Vascular calcification and stone disease: A new look towards the mechanism

Journal of Cardiovascular Development and Disease

Volumn 2, Issue 3, 2015, Pages 141-164

  Yiu, Allen J ^a   Callaghan, Daniel ^a,b   Sultana, Razia ^a   Bandyopadhyay, Bidhan C ^a,b,c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Calcification; Calcium phosphate; Calculi; Ectopic; Kidney; Ossification; Physiologic

Indexed keywords

EID: 84993549322     PISSN: None     EISSN: 23083425     Source Type: Journal    
DOI: 10.3390/jcdd2030141     Document Type: Review

References (152)

1. Metheny, N.M. Fluid and Electrolyte Balance: Nursing Considerations, 5th ed.; Jones & Bartlett Learning: St. Louis, MO, USA, 2010.
2. Clapham, D.E. Calcium signaling. Cell. 2007, 131, 1047–1058.
3. Hopkins, C.R.; Walker, A.M. Calcium as a second messenger in the stimulation of luteinizing hormone secretion. Mol. Cell. Endocrinol. 1978, 12,189–208.
4. Worcester, E.M.; Coe, F.L. Nephrolithiasis. Prim. Care 2008, 35, 369–391.
5. Moe, S.M.; Chen, N.X. Mechanisms of vascular calcification in chronic kidney disease. J. Am. Soc. Nephrol. 2008, 1, 213–216.
6. Schepers, M.S.J.; van Ballegooijen, E.S.; Bangma, C.H.; Verkoelen, C.F. Crystals cause acute necrotic cell death in renal proximal tubule cells, but not in collecting tubule cells. Kidney Int. 2005, 68, 1543–1553.
7. Coe, F.L; Evan, A.P.; Worcester, E.M.; Lingeman, J.E. Three pathways for human kidney stone formation. Urol. Res. 2010, 38, 147–160.
8. Khan, S.R.; Canales, B.K. Unified theory on the pathogenesis of Randall’s plaques and plugs. Urolithiasis 2015, 43, S109–S123.
9. Canales, B.K.; Anderson, L.; Higgins, L; Ensrud-Bowlin, K.; Roberts, K.P.; Wu, B.; Kim, I.W.; Monga, M. Proteome of Human Calcium Kidney Stones. Urology 2010, 76, e13–e20.
10. Parks, J.H.; Coe, F.L.; Evan, A.P.; Worcester, E.M. Urine pH in renal calcium stone formers who do and do not increase stone phosphate content with time. Nephrol. Dial. Transpl. 2009, 24, 130–136.
11. Callaghan, D.; Bandyopadhyay, B.C. Calcium Phosphate Kidney Stone: Problems and Perspectives. Anat. Physiol. 2012, 2, e118. doi:10.4172/2161-0940.1000e118.
12. Villa-Bellosta, R.; Millan, A.; Sorribas, V. Role of calcium-phosphate deposition in vascular smooth muscle cell calcification. Am. J. Physiol. Cell. Physiol. 2011, 300, C210–C220.
13. Tiselius, H.G. The role of calcium phosphate in the development of Randall’s plaques. Urolithiasis 2013, 41, 369–377.
14. Kumar, V.; Farell, G.; Yu, S.; Harrington, S.; Fitzpatrick, L.; Rzewuska, E.; Miller, V.M.; Lieske, J.C. Cell biology of pathologic renal calcification: contribution of crystal transcytosis, cell-mediated calcification, and nanoparticles. J. Investig. Med. 2006, 54, 412–424.
15. Sage, A.P.; Lu, J, Tintut, Y., Demer, L.L. Hyperphosphatemia-induced nanocrystals upregulate the expression of bone morphogenetic protein-2 and osteopontin genes in mouse smooth muscle cells in vitro. Kidney Int. 2011, 79, 414–422.
16. Shroff, R.; Long, D.A. Shanahan, C.M. Mechanistic insights into vascular calcification in CKD. J. Am. Soc. Nephrol. 2013, 24, 179–189.
17. Gilbert, S.F. Osteogenesis: The development of bones. In Developmental Biology, 6th ed.; Sinauer Associates: Sunderland, UK, 2000. Available online: http://www.ncbi.nlm.nih.gov/books/NBK10056/(accessed on 12 January 2015).
18. Zhu, D.; Mackenzie, N.C.; Farquharson, C.; Macrae, V.E. Mechanisms and clinical consequences of vascular calcification. Front. Endocrinol. 2012, 3, 95, doi:10.3389/fendo.2012.00095.
19. Moe, S.M. Vascular Calcification: The Three-Hit Model. J. Am. Soc. Nephrol. 2009, 20, 1162–1164.
20. Rule, A.D.; Krambeck, A.E.; Lieske, J.C. Chronic kidney disease in kidney stone formers. Clin. J. Am. Soc. Nephrol. 2011, 6, 2069–2075.
21. Davidovich, E.; Davidovits, M.; Peretz, B.; Shapira, J.; Aframian, D.J. The correlation between dental calculus and disturbed mineral metabolism in paediatric patients with chronic kidney disease. Nephrol. Dial. Transpl. 2009, 24, 2439–2445.
22. Pastor-Ramos, V.; Cuervo-Díaz, A.; Aracil-Kessler, L.; Sialolithiasis. Proposal for a new minimally invasive procedure: Piezoelectric surgery. J. Clin. Exp. Dent. 2014, 6, e295–e298. doi:10.4317/jced.51253.
23. Rzymska-Grala, I.; Stopa, Z.; Grala, B.; Gołębiowski, M.; Wanyura, H.; Zuchowska, A.; Sawicka, M.; Zmorzyński, M. Salivary gland calculi—contemporary methods of imaging. Pol. J. Radiol. 2010, 75, 25–37.
24. Kraai, J.S.; Karagozoglu, K.H.; Forouzanfar, T.; Veerman, E.C.I.; Brand, H.S. Salivary stones: Symptoms, aetiology, biochemical composition and treatment. Br. Dent. J. 2014, 217, E23. doi:10.1038/sj.bdj.2014.1054.
25. Mimura, M.; Tanaka, N.; Ichinose, S.; Kimijima, Y.; Amagasa, T.; Possible etiology of calculi formation in salivary glands: biophysical analysis of calculus. Med. Mol. Morphol. 2005, 38, 189–195.
26. Baurmash, H.D. Submandibular salivary stones: current management modalities. J. Oral Maxillofac. Surg. 2004, 62, 369–378.
27. Fink, H.A.; Wilt, T.J.; Eidman, K.E.; Garimella, P.S.; MacDonald, R.; Rutks, I.R.; Brasure, M.; Kane, R.L.; Monga, M. Recurrent Nephrolithiasis in Adults: Comparative Effectiveness of Preventive Medical Strategies; Executive Summary; Agency for Healthcare Research and Quality; Rockville, MD, USA, July 2012. Available online: http://www.ncbi.nlm.nih.gov/books/NBK99757/(accessed on 24 May 2015).
28. Robertson, W.G.; Potenstial role of fluctuations in the composition of renal tubular fluid through the nephron in the initiation of Randall’s plugs and calcium oxalate crystalluria in a computer model of renal function. Urolithiasis 2015, 43, S93–S107.
29. Verkoelen, C.F. Crystal retention in renal stone disease: A crucial role for the glycosaminoglycan hyaluronan? J. Am. Soc. Nephrol. 2006, 17, 1673–1687.
30. Arcidiacono, T.; Mingione, A.; Macrina, L.; Pivari.; Soldati, L.; Vezzoli, G. Idiopathic Calcium Nephrolithiasis: A Review of Pathogenic Mechanisms in the Light of Genetic Studies. Am. J. Nephrol. 2014, 40, 499–506.
31. Koul, H.K. Koul, S.; Fu, S.; Santosham, V.; Seikhon, A.; Menon, M. Oxalate: from crystal formation to crystal retention. J. Am. Soc. Nephrol. 1999, 10, S417–S421.
32. Benedetto, A.; Accetta, G.; Fujita, Y.; Charras, G. Spatiotemporal control of gene expression using microfluidics. Lab. Chip. 2014, 14, 1336–1347.
33. Wei, Z.; Amponsah, P.K.; Al-Shatti, M.; Nie, Z. Bandyopadhyay, B.C. Engineering of polarized tubular structures in a microfluidic device to study calcium phosphate stone formation. Lab. Chip. 2012, 12, 4037–4040.
34. Evan, A.P. Physiopathology and etiology of stone formation in the kidney and the urinary tract. Pediatr. Nephrol. 2010, 25, 831–841, doi:10.1007/s00467-009-1116-y.
35. Stoller, M.L.; Meng, M.V.; Abrahams, H.M.; Kane, J.P. The primary stone event: a new hypothesis involving a vascular etiology. J. Urol. 2004, 171, 1920–1924.
36. Taylor, E.R.; Stoller, M.L. Vascular theory of the formation of Randall plaques. Urolithiasis 2015, 43, S41–S45. doi:10.1007/s00240-014-0718-4.
37. Bagga, H.S.; Chi, T.; Miller, J.; Stoller, M.L. New Insights Into the Pathogenesis of Renal Calculi. Urol. Clin. North. Am. 2013, 40, 1–12.
38. Fitzpatrick, L.A.; Severson, A.; Edwards, W.D.; Ingram, R.T. Diffuse calcification in human coronary arteries. Association of osteopontin with atherosclerosis. J. Clin. Invest. 1994, 94, 1597–1604.
39. Sangiorgi, G.; Rumberger, J.A.; Severson, A; Edwards, W.D.; Gregoire, J.; Fitzpatrick, L.A.; Schwartz, R.S. Arterial Calcification and Not Lumen Stenosis Is Highly Correlated With Atherosclerotic Plaque Burden in Humans: A Histologic Study of 723 Coronary Artery Segments Using Nondecalcifying Methodology. J. Am. Coll. Cardiol. 1998, 31, 126–133.
40. Blankenhorn, D.H. Coronary Arterial Calcification A Review. Am. J. Med. Sci. 1961, 242, 1–9.
41. Grases, F.; Santiago, C.; Simonet, B.M.; Costa-Bauzá, A. Sialolithiasis: mechanism of calculi formation and etiologic factors. Clin. Chim. Acta. 2003, 334, 131–136.
42. Sabot, J.F.; Gustin, M.P.; Delahougue, K.; Faure, F.; Machon, C.; Hartmann, D.J. Analytical investigation of salivary calculi, by mid-infrared spectroscopy. Analyst. 2012, 137, 2095–2100.
43. Lee, L.T.; Wong, Y.K. Pathogenesis and diverse histologic findings of sialolithiasis in minor salivary glands. J. Oral Maxillofac. Surg. 2010, 68, 465–470.
44. Su, Y.X.; Zhang, K.; Ke, Z.F.; Zheng, G.S.; Chu, M.; Liao, G.Q. Increased calcium and decreased magnesium and citrate concentrations of submandibular/sublingual saliva in sialolithiasis. Arch. Oral Biol. 2010, 55, 15–20.
45. Westhofen, M.; Schäfer, H.; Seifert G. Calcium redistribution, calcification and stone formation in the parotid gland during experimental stimulation and hypercalcaemia. Cytochemical and X-ray microanalytical investigations. Virchows. Arch. A Pathol. Anat. Histopathol. 1984, 402, 425–438.
46. Waseem, Z.; Forte, V. An unusual case of bilateral submandibular sialolithiasis in a young female patient. Int. J. Pediatr. Otorhinolaryngol. 2005, 69, 691–694.
47. 2+ sensing in salivary ductal cells. J. Biol. Chem. 2012, 287, 30305–30316.
48. Proia, A.D.; Brinn, N.T. Identification of calcium oxalate crystals using alizarin red S stain. Arch. Pathol. Lab. Med. 1985, 109, 186–189.
49. Luna, L.G. Gross, M.A. Artifacts simulating calcification associated with improper buffering of formalin fixative. Am. J. Med. Technol. 1965, 31, 412–416.
50. Linnes, M.P.; Krambeck, A.E.; Cornell, L.; Williams, J.C., Jr.; Korinek, M.; Bergstralh, E.J.; Li, X.; Rule, A.D.; McCollough, C.M.; Vrtiska, T.J.; et al. Phenotypic characterization of kidney stone formers by endoscopic and histological quantification of intrarenal calcification. Kidney Int. 2013, 84, 818–825.
51. Frick, K.K, Bushinsky, D.A. Molecular mechanisms of primary hypercalciuria. J. Am. Soc. Nephrol. 2003, 14, 1082–1095.
52. Daudon, M.; Bazin, D.; Letavernier, E. Randall’s plaque as the origin of calcium oxalate kidney stones. Urolithiasis 2015, 43 (Suppl 1), 5–11. doi:10.1007/s00240-014-0703-y.
53. Evan, A.P.; Weinman, E.J.; Wu, X.R.; Lingeman, J.E.; Worcester, E.M.; Coe, F.L. Comparison of the pathology of interstitial plaque in human ICSF stone patients to NHERF-1 and THP-null mice. Urol. Res. 2010, 38, 439–452.
54. Karim, Z.; Gérard, B.; Bakouh, N.; Alili, R.; Leroy, C.; Beck, L.; Silve, C.; Planelles, G.; Urena-Torres, P.; Grandchamp, B. et al. NHERF1 mutations and responsiveness of renal parathyroid hormone. N. Engl. J. Med. 2008, 359, 1128–1135.
55. Levi, M.; Breusegem, S. Renal phosphate-transporter regulatory proteins and nephrolithiasis. N. Engl. J. Med. 2008, 359, 1171–1173.
56. Prié, D.; Ravery, V.; Boccon-Gibod, L.; Friedlander G. Frequency of renal phosphate leak among patients with calcium nephrolithiasis. Kidney Int. 2001, 60, 272–276.
57. Khan, S.R.; Glenton, P.A. Calcium oxalate crystal deposition in kidneys of hypercalciuric mice with disrupted type IIa sodium-phosphate cotransporter. Am. J. Physiol. Renal Physiol. 2008, 294, F1109–1115.
58. Khan, S.R.; Canales, B.K. Ultrastructural Investigation of Crystal deposits in Npt2a knockout mice: Are they similar to Human Randall’s plaques? J. Urol. 2011, 186, 1107–1113.
59. Chau, H.; El-Maadawy, S.; McKee, M.D. Tenenhouse, H.S. Renal calcification in mice homozygous for the disrupted type IIa Na/Pi cotransporter gene Npt2. J. Bone Miner. Res. 2003, 18, 644–657.
60. Prié, D.; Huart, V.; Bakouh, N.; Planelles, G.; Dellis, O.; Gérard, B.; Hulin, P.; Benqué-Blanchet, F.; Silve, C.; Grandchamp, B.; et al. Nephrolithiasis and osteoporosis associated with hypophosphatemia caused by mutations in the type 2a sodium-phosphate cotransporter. N. Engl. J. Med. 2002, 347, 983–991.
61. Gray, R.W.; Wilz, D.R.; Caldas, A.E.; Lemann, J., Jr. The importance of phosphate in regulating plasma 1,25-(OH)2-vitamin D levels in humans: Studies in healthy subjects, in calcium-stone formers and in patients with primary hyperparathyroidism. J. Clin. Endocrinol. Metab. 1977, 45, 299–306.
62. Portale, A.A.; Halloran, B.P.; Morris, R.C.Jr. Physiologic regulation of the serum concentration of 1,25-dihydroxyvitamin D by phosphorus in normal men J. Clin. Invest. 1989, 83, 1494–1499.
63. Lederer, E.; Miyamoto, K. Clinical consequences of mutations in sodium phosphate cotransporters. Clin. J. Am. Soc. Nephrol. 2012, 7, 1179–1187.
64. Williams, C.P.; Child, D.F.; Hudson, P.R.; Soysa, L.D.; Davies, G.K.; Davies, M.G.; de Bolla, A.R. Inappropriate phosphate excretion in idiopathic hypercalciuria: The key to a common cause and future treatment? J. Clin. Pathol. 1996, 49, 881–888.
65. Block, G.A.; Hulbert-Shearon, T.E.; Levin, N.W.; Port, F.K. Association of serum phosphorus and calcium x phosphate product with mortality risk in chronic hemodialysis patients: A national study. Am. J. Kidney Dis. 1998, 31, 607–617.
66. Ganesh, S.K.; Stack, A.G.; Levin, N.W. Hulbert-Shearon, T.; Port, F.K. Association of elevated serum PO4, CaxPO4 product, and parathyroid hormone with cardiac mortality risk in chronic hemodialysis patients. J. Am. Soc. Nephrol. 2001, 12, 2131–2138.
67. Alam, M.U.; Kirton, J.P.; Wilkinson, F.L.; Towers, E.; Sinha, S.; Rouhi, M.; Vizard, T.N.; Sage, A.P.; Martin, D.; Ward, D.T.; et al. Calcification is associated with loss of functional calcium-sensing receptor in vascular smooth muscle cells. Cardiovasc. Res. 2009, 81, 260–268.
68. Shanahan, C.M.; Crouthamel, M.H.; Kapustin, A.; Giachelli, C.M. Arterial calcification in chronic kidney disease: Key roles for calcium and phosphate. Circ. Res. 2011, 109, 697–711.
69. Parks, J.H.; Worcester, E.M.; Coe, F.; Evan, A.P. Lingeman J.E. Clinical implications of abundant calcium phosphate in routinely analyzed kidney stones. Kidney Int. 2004, 66, 777–785.
70. Reynolds, J.L.; Joannides, A.J. Skepper, J.N.; McNair, R.; Schurgers, L.J.; Proudfoot, D.; Jahnen-Dechent, W.; Weissberg, P.L.; Shanahan, C.M. Human vascular smooth muscle cells undergo vesicle-mediated calcification in response to changes in extracellular calcium and phosphate concentrations: A potential mechanism for accelerated vascular calcification in ESRD. J. Am. Soc. Nephrol. 2004, 15, 2857–2867.
71. Cozzolino, M.; Brancaccio, D.; Gallieni, M.; Slatopolsky, E. Pathogenesis of vascular calcification in chronic kidney disease. Kidney Int. 2005, 68, 429–436.
72. Jono, S.; McKee, M.D.; Murry, C.E.; Shioi, A.; Nishizawa, Y.; Mori, K.; Morii, H.; Giachelli, CM. Phosphate regulation of vascular smooth muscle cell calcification. Circ. Res. 2000, 87, E10–E17.
73. Li, X.; Yang, H.Y.; Giachelli, C.M. BMP-2 promotes phosphate uptake, phenotypic modulation, and calcification of human vascular smooth muscle cells. Atherosclerosis 2008, 199, 271–277.
74. Steitz, S.A.; Speer, M.Y.; Curinga, G.; Yang, H.Y.; Haynes, P.; Aebersold, R.; Schinke, T.; Karsenty, G.; Giachelli, C.M. Smooth muscle cell phenotypic transition associated with calcification: upregulation of Cbfα1 and downregulation of smooth muscle lineage markers. Circ. Res. 2001, 89, 1147–1154.
75. −/− mice. Arterioscler. Thromb. Vasc. Biol. 2005, 25, 686–691.
76. Speer, M.Y.; Yang, H.Y; Brabb, T.; Leaf, E.; Look, A.; Lin, W.L.; Frutkin, A.; Dichek, D.; Giachelli, C.M. Smooth muscle cells give rise to osteochondrogenic precursors and chondrocytes in calcifying arteries. Circ. Res. 2009, 104, 733–741.
77. Zavaczki, E.; Jeney, V.; Agarwal, A.; Zarjou, A.; Oros, M.; Katkó, M.; Varga, Z.; Balla, G.; Balla, J. Hydrogen sulfide inhibits the calcification and osteoblastic differentiation of vascular smooth muscle cells. Kidney Int. 2011, 80, 731–739.
78. Zhu, D.; Mackenzie, N.C.; Millán, J.L.; Farquharson, C.; MacRae, V.E. The appearance and modulation of osteocyte marker expression during calcification of vascular smooth muscle cells. PLoS ONE. 2011, 6, e19595.
79. Demer, L.L. Lipid Hypothesis of Cardiovascular Calcification. Circulation. 1997, 95, 297–298.
80. Sarig, S.; Weiss, T.A.; Katz, I.; Kahana, F.; Azoury, R.; Okon, E.; Kruth, H.S. Detection of cholesterol associated with calcium mineral using confocal fluorescence microscopy. Lab. Invest. 1994, 71, 782–787.
81. Kini, U.; Nandeesh, B.N. Physiology of bone formation, remodeling and metabolism. In Radionuclide and Hybrid Bone Imaging; Fogelman, I., Gnanasegaran, G., van der Wall, H., Eds;. Springer-Verlag: Berlin, Germany, 2012; pp. 29–57.
82. Komori, T. Regulation of osteoblast differentiation by Runx2. Adv. Exp. Med. Biol. 2010, 658, 43–49.
83. Dong, S.; Ying, D.; Duan, X.; Zhu, C.; Liu, G.; Mi, J. Effect of core-binding factor α1 on the expression of osteoblast gene marker mesenchymal stem cells. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 2005, 19, 746–750. Available online: http://www.ncbi.nlm.nih.gov/pubmed/16206768 (accessed on 22 May 2015).
84. Nishimura, R.; Hata, K.; Harris, S.E.; Ikeda, F.; Yoneda, T. Core-binding factor α1 (Cbfα1) induces osteoblastic differentiation of C2C12 cells without interactions with Smad1 and Smad5. Bone 2002, 31, 303–312.
85. Kugimiya, F.; Kawaguchi, H.; Kamekura, S.; Chikuda, H.; Ohba, S.; Yano, F.; Ogata, N.; Katagiri, T.; Harada, Y.; Azuma, Y.; et al. Involvement of endogenous bone morphogenetic protein (BMP)2 and BMP6 in bone formation. J. Biol. Chem. 2005, 280, 35704–35712.
86. Tsuji, K.; Bandyopadhyay, A.; Harfe, B.D.; Cox, K.; Kakar, S.; Gerstenfeld, L; Einhorn, T.; Tabin, C.J.; Rosen, V. BMP2 activity, although dispensable for bone formation, is required for the initiation of fracture healing. Nat. Genet. 2006, 38, 1424–1429.
87. Komori, T.; Yagi, H.; Nomura, S.; Yamaguchi, A.; Sasaki, K.; Deguchi, K.; Shimizu, Y.; Bronson, R.T.; Gao, Y.H.; Inada, M.; et al. Targeted disruption of Cbfα1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997, 89, 755–764.
88. Otto, F.; Thornell, A.P.; Crompton, T.; Denzel, A.; Gilmour, K.C.; Rosewell, I.R.; Stamp, G.W.; Beddington, R.S.; Mundlos, S.; Olsen, B.R.; et al. Cbfα1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 1997, 30, 765–771.
89. Phimphilai, M.; Zhao, Z.; Boules, H.; Roca, H.; Franceschi, R.T. BMP signaling is required for RUNX2-dependent induction of the osteoblast phenotype. J. Bone Miner. Res. 2006, 21, 637–646.
90. Lin, G.L.; Hankenson, K.D. Integration of BMP, Wnt, and Notch signaling pathways in osteoblast differentiation. J. Cell. Biochem. 2011, 112, 3491–3501.
91. Bandyopadhyay, A.; Tsuji, K.; Cox, K.; Harfe, B.D.; Rosen, V.; Tabin, C.J. Genetic analysis of the roles of BMP2, BMP4, and BMP7 in limb patterning and skeletogenesis. PLoS Genet. 2006, 2, e216.
92. Rong, S.; Zhao, X.; Jin, X.; Zhang, Z.; Chen, L.; Zhu, Y.; Yuan, W. Vascular calcification in chronic kidney disease is induced by bone morphogenetic protein-2 via a mechanism involving the Wnt/β-catenin pathway. Cell. Physiol. Biochem. 2014, 34, 2049–2060.
93. Cserjesi, P.; Brown, D.; Ligon, K.L.; Lyons, G.E.; Copeland, N.G.; Gilbert, D.J.; Jenkins, N.A.; Olson, E.N. Scleraxis: A basic helix-loop-helix protein that prefigures skeletal formation during mouse embryogenesis. Development 1995, 121, 1099–1110.
94. Sosic, D.; Brand-Saberi, B.; Schmidt, C.; Christ, B.; Olson, E. Regulation of paraxis expression and somite formation by ectoderm-and neural tube-derived signals. Dev. Biol. 1997, 185, 229–243.
95. Oh, C.D. Lu, Y.; Liang, S.; Mori-Akiyama, Y.; Chen, D.; de Crombrugghe, B.; Yasuda, H. SOX9 regulates multiple genes in chondrocytes, including genes encoding ECM proteins, ECM modification enzymes, receptors, and transporters. PLoS ONE 2014, 17, e107577.
96. Lefebvre, V.; de Crombrugghe, B. Toward understanding SOX9 function in chondrocyte differentiation. Matrix Biol. 1998, 16, 529–540.
97. Akiyama, H.; Chaboissier, M.C.; Martin, J.F.; Schedl, A.; De, C.B. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev. 2002, 16, 2813–2828.
98. Briot, A.; Jaroszewicz, A.; Warren, C.M.; Lu, J.; Touma, M.; Rudat, C.; Hofmann, J.J.; Airik, R.; Weinmaster, G.; Lyons, K.; et al. Repression of sox9 by jag1 is continuously required to suppress the default chondrogenic fate of vascular smooth muscle cells. Dev. Cell 2014, 31, 707–721.
99. Khan, S.R. Reactive oxygen species, inflammation and calcium oxalate nephrolithiasis. Transl. Androl. Urol. 2014, 3, 256–276.
100. Gambaro, G.; Abaterusso, C.; Fabris, A.; Ruggera, L.; Zattoni, F.; Del Prete, D.; D’Angelo, A.; Anglani, F. The origin of nephrocalcinosis, Randall’s plaque and renal stones: A cell biology viewpoint. Arch. Ital. Urol. Androl. 2009, 81, 166–170.
101. Grases, F.; Costa-Bauzá, A.; Prieto, R.M.; Conte, A.; Servera, A. Renal papillary calcification and the development of calcium oxalate monohydrate papillary renal calculi: A case series study. BMC Urol. 2013, 13, 14, doi:10.1186/1471-2490-13-14.
102. Grases, F.; Costa-Bauzá, A.; Gomila, I.; Conte, A. Origin and types of calcium oxalate monohydrate papillary renal calculi. Urology 2010, 76, 1339–1345.
103. Grases, F.; Costa–Bauzá, A.; Bonarriba, C.R.; Pieras, E.C.; Fernández, R.A.; Rodríguez, A. On the origin of calcium oxalate monohydrate papillary renal stones. Urolithiasis 2015, 43, S33–S39.
104. Khan, S.; Rodriguez, D.E.; Gower, L.B.; Monga, M. Association of Randall plaque with collagen fibers and membrane vesicles. J. Urol. 2012, 187, 1094–1100.
105. Tiselius, H.G. A hypothesis of calcium stone formation: an interpretation of stone research during the past decades. Urol. Res. 2011, 39, 231–243.
106. Shavit, L.; Girfoglio, D.; Vijay, V.; Goldsmith, D.; Ferraro, P.M.; Moochhala, S.H.; Unwin, R. Vascular calcification and bone mineral density in recurrent kidney stone formers. Clin. J. Am. Soc. Nephrol. 2015, 10, 278–285.
107. Lauderdale, D.S.; Thisted, R.A.; Wen, M.; Favus, M.J. Bone mineral density and fracture among prevalent kidney stone cases in the Third National Health and Nutrition Examination Survey. J. Bone Miner. Res. 2001, 16, 1893–1898.
108. Bataille, P.; Achard, J.M.; Fournier, A.; Boudailliez, B.; Westeel, P.F.; el Esper, N.; Bergot, C.; Jans, I.; Lalau, J.D.; Petit, J.; et al. Diet, vitamin D and vertebral mineral density in hypercalciuric calcium stone formers. Kidney Int. 1991, 39, 1193–1205.
109. Pietschmann, F.; Breslau, N.A.; Pak, C.Y. Reduced vertebral bone density in hypercalciuric nephrolithiasis. J. Bone Miner. Res. 1992, 7, 1383–1388.
110. Jaeger, P.; Lippuner, K.; Casez, J.P.; Hess, B.; Ackermann, D.; Hug, C. Low bone mass in idiopathic renal stone formers: magnitude and significance. J. Bone Miner. Res. 1994, 9, 1525–1532.
111. Asplin, J.R.; Bauer, K.A.; Kinder, J.; Müller, G.; Coe, B.J.; Parks, J.H.; Coe, F.L. Bone mineral density and urine calcium excretion among subjects with and without nephrolithiasis. Kidney Int. 2003, 63, 662–669.
112. Sella, S.; Cattelan C, Realdi G, Giannini S. Bone disease in primary hypercalciuria. Clin. Cases Miner. Bone Metab. 2008, 5,118–126.
113. Arrabal-Polo, M.A.; Del, C.C.M.; Canales, B.K.; Arrabal-Martín, M. Calcium nephrolithiasis and bone demineralization: pathophysiology, diagnosis, and medical management. Curr. Opin. Urol. 2014, 24, 633–638.
114. Gambaro, G.; Ferraro, P.M.; Capasso, G. Calcium nephrolithiasis, metabolic syndrome and the cardiovascular risk. Nephrol. Dial. Transplant. 2012, 27, 3008–3010.
115. Gambaro, G.; Fabris, A.; Abaterusso, C.; Cosaro, A.; Ceol, M.; Mezzabotta, F.; Torregrossa, R.; Tiralongo, E.; del Prete, D.; D’Angelo, A.; et al. Pathogenesis of nephrolithiasis: recent insight from cell biology and renal pathology. Clin. Cases Miner. Bone Metab. 2008, 5, 107–109.
116. Jia, Z.; Wang, S.; Tang, J.; He, D.; Cui, L.; Liu, Z.; Guo, B.; Huang, L.; Lu, Y.; Hu, H. Does crystal deposition in genetic hypercalciuric rat kidney tissue share similarities with bone formation? Urology 2014, 83, e7–e14.
117. He, D.; Wang, S.; Jia, Z.; Cui, L.; Lu, Y.; Hu, H.; Qin, B. Calcium ions promote primary renal epithelial cell differentiation into cells with bone-associated phenotypes via transforming growth factor-β1-induced epithelial-mesenchymal transition in idiopathic hypercalciuria patients. Mol. Med. Rep. 2015, 11, 2199–2206.
118. Salama, R.H.; Alghasham, A.; Mostafa, MS.; El-Moniem, A.E. Bone morphogenetic protein-2 will be a novel biochemical marker in urinary tract infections and stone formation. Clin. Biochem. 2012, 45, 766–769.
119. Shao, J.S.; Cheng, S.L.; Sadhu, J.; Towler, D.A.; Inflammation and the osteogenic regulation of vascular calcification: A review and perspective. Hypertension 2010, 55, 579–592.
120. Duer, M.J.; Friscić, T.; Proudfoot, D.; Reid, D.G.; Schoppet, M.; Shanahan, C.M.; Skepper, J.N.; Wise, E.R. Mineral surface in calcified plaque is like that of bone: further evidence for regulated mineralization. Arterioscler. Thromb. Vasc. Biol. 2008, 28, 2030–2034.
121. Demer, L.L.; Tintut, Y. Vascular calcification: pathobiology of a multifaceted disease. Circulation 2008, 117, 2938–2948.
122. Sun, Y.; Byon, C.H.; Yuan, K.; Chen, J.; Mao, X.; Heath, J.M.; Javed, A.; Zhang, K.; Anderson, P.G.; Chen, Y. Smooth muscle cell-specific runx2 deficiency inhibits vascular calcification. Circ. Res. 2012, 111, 543–552.
123. Chen, N.X.; Moe, S.M. Vascular calcification: Pathophysiology and risk factors. Curr. Hypertens. Rep. 2012, 14, 228–237.
124. Fantus, D.; Awan, Z.; Seidah, N.G.; Genest, J. Aortic calcification: Novel insights from familial hypercholesterolemia and potential role for the low-density lipoprotein receptor. Atherosclerosis 2013, 226, 9–15.
125. −/− mice. Arterioscler. Thromb. Vasc. Biol. 2007, 27, 2589–2596.
126. New, S.E.; Aikawa, E. Molecular imaging insights into early inflammatory stages of arterial and aortic valve calcification. Circ. Res. 2011, 108, 1381–1391.
127. Kapustin, A.N.; Davies, J.D.; Reynolds, J.L.; McNair, R.; Jones, G.T.; Sidibe, A.; Schurgers, L.J.; Skepper, J.N.; Proudfoot, D.; Mayr, M.; et al. Calcium regulates key components of vascular smooth muscle cell-derived matrix vesicles to enhance mineralization. Circ. Res. 2011, 109, e1–e12.
128. Shroff, R.C.; McNair, R.; Skepper, J.N.; Figg, N.; Schurgers, L.J.; Deanfield, J.; Rees, L.; Shanahan, C.M. Chronic mineral dysregulation promotes vascular smooth muscle cell adaptation and extracellular matrix calcification. J. Am. Soc. Nephrol. 2010, 21, 103–112.
129. Lieske, J.C.; Norris, R.; Toback, F.G.; Adhesion of hydroxyapatite crystals to anionic sites on the surface of renal epithelial cells. Am. J. Physiol. 1997, 273, F224–F233.
130. Moe, S.M.; Chen, N.X. Vascular calcification in end stage renal disease. Clin. Calcium. 2002, 12, 1417–1422.
131. Czarny, M.J.; Resar, J.R. Diagnosis and management of valvular aortic stenosis. Clin. Med. Insights Cardiol. 2014, 8, S15–S24.
132. Aksoy, O.; Cam, A.; Agarwal, S.; Ige, M.; Yousefzai, R.; Singh, D.; Griffin, B.P.; Schoenhagen, P.; Kapadia, S.R.; Tuzcu, M.E. Significance of aortic valve calcification in patients with low-gradient low-flow aortic stenosis. Clin. Cardiol. 2014, 37, 26–31.
133. Goodman, W.G. Vascular calcification in end-stage renal disease. J. Nephrol. 2002, 15, S82–S85.
134. Wang, A.Y.; Ho, S.S.; Wang, M.; Liu, E.K.; Ho, S.; Li, P.K.; Lui, S.F.; Sanderson, J.E. Cardiac valvular calcification as a marker of atherosclerosis and arterial calcification in end-stage renal disease. Arch. Intern. Med. 2005, 165, 327–332.
135. Ferranti, C.; Coopmans, D.Y.G.; Biganzoli, E.; Bergonzi, S.; Mariani, L.; Scaperrotta, G.; Marchesini, M. Relationships between age, mammographic features and pathological tumour characteristics in non-palpable breast cancer. Br. J. Radiol. 2000, 73, 698–705.
136. Cox, R.F.; Hernandez-Santana, A.; Ramdass, S.; McMahon, G.; Harmey, J.H.; Morgan, M.P. Microcalcifications in breast cancer: Novel insights into the molecular mechanism and functional consequence of mammary mineralisation. Br. J. Cancer 2012, 106, 525–537.
137. Morgan, M.P.; Cooke, M.M.; McCarthy, G.M. Microcalcifications associated with breast cancer: An epiphenomenon or biologically significant feature of selected tumors? J. Mammary Gland Biol. Neoplasia 2005, 10, 181–187.
138. Haka, A.S.; Shafer-Peltier, K.E.; Fitzmaurice, M.; Crowe, J.; Dasari, R.R.; Feld, M.S. Identifying microcalcifications in benign and malignant breast lesions by probing differences in their chemical composition using Raman spectroscopy. Cancer Res. 2002, 62, 5375–5380.
139. Baker, R.; Rogers, K.D.; Shepherd, N.; Stone, N. New relationships between breast microcalcifications and cancer. Br. J. Cancer 2010, 103, 1034–1039.
140. Morgan, M.P.; Cooke, M.M.; Christopherson, P.A.; Westfall, P.R.; McCarthy, G.M. Calcium hydroxyapatite promotes mitogenesis and matrix metalloproteinase expression in human breast cancer cell lines. Mol. Carcinog. 2001, 32, 111–117.
141. Liu, F.; Bloch, N.; Bhushan, K.R.; De Grand, A.M.; Tanaka, E.; Solazzo, S.; Mertyna, P.M.; Goldberg, N.; Frangioni, J.V.; Lenkinski, R.E. Humoral bone morphogenetic protein 2 is sufficient for inducing breast cancer microcalcification. Mol. Imaging 2008, 7, 175–186.
142. Shobeiri, N.; Adams, M.A.; Holden, R.M. Phosphate: An old bone molecule but new cardiovascular risk factor. Br. J. Clin. Pharmacol. 2014, 77, 39–54.
143. Cox, R.F.; Jenkinson, A.; Pohl, K.; O’Brien, F.J.; Morgan, M.P. Osteomimicry of Mammary Adenocarcinoma Cells in Vitro; Increased Expression of Bone Matrix Proteins and Proliferation within a 3D Collagen Environment. PLoS ONE 2012, 7, e41679. doi:10.1371/journal.pone.0041679.
144. Chen, N.X.; O’Neill, K.D.; Duan, D.; Moe, S.M. Phosphorus and uremic serum up-regulate osteopontin expression in vascular smooth muscle cells. Kidney Int. 2002, 62, 1724–1731.
145. Bellahcène, A.; Merville, M.P.; Castronovo, V. Expression of bone sialoprotein, a bone matrix protein, in human breast cancer. Cancer Res. 1994, 54, 2823–2826.
146. Bellahcène, A.; Castronovo, V. Increased expression of osteonectin and osteopontin, two bone matrix proteins, in human breast cancer. Am. J. Pathol. 1995, 146, 95–100.
147. Scimeca, M.; Giannini, E.; Antonacci, C.; Pistolese, C.A.; Spagnoli, L.G.; Bonanno, E. Microcalcifications in breast cancer: an active phenomenon mediated by epithelial cells with mesenchymal characteristics. BMC Cancer. 2014, 14, 286, doi:10.1186/1471-2407-14-286.
148. Koori, K.; Maeda, H.; Fujii, S.; Tomokiyo, A.; Kawachi, G.; Hasegawa, D.; Hamano, S.; Sugii, H.; Wada, N.; Akamine, A. The roles of calcium-sensing receptor and calcium channel in osteogenic differentiation of undifferentiated periodontal ligament cells. Cell. Tissue Res. 2014, 357, 707–718.
149. 2+]i in rat distal pulmonary arterial smooth muscle cells. Am. J. Physiol. Cell. Physiol. 2013, 304, C833–C843.
150. Cross, B.M.; Breitwieser, G.E.; Reinhardt, T.A.; Rao, R. Cellular calcium dynamics in lactation and breast cancer: from physiology to pathology. Am. J. Physiol. Cell. Physiol. 2014, 306, C515–C526, doi:10.1152/ajpcell.00330.2013.
151. Pampena, D.A.; Robertson, K.A.; Litvinova, O.; Lajoie, G.; Goldberg, H.; Hunter, G.K. Inhibition of hydroxyapatite formation by osteopontin phosphopeptides. Biochem. J. 2004, 378, 1083–1087.
152. Matsuzaki, H.; Katsumata, S.; Uehara, M.; Suzuki, K.; Miwa, M. High-phosphorus diet induces osteopontin expression of renal tubules in rats. J. Clin. Biochem. Nutr. 2007, 41, 179–183.