, 22, 77-85
9. Canales, B. K.; Anderson, L.; Higgins, L.; Slaton, J.; Roberts, K. P.; Liu, N.; Monga, M. Second Prize: comprehensive proteomic analysis of human calcium oxalate monohydrate kidney stone matrix J. Endourol. 2008, 22, 1161-1167
10. Merchant, M. L.; Cummins, T. D.; Wilkey, D. W.; Salyer, S. A.; Powell, D. W.; Klein, J. B.; Lederer, E. D. Proteomic analysis of renal calculi indicates an important role for inflammatory processes in calcium stone formation Am. J. Physiol. Renal Physiol. 2008, 295, F1254-F1258
11. Adachi, J.; Kumar, C.; Zhang, Y.; Olsen, J. V.; Mann, M. The human urinary proteome contains more than 1500 proteins, including a large proportion of membrane proteins Genome Biol. 2006, 7, R80.2-R80.16
12. Morse, R. M.; Resnick, M. I. A new approach to the study of urinary macromolecules as a participant in calcium oxalate crystallization J. Urol. 1988, 139, 869-873
13. Doyle, I. R.; Ryall, R. L.; Marshall, V. R. Inclusion of proteins into calcium oxalate crystals precipitated from human urine: a highly selective phenomenon Clin. Chem. 1991, 37, 1589-1594
14. Kumar, V.; Farell, G.; Deganello, S.; Lieske, J. C. Annexin II is present on renal epithelial cells and binds calcium oxalate monohydrate crystals J. Am. Soc. Nephrol. 2003, 14, 289-297
15. Grover, P. K.; Thurgood, L. A.; Ryall, R. L. Effect of urine fractionation on attachment of calcium oxalate crystals to renal epithelial cells: implications for studying renal calculogenesis Am. J. Physiol. Renal Physiol. 2007, 292, F1396-1403
16. Grover, P. K.; Thurgood, L. A.; Wang, T.; Ryall, R. L. 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. 2010, 105, 708-715
17. Ryall, R. L.; Fleming, D. E.; Grover, P. K.; Chauvet, M. C.; Dean, C. J.; Marshall, V. R. The hole truth: intracrystalline proteins and calcium oxalate kidney stones Mol. Urol. 2000, 4, 391-402
18. Ryall, R. L.; Fleming, D. E.; Doyle, I. R.; Evans, N. A.; Dean, C. J.; Marshall, V. R. Intracrystalline proteins and the hidden ultrastructure of calcium oxalate urinary crystals: implications for kidney stone formation J. Struct. Biol. 2001, 134, 5-14
19. Fleming, D. E.; Van Riessen, A.; Chauvet, M. C.; Grover, P. K.; Hunter, B.; van Bronswijk, W.; Ryall, R. L. Intracrystalline proteins and urolithiasis: a synchrotron X-ray diffraction study of calcium oxalate monohydrate J. Bone Miner. Res. 2003, 18, 1282-1291
20. Chauvet, M. C.; Ryall, R. L. Intracrystalline proteins and calcium oxalate crystal degradation in MDCK II cells J. Struct. Biol. 2005, 151, 12-17
21. Stapleton, A. M. F.; Ryall, R. L. Blood coagulation proteins and urolithiasis are linked: Crystal matrix protein is the F1 activation peptide of human prothrombin Br. J. Urol. 1995, 7, 712-719
22. Atmani, F.; Khan, S. R. Quantification of proteins extracted from calcium oxalate and calcium phosphate crystals induced in vitro in the urine of healthy controls and stone-forming patients Urol. Int. 2002, 68, 54-59
23. Nishio, S.; Hatanaka, M.; Takeda, H.; Iseda, T.; Iwata, H.; Yokoyama, M. Analysis of urinary concentrations of calcium phosphate associated proteins; alpha2-HS-glycoprotein, prothrombin F1 and osteopontin J. Am. Nephrol. Soc. 1999, 10, S394-S396
24. Dawson, C. J.; Grover, P. K.; Ryall, R. L. Inter-α-trypsin inhibitor in urine and calcium oxalate urinary crystals Br. J. Urol. 1998, 81, 20-26
25. Atmani, F.; Glenton, P. A.; Khan, S. R. Identification of proteins extracted from calcium oxalate and calcium phosphate crystals induced in the urine of healthy and stone forming subjects Urol. Res. 1998, 26, 201-207
26. Ryall, R. L.; Chauvet, M. C.; Grover, P. K. Intracrystalline proteins and urolithiasis: a comparison of the protein content and ultrastructure of urinary calcium oxalate monohydrate and dihydrate crystals Brit. J. Urol. 2005, 96, 654-663
27. Morse, R. M.; Resnick, M. I. A study of the incorporation of urinary macromolecules onto crystals of different mineral compositions J. Urol. 1989, 141, 641-644
28. Mandel, N. S.; Mandel, G. S. Urinary tract stone incidence in the US veteran population II. Geographical analysis of variations in composition J. Urol. 1989, 142, 1516-1521
29. Dyer, R.; Nordin, B. E. Urinary crystals and their relation to stone formation Nature 1967, 215, 751-752
30. Elliot, J. S.; Rabinowitz, I. N. Calcium oxalate crystalluria: crystal size in urine J. Urol. 1980, 123, 324-327
31. Wesson, J. A.; Worcester, E. Formation of hydrated calcium oxalates in the presence of poly-L-aspartic acid Scan. Microsc. Int. 1996, 10, 415-424
32. Havanapan, P. O.; Thongboonkerd, V. Are protease inhibitors required for gel-based proteomics of kidney and urine J. Proteome Res. 2009, 8, 3109-3117
33. Ryall, R. L.; Hibberd, C. M.; Marshall, V. R. A method for studying inhibitory activity in whole urine Urol. Res. 1985, 13, 285-289
34. Ryall, R. L.; Grover, P. K.; Thurgood, L. A.; Chauvet, M. C.; Fleming, D. E.; van Bronswijk, W. 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. 2007, 35, 1-14
35. Buchholz, N.-P.; Kim, D. S.; Grover, P. K.; Dawson, C. J.; Ryall, R. L. The effect of warfarin therapy on the charge properties of urinary prothrombin fragment 1 and crystallization of calcium oxalate in undiluted human urine J. Bone Min. Res. 1999, 14, 1003-1012
36. Jin, L. T.; Hwang, S. Y.; Yoo, G. S.; Choi, J. K. A mass spectrometry compatible silver staining method for protein incorporating a new silver sensitizer in sodium dodecyl sulfate-polyacrylamide electrophoresis gels Proteomics 2006, 6, 2334-2337
37. Mandel, I.; Mandel, N. Structure and Compositional Analysis of Kidney Stones. In Urinary Stone Disease: The Practical Guide to Surgical Management; Stoller, M. L.; Meng, M. V., Eds.; Spinger: New York, 2007.
38. Shevchenko, A.; Wilm, M.; Vorm, O.; Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels Anal. Chem. 1996, 68, 850-858
39. Jensen, O. N.; Podtelejnikov, A. V.; Mann, M. Identification of the components of simple protein mixtures by high-accuracy peptide mass mapping and database searching Anal. Chem. 1997, 69, 4741-4750
40. Ding, Q.; Xiao, L.; Xiong, S.; Jia, Y.; Que, H.; Guo, Y.; Liu, S. Unmatched masses in peptide mass fingerprints caused by cross-contamination: an updated statistical result Proteomics 2003, 3, 1313-1317
41. Jones, W. T.; Resnick, M. I. The characterization of soluble matrix proteins in selected human renal calculi using two-dimensional polyacrylamide gel electrophoresis J. Urol. 1990, 144, 1010-1014
42. Thongboonkerd, V.; Chutipongtanate, S; Kanlaya, R. Systematic evaluation of sample preparation methods for gel-based human urinary proteomics: quantity, quality, and variability J. Proteome Res. 2005, 5, 183-191
43. Eichner, R.; Kahn, M. Differential extraction of keratin subunits and filaments from normal human epidermis J. Cell Biol. 1990, 110, 1149-1158
44. Plowman, J. E. The proteomics of keratin proteins J. Chromatogr., B: Anal. Technol. Biomed Life Sci. 2007, 849, 181-189
45. Fox, K.; Castanha, E.; Fox, A.; Feigley, C.; Salzberg, D. Human K10 epithelial keratin is the most abundant protein in airborne dust of both occupied and unoccupied school rooms J. Environ. Model. 2007, 10, 55-59
46. Trisillis, A. L.; Regec, A. L.; Trump, B. F. Isolation, culture and characterization of human renal tubular cells J. Urol. 1985, 133, 324-329
47. Achtstaötter, T.; Moll, R.; Moore, B.; Franke, W. W. Cytokeratin polypeptide patterns of different epithelia of the human male urogenital tract: immunofluoresence and gel electrophoretic studies J. Histochem. Cytochem. 1985, 33, 415-426
48. Schaafsma, H. E.; Ramaekers, F. C. S.; van Muijen, G. N. P.; Ooms, E. C. M.; Ruiter, D. J. Distribution of cytokeratin polypeptides in epithelia of the adult human urinary tract Histochemistry 1989, 91, 151-159
49. Prescott, L. F. The normal urinary excretion rates of renal tubular cells, leucocytes and red blood cells Clin. Sci. 1966, 31, 425-435
50. Addadi, L.; Weiner, S. Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization Proc. Natl. Acad. Sci. U.S.A. 1985, 82, 4110-4114
51. Lieske, J. C.; Swift, H.; Martin, T.; Patterson, B.; Toback, F. G. Renal epithelial cells rapidly bind and internalize calcium oxalate monohydrate crystals Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 6987-6991
52. Thongboonkerd, V.; Semangoen, T.; Sinchaikul, S.; Chen, S. T. Proteomic analysis of calcium oxalate monohydrate crystal-induced cytotoxicity in distal renal tubular cells J. Proteome Res. 2008, 7, 4689-4700
53. Semangoen, T.; Sinchaikul, S.; Chen, S. T.; Thongboonkerd, V. Altered proteins in MDCK renal tubular cells in response to calcium oxalate dihydrate crystal adhesion: a proteomics approach J. Proteome Res. 2008, 7, 2889-2896
54. Bautista, D. S.; Densteldt, J.; Chambers, A. F.; Harris, J. F. Low molecular weight variants of osteopontin generated by serine proteases in urine of patients with kidney stones J. Cell Biochem. 1996, 61, 402-409
55. Theodorescu, D.; Mischak, H. Mass spectrometry based proteomics in urine biomarker discovery World J. Urol. 2007, 25, 435-443
56. Kasemo, B.; Lausmaa, J. Material-tissue interfaces: the role of surface properties and processes Env. Health. Persp. 1994, 102 (5) 41-45
57. Wheeler, A. P.; Rusenko, K. W.; George, J. W.; Sikes, C. S. Evaluation of calcium binding by molluscan shell organic matrix and its relevance to biomineralization Comp. Biochem. Physiol. 1987, 87B, 953-960
58. Pereira-Mouriès, L.; Almeida, M. J.; Ribeiro, C.; Peduzzi, J.; Barthélemy, M.; Milet, C.; Lopez, E. Soluble silk-like organic matrix in the nacreous layer of the bivalve Pinctada maxima Eur. J. Biochem. 2002, 269, 4994-5003
59. Aizenberg, J.; Hanson, J.; Ilan, M.; Leiserowitz, L.; Koetzle, T. F.; Addadi, L.; Weiner, S. Morphogenesis of calcitic sponge spicules: a role for specialized proteins interacting with growing crystals FASEB J. 1995, 9, 262-268
60. Mann, S.; Archibald, D. D.; Didymus, J. M.; Douglas, T.; Heywood, B. R.; Meldrum, F. C.; Reeves, N. J. Crystallization at inorganic-organic interfaces: biominerals and biomimetic synthesis Science 1993, 261, 1286-1292
61. Moradian-Oldak, J.; Frolow, F.; Addadi, L.; Weiner, S. Interactions between acidic matrix macromolecules and calcium phosphate ester crystals: relevance to carbonate apatite formation in biomineralization Proc. R. Soc. Lond., B 1992, 247, 47-55
62. Albeck, S.; Addadi, L.; Weiner, S. Regulation of calcite crystal morphology by intracrystalline acidic proteins and glycoproteins Conn. Tissue Res. 1996, 35, 365-370
63. Walton, R. C.; Kavanagh, J. P.; Heywood, B. R.; Rao, P. N. The association of different urinary proteins with calcium oxalate hydromorphs. Evidence for non-specific interactions Biochim. Biophys. Acta 2005, 1723, 175-183
64. Wang, H. C.; Kurimoto, M.; Kahr, B.; Chmielewski, J. α-Lactose monohydrate single crystals as hosts for matrix isolation of guest biopolymers Bioorg. Med. Chem. 2001, 9, 2279-2283
65. Heywood, B. R. Biomineralization: New directions in crystal science Microsc. Res. Tech. 1994, 27, 376-388
66. Hanein, D.; Sabanay, H.; Addadi, L.; Geiger, B. Selective interaction of cells with crystal surfaces. Implications for the mechanism of cell adhesion J. Cell Sci. 1993, 104, 275-288
67. Mann, S. The chemistry of form Angew. Chem., Int. Ed. 2000, 39, 3392-3406
68. Aizenberg, J.; Hanson, J.; Koetzle, T. F.; Weiner, S.; Addadi, L. Control of macromolecule distribution within synthetic and biogenic single calcite crystals J. Am. Chem. Soc. 1997, 119, 881-886
69. Clark, R. H.; Campbell, A. A.; Klumb, L. A.; Long, C. J.; Staytons, P. S. Protein electrostatic surface distribution can determine whether calcium oxalate crystal growth is promoted or inhibited Calcif. Tissue Int. 1999, 64, 516-521
70. De Yoreo, J. J.; Dove, P. M. Shaping crystals with biomolecules Science 2004, 306, 1301-1302
71. Wiessner, J. H.; Hung, L. Y.; Mandel, N. S. Crystal attachment to injured renal collecting duct cells: Influence of urine proteins and pH Kidney Int. 2003, 63, 1313-1320
72. Lepage, L.; Tawashi, R. Growth and characterization of calcium oxalate dihydrate crystals (weddellite) J. Pharm. Sci. 1982, 71, 1059-1062
73. Wiessner, J. H.; Mandel, G. S.; Mandel, N. S. Membrane interactions with calcium oxalate crystals: variation in hemolytic potentials with crystal morphology J. Urol. 1986, 135, 835-839
74. Wilt, F. H. Developmental biology meets materials science: Morphogenesis of biomineralized structures Dev. Biol. 2005, 280, 15-25
75. Thurgood, L. A.; Cook, A. F.; Sørensen, E. S.; Ryall, R. L. Face-specific incorporation of osteopontin unto urinary and inorganic calcium oxalate monohydrate and dihydrate crystals. Urol. Res. 2010, in press.
76. Qiu, S. R.; Wierzbicki, A.; Orme, C. A.; Cody, A. M.; Hoyer, J. R.; Nancollas, G. H.; Zepeda, A.; De Yoreo, J. J. Molecular modulation of calcium oxalate crystallization by osteopontin and citrate Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 1811-1815
77. Hoyer, J. R.; Otvos, L., Jr.; Urge, L. Osteopontin in urinary stone formation Ann. N.Y. Acad. Sci. 1995, 760, 257-265
78. Kleinman, J. G.; Wesson, J. A.; Hughes, J. Osteopontin and calcium stone formation Nephron Physiol. 2004, 98, 43-47
79. Grover, P. K.; Ryall, R. L. Effect of prothrombin and its activation fragments on calcium oxalate crystal growth and aggregation in undiluted human urine in vitro: relationship between protein structure and inhibitory activity Clin. Sci. 2002, 102, 425-434
80. Pillay, S. N.; Asplin, J. R.; Coe, F. L. Evidence that calgranulin is produced by kidney cells and is an inhibitor of calcium oxalate crystallization Am. J. Physiol. Renal Physiol. 1998, 275, F255-261
81. Médétognon-Benissan, J.; Tardivel, S.; Hennequin, C.; Daudon, M.; Druöeke, T.; Lacour, B. Inhibitory effect of bikunin on calcium oxalate crystallization in vitro and urinary bikunin decrease in renal stone formers Urol. Res. 1999, 27, 69-75
82. Tardivel, S.; Médétognon, J.; Randoux, C.; Kébédé, M.; Druöeke, T.; Daudon, M.; Hennequin, C.; Lacour, B. Alpha-1-microglobulin: inhibitory effect on calcium oxalate crystallization in vitro and decreased urinary concentration in calcium oxalate stone formers Urol. Res. 1999, 27, 243-249
83. Dean, C.; Kanellos, J.; Pham, H.; Gomes, M.; Oates, A.; Grover, P. K.; Ryall, R. L. Effects of inter-alpha-inhibitor and several of its derivatives on calcium oxalate crystallization in vitro Clin. Sci. 2000, 98, 471-480
84. Matsuo, M. Increased expression of heparan sulfate proteoglycan on the cultured renal epithelial cells during oxalate exposure Kurume Med. J. 2008, 55, 19-28
85. Worcester, E. M.; Nakagawa, Y.; Wabner, C. L.; Coe, F. L. Crystal adsorption and growth slowing by nephrocalcin, albumin and Tamm-Horsfall protein Am. J. Physiol. Renal Physiol. 1988, 255, F1199-1205
86. Grover, P. K.; Moritz, R. L.; Simpson, R. J.; Ryall, R. L. Inhibition of growth and aggregation of calcium oxalate crystals in vitro - a comparison of four human proteins FEBS 1998, 253, 637-644